Maataloustieteellinen Aikakauskirja
Journal of Agricultural Science in Finland
Vol. 57: 1—66, 1985

Host-pathogen interaction between spring wheat and
Septoria nodorum with reference
to resistance breeding

Selostus: Kevätvehnän Septoria nodorum -resistenssi
taudinkestävyysjalostuksen näkökulmasta

REIJO KARJALAINEN

Departments of Plant Pathology
and Plant Breeding
University of Helsinki
SF-00710 Helsinki 71, Finland

SUOMEN MAATALOUSTIETEELLINEN SEURA, HELSINKI

https://www.c-info.fi/en/info/?token=arPjuP7RUwTsbakK.X4pgWXLJIRSItSHJuNT2mg.P8xm9ZgOkZqdW91_bPAmOKReHdGbwhaRdbW9M6Qdg3pwP9G-nmWiknHFbKnc-h1aPFwMj5sjpp2Y4rTA0uCxGzaXyDt0rw4YBF64CM87lEr14FwktslmQkv3X8zjK1DvRFD284Mxf3VZ9FGbv1e2S4wM7ifejt41jBHEac_U-A




yja ffini/c/cu





5

Preface

The present investigations were carried out at the Departments of Plant
Pathology and Plant Breeding, University of Helsinki. Part of the first
field trials were carried out at the Hankkija Plant Breeding Institute, Hy-
rylä. Electron microscopic work was performed at the Department of
Electron Microscopy, University of Helsinki.

I wish to express my deep gratitude to Professors Eeva Tapio and Peter
Tigerstedt for their support and encouragement during the progress of this
work.

I am grateful to Professors Eeva Tapio, Erkki Kivi, and Peter Tiger-
stedt, and Docent Kari Lounatmaa for constructive criticism and com-
ments of the manuscript.

I am pleased to extend my best thanks to Drs Peter R. Scott and Petur
Benedikz, Plant Breeding Institute, Cambridge, England, and Mr. Jan
Jönsson, M. Sci., Weibullsholm Plant Breeding Institute, Sweden, for
valuable advice and discussions of problems related to wheat breeding for
Septoria resistance.

1 am grateful to my fellow co-workers and colleagues Docent Kari Lou-
natmaa, Ms Aino Laitinen, M. Sei., and Mr Tapio Juuti, M. Sei., for dis-
cussions and interest during this investigation.

I also wish to thank Ms Eila Lonka, Kirsti Nieminen, Pirkko Korho-
nen, Terttu Parkkali, and Heather MacKenzie, and Mr Jouko Närhi for
technical assistance. I am grateful to Mr Simo Lehtinen, M. Sei., and Ilkka
Reima, M. Sei., for technical advice while I was using electron microscopy,
and to Ms Karita Ahlqvist and Arja Rantanen for skilful technical assist-
ance.

My warm thanks are due to Mr Robert Harper and Ms Sinikka Karjalai-
nen, M. Sei., for the linguistic revision of the English text.

Financial support has been given by the Finnish Academy of Sciences,
and grants by the August Johannes and Aino Tiura Agricultural Research
Foundation and the Finnish Cultural Foundation.

I am grateful to the Scientific Agricultural Society of Finland for in-
cluding this study in their series of publications.

Finally I wish to express my sincere thanks to my wife Sinikka for her
help and patience during my work.

Helsinki, April 1985 Reijo Karjalainen





JOURNAL OF AGRICULTURAL SCIENCE IN FINLAND
Maataloustieteellinen Aikakauskirja

Vol. 57: 1—66. 1985

Host-pathogen interaction between spring wheat and Septoria nodorum
with reference to resistance breeding

Abstract. Host-pathogen interaction between spring wheat and Seploria nodorum Berk,

with applications for wheat breeding were studied.
Ultrastructure of interactions was studied using electron microscopic techniques. Fol-

lowing inoculation, conidia of S. nodorum germinate, form appressoria and a penetration peg
which directly penetrates through the cell walls. It is suggested that most penetration attempts
fail because of cellular defence reactions, formation of papillae and cell wall alterations.

Inoculation with low spore concentration reduced grain yield of Flankkija’s Taava
cultivar by 10 % and 1000-grain weight by 14 %. Inoculation with high spore concentration
on large plots of Tähti cultivar reduced grain yield by 32 % and 1000-grain weight by 18 %.

Inoculation with high spore concentration on normal breeding plots of Tähti cultivar reduced
grain yield by 35 % and 1000-grain weight by 21 % and the grain yield of Kadett cultivar by
27 % and 1000-grain weight by 20 %.

Inheritance studies on F 2 progenies of spring wheat crosses involving susceptible and
moderately or highly resistant parents suggest that heredity component of symptom express-
ion is moderate level and breeding success depends mainly on efficient screening techniques.
Resistance was associated with tallness in crosses, and cultivar trials suggest that resistance
is positively associated with late maturation time.

Field screening techniques based on small plots and artificial inoculation showed that the
most resistant entries were wild Trilicum species and late and tall cultivars. Seedlingplant tests
based on attached seedling leaves and detached leaves revealed easily the most resistant and
most susceptible cultivars. The overall correlation between seedling tests and field tests was
quite high.

The results are discussed in relation to wheat breeding strategies for resistance to S. nodo-
rum.

Index words: Wheat, Seploria nodorum, resistance breeding

7





9

CONTENTS

Abstract 7

1. INTRODUCTION 11

2. LITERATURE REVIEW ON CURRENT IDEAS OF HOST-PATHOGEN IN-
TERACTIONS 13
2.1. Genetic aspects of host-pathogen interactions 13
2.2. Determinants of pathogenicity and virulence 13
2.3. Molecular aspects of interactions 14
2.4. Effects of resistance on disease development 15

3. SEPTORIA NODORUM ON WHEAT: A POLYGENIC HOST-PATHOGEN
SYSTEM 18

3.1. Description, host range and distribution of the disease 18
3.2. Epidemiology 20

3.2.1. Primary sources of infection 20
3.2.2. Factors affecting infection and symptom expression 20

3.3. Control measures 21

4. THE AIM OF THE PRESENT EXPERIMENTAL STUDY 23

5. MATERIALS AND METHODS 25

6. RESULTS AND DISCUSSION 28
6.1. Host-pathogen interaction at the cellular level 28

6.1.1. Ultrastructural aspects of Septoria nodorum 28
6.1.2. Penetration 30
6.1.3. Nature of cellular resistance reactions 33
6.1.4. Pathological alterations in host ultrastructure 35

6.2. Effects of S. nodorum on wheat yield and yield components 35
6.3. Genetic nature of resistance 39

6.3.1. Inheritance of resistance 39
6.3.2. Association of resistance with agronomic traits 41

6.4. Assessment of disease resistance 44
6.4.1. Detection of resistance at the adult plant stage under field conditions 44



10

6.4.2. Detection of resistance at the seedling plant stage under glasshouse
conditions 47

7. GENERAL DISCUSSION PERSPECTIVES FOR FUTURE WHEAT BREED-
ING FOR DISEASE RESISTANCE 52

REFERENCES 56

SELOSTUS 66



1. Introduction

Current emphasis in agricultural research
is to devote more efforts on finding methods
to reduce production costs and the risk of en-
vironmental pollution. Genetic plant protec-
tion is cheaper for the grower than other
forms of protection (Pesola 1930, Riley

1979), and it offers the ideal method to con-
trol plant diseases biologically (Hagedorn
1983). Plant breeding through the develop-
ment of resistant cultivars has made remark-
able contribution to controlling many im-
portant pests and diseases (Hagberg and
Gustafsson 1981, Lupton 1984). For ex-
ample, Hagedorn (1983) states that over ten
years ago it was estimated that more than
75 % of the crop acreage in the United States
was being planted with disease-resistant cul-
tivars, with an annual value to growers of
over a billion dollars. In addition, Doodson
(1981) showed the significant economic bene-
fits of growing winter wheat cultivars resis-
tant to leaf diseases over a ten year period in
England and Wales.

The roots of resistance breeding date back
to the history of human cultural evolution,
but the rediscovery of Mendel’s work was
the turning point for scientific resistance
breeding. Biffen (1905) found that the re-
sistance of wheat progenies to yellow rust
followed Mendel’s laws, and he suggested
that cultivar resistance could be improved
through selection. Scientific progress in re-
sistance breeding over the past 80 years has
not been a steady process but one where
great momentary advances and long steady
periods alternate, a phenomenon well known
in many areas of science (Kuhn 1962).

The first era of resistance breeding was
based almost totally on easily detectable types
of resistance conferred by a few major genes.
However, it soon appeared that resistance
breeding was not always successful. The ex-
planation for this was provided by Barrus
in 1911 (ref. Ellingboe 1981) who reported
that two isolates of Colletotrichum linde-
muthianum possessed differential pathoge-
nicity on bean cultivars. This was the be-
ginning of the era of physiological specializ-
ation studies, and many methods developed
for race surveys at that time are still used
today.

The next peak in the ideology of resistance
breeding was in 1946—1947 when Flor in-
troduced his gene-for-gene theory. This was
a turning point in the history of plant pathol-
ogy, and the theory is still one of the most
important discoveries in this field (Ellingboe
1981, Vanderplank 1982). Subsequent de-
velopment based on analysis of several host-
pathogen systems, and in many cases it was
found difficult to detect a gene-for-gene pat-
tern. Vanderplank (1963, 1968) made a
substantial contribution to the development
of new ideas and lead the way to more theory-
orientated analyses of host-pathogen inter-
actions. He introduced the terms vertical and
horizontal resistance, the former being race-
specific and liable to breakdown by new
virulent strains, the latter race-non-specific,
stable and controlled by many minor genes.
However, later studies (e.g. Nelson 1978,
Parlevliet 1979, Ellingboe 1981) have chal-
lenged many of Vanderplank’s hypotheses
and shown that in many cases the definitions

11



vertical and horizontal are far too simple to
explain the genetic basis of durability of cul-
tivar resistance.

In the 19705, resistance research has ad-
vanced in two main areas. The application
of population genetics to epidemiology has
given new ideas about the dynamics of path-
ogen populations, for example, about viru-
lence genes and selection pressures caused
by resistant cultivars (Person et al. 1976,
Leonard 1977, Wolfe and Barrett 1977,
Zadoks and Schein 1979). Over the last ten
years great efforts have been made to reveal
the biochemical and molecular basis of re-
sistance and to shed light on the crucial prob-
lems of recognition in host-pathogen interac-
tions (Friend and Threlfall 1976, Daly

and Uritani 1979).
Currently, some of the greatest expecta-

tions are focused on the applications of re-
combinant DNA techniques for resistance
breeding (Ellingboe 1981, Foard et al. 1983,
Comai and Stalker 1984). Genetic engineer-
ing can substantially speed up selection (Day
1984 b). For example, cDNA probes can now

be routinely used in virus resistance screening
(Flavell et al. 1983, Baulcombe et al.
1984). Further, better understanding of path-

ogenicity and virulence can give new tools
for resistance breeding.

Another area of much interest is the identi-
fication of primary gene products of single
resistance genes (Foard et al. 1983, Kuhn et
al. 1984) because the availability of purified
DNA sequences is required for utilizing novel
ways of introducing genes into plants by
genetic engineering. It is probable that within
the next five years genes coding for some
single gene resistance could be transferred
into agronomically accepted crop cultivars
using vectors such as Ti plasmid or trans-
posons.

Research on cereal disease resistance in
Finland has a long but discontinuous tradi-
tion. For example, Pesola (1927) made an
extensive study on yellow rust resistance of
spring wheat and Kivi (1956) on stem rust of
spring wheat. Since those days breeding ef-
forts have been concentrated on improving
the level of powdery mildew resistance (Nis-
sinen 1973). Furthermore, the breeding for
resistance in winter cereals to fungi causing
winter damage has long been an important
research aim (e.g. Pohjanheimo 1962, Jama-
lainen 1969).

12



2. Literature review on current ideas of host-pathogen interactions

2.1. Genetic aspects of host-pathogen
interactions

Resistance to many plant diseases is mono-
genically inherited (Russell 1978, Leonard
1984). The difference between resistance and
susceptibility in segregation populations is
clear-cut, and if resistance is dominant, it is
easy to use in plant breeding (Russell 1978).
However, host reaction to the disease can be
more complicated. There is evidence of host
resistance controlled by a few oligogenes and
even polygenes (Day 1974), and if each of
these genes has a small effect, the expression
of resistance is continuous in segregation
populations and its detection is difficult in
plant breeding (Russell 1978).

When studying the inheritance of resistance
in flax and the pathogen virulence of its
obligatory parasite, Melampsora I ini, Flor
(1946, 1947) found that for each gene con-
ditioning resistance in the host there was a
specific matching gene conditioning virulence
in the pathogen. Thus a resistant (incom-
patible) reaction occurs when the host has a
dominant gene for resistance that is not
matched by a corresponding gene for viru-
lence in the pathogen (Table 1). This gene-
for-gene hypothesis suggests (Person and
Mayo 1974, Ellingboe 1982) that the allele
for avirulence in the parasite and the cor-
responding allele for resistance in the host
play a key role in determining the reaction
that will be incompatible.

It has been suggested (Sidhu 1975) that the
gene-for-gene pattern applies to a wide range
of host-parasite interactions and Ellingboe

Table 1. Patterns of a gene-for-gene interaction. R and
r denote host genes which segregate for resis-
tance (dominant) and susceptibility (recessive)
in F, populations that have been inoculated
with a parasitic strain of genotype AA or Aa.
A and a denote genes, which in F 2 popula-
tions of the parasite inoculated to the RR or
Rr host, segregate for avirulence (dominant)
and virulence (recessive). When dominant
gene for resistance (R) interacts with domi-
nant gene for avirulence (A), it generates the
incompatible reaction ( —), while compatible
reaction (+) indicates host susceptibility and
parasite virulence. (Adapted from Person
and Mayo 1974).

Complete pattern

Genotype: RR Rr rr Simplified pattern

AA + Genotype: R— rr

Aa + A— +

aa + + + aa + +

(1981, 1982) has stated that about 95 % ofall
analyzed disease resistance follows this pat-
tern. However, Day et al. (1983) argue on
several grounds that in a sense gene-for-gene
systems are the tops of icebergs. Further,
Johnson (1983, 1984) gives several examples
of host-parasite interactions where signifi-
cant interaction between parasite genes and
host genotype genes does not exist.

2.2. Determinants of pathogenicity
and virulence

Plant disease is the outcome of interactions
between the plant, pathogen and the environ-

13



ment (Kosuge et al. 1983). The precise mech-
anisms by which a pathogen causes disease
in plants are poorly understood (Kado and
Lurquin 1982, Daniels 1984). Disease re-
sponse is related to pathogen pathogenicity,
a qualitative term which defines the ability of
an organism to cause a disease on its host,
and virulence, a quantitative term which
defines the severity of disease caused by the
pathogen (Kosuge et al. 1983).

Classical genetics has shown (Day 1974)
that there can be single, few or many genes
coding for pathogenicity or virulence in the
pathogen. Hitherto, very little is known
about the primary products of such genes
because the genetics of many pathogens is
poorly known (Day 1984 a). However, it is
known (Kado and Lurquin 1982) that the
genes of the pathogen code for products
which in turn directly or indirectly cause the
disease response in the plant. Thus it appears
that increasing attention should be paid to
revealing the nature of pathogen and on
trying to determine its inherent weakness
(Kado and Lurquin 1982). It is apparent
that the genes for virulence are there for the
pathogen to grow and colonize the host while
the genes for pathogenicity code for products
that alter cell function (Kado and Lurquin
1982).

There are many pathogenicity and viru-
lence determinants such as toxins, cell wall
degrading enzymes, and polysaccharides
demonstrated to be involved in disease re-
sponse (Cooper 1983), but their precise role
in disease mechanisms is poorly understood.
The application of recombinant DNA tech-
niques to pathogenicity studies (Comai and
Kosuge 1982) has recently made it possible
to achieve considerable progress in revealing
the nature of pathogenicity and virulence.
Recently, some workers have been able to
isolate and clone genes coding for pathoge-
nicity and virulence in bacteria, Erwinia sp.
(Keen et al. 1984), Pseudomonas sp. (Comai
and Kosuge 1982, Staskawicz et al. 1984),
and Xanthomonas sp. (Daniels et al. 1984).
Furthermore, Yoder (1983) has been able to

construct a gene vector amenable to patho-
genic fungi for the cloning of genes coding
for toxin production, and Soliday et al.
(1984) were able to clone and sequence the
gene coding for cutinase, an enzyme involved
in the fungal penetration of plants. Thus,
recombinant DNA techniques have already
proved to be a powerful tool in pointing the
way to a better understanding of the nature
of plant pathogens. It is evident that the
precise understanding of gene functions in
virulence and pathogenicity will open new
ideas for disease control.

2.3. Molecular aspects of interactions

Several models have been proposed to ex-
plain molecular mechanisms in gene-for-gene
host-parasite systems (Day 1974, Albersheim
and Anderson-Prouty 1975, Chakravorty

and Shaw 1977, Ellingboe 1982), but no
testable models have yet been published. It is
assumed (Keen 1982, Callow 1984) that the
high degree of specificity exhibited by gene-
for-gene systems suggests highly selective
host receptors capable of detecting specific
features of parasite races. The hypothesis
now widely accepted (Keen 1982) is based
on the idea that genetically determined early
recognition phase appears before the invoca-
tion of the biochemical and histological
events that stop the colonization of the path-
ogen. Keen (1982) has recently introduced
the elicitor-receptor model to explain the
molecular control of gene-for-gene interac-
tions. The driving force in this model is the
presence in plant cells of specific surface
receptors, probably proteins or glycoproteins,
that recognize the surface molecules of in-
compatible but not compatible pathogen
races. Consequently, incompatible races in-
itiate active defence, particularly phytoalexin
accumulation, which inhibits the growth of
the pathogen (Keen 1982). Evidence to sup-
port this model is at the moment limited.
There are extensive data of elicitors isolated

14



from fungal cell walls (West 1981, Keen et
al. 1983, Darvill and Albersheim 1984) as
well as from plant cell walls (Davis et al.
1984) which can induce phytoalexin accumu-
lation. However, there is only one report of
a receptor on plant membrane for a fungal
elicitor (Yoshikawa et al. 1983).

Recently, Bell et al. (1984) provided mol-
ecular evidence that the induction of mRNA
activities encoding enzymes of phytoalexin
biosynthesis is a key component in the regula-
tion of phytoalexin accumulation in rela-
tion to hypersensitive resistance in an in-
compatible interaction. Further, they sug-
gest that the induction of chalcone synthase
mRNA activity at the early stages of incom-
patible interactions represents an early bio-
chemical event in a causally related sequence
leading from genetically specified recognition
in an intact host-pathogen system to oper-
ation of a defined well-characterized defence
response. Application of recombinant DNA
techniques to Pseudomonas syringae pv. gly-
cinea-soybean systems, Staskawicz et al.
(1984) were able to identify the gene respon-
sible for race-specificity, and they also pro-
vided evidence that incompatible races play
an active role in defence in gene-for-gene
systems.

However, recent progress has shed only
some light on the understanding of the mol-
ecular basis of disease resistance in detail.
Day (1984 a) has suggested that the progress
in revealing the mechanisms of resistance
and specificity has been slow in gene-for-
gene systems principally because the mech-
anism of specificity determination is a great
deal more complex than the genetic control
implies. In addition, Daly (1984) states that
the basic problem with current genetic and
recognition models is that they are static with-
out the known plasticity of natural disease
reaction. The present models of molecular
control of resistance seem to be valid to a
limited extent in only some gene-for-gene
systems, and they probably throw very little
light on host-pathogen systems which are
controlled by more complex genetic systems.

2.4. Effects of resistance on disease
development

In the course of evolution, crop plants
have developed diverse defence mechanisms
to limit the damage caused by numerous mi-
cro-organisms. Defence mechanisms can be
broadly classified into three groups: disease
escape, resistance, and tolerance (Russell
1978, Parlevliet 1981). Escape mechanisms
include various forms such as morphological
traits and different timing of flowering
(Agrios 1980), which operate before the con-
tact between host and pathogen is established.
Tolerance means that plants are diseased but
they suffer only little damage. Resistance to
pathogens involves diverse physiological,
histological, and biochemical mechanisms
which can be effective before the physical
contact between host and pathogen or in-
duced after parasitic attack (Russell 1978).
Respiration studies (Smedegärd-Petersen
and Stolen 1980, Uritani and Asahi 1980,
Kosuge and Kimpel 1981) suggest that the
expression of active defence mechanisms is an
energy-requiring biosynthetic process, which
is likely to deprive host energy. This sugges-
tion has recently been confirmed by yield ex-
periments (Smedegärd-Petersen 1982) which
show a yield reduction in barley after inocula-
tion with avirulent fungi and by bioenergetic
calculations made by Mitra and Bhatia
(1982).

Vanderplank (1963, 1968) divided resis-
tance to plant pathogens into two types, hori-
zontal and vertical. According to his defini-
tion, resistance is horizontal if its variation
is independent of pathogen variation, and
vertical if variation in the pathogen is quali-
tatively associated with the variation in the
host. The effect of different types of resis-
tance on disease development according to
Vanderplank (1968) is presented in Fig. 1.
The magnitude of host resistance on patho-
gen development can range from very small
to very large (Fry 1982). Monogenic resis-
tance, hypersensitive type, often gives com-
plete protection against specific races of the

15



pathogen, while quantitative resistance (terms
horizontal and partial are also used) is char-
acterized by a reduced rate of epidemic devel-
opment resulting from factors that reduce
infection efficiency, extend the latent per-
iod, and reduce sporulation (Umaerus 1970,
Zadoks 1971, Parlevliet 1979, Kranz
1983). Thus it is obvious that the detection of
quantitative resistance is difficult mainly be-
cause it is easily masked by environmental
factors and the effect of growth stage of the
plant (Parlevliet 1979). In addition, it is
difficult to accurately assess the practical val-
ue of quantitative resistance in crop produc-
tion (Leonard and Mundt 1984).

The widescale use of monogenic resistance,
following the gene-for-gene pattern, in a crop
imposes extreme selection pressure on the
pathogen population that can lead to a rapid
build-up of pathogen races with genes for
virulence that match the resistance genes
used in the cultivars (Vanderplank 1968,
Leonard 1977, 1984). The recent history
concerning breakdown of host resistance
based on single major genes is well docu-
mented as far as the biotrophic pathogens,
for example stem rust of wheat and powdery
mildew of barley, are concerned (Wolfe and
SCHWARZBACH 1978, JORGENSEN 1983, LeO-

nard 1984). Particularly after Vanderplank

(1963, 1968) had introduced his ideas of
horizontal resistance and its better durability
over vertical resistance, breeders widely began
to incorporate quantitative resistance into
breeding lines. For a long time it was assumed
(Vanderplank 1963, Nelson 1978) that it
is very difficult for pathogens to adapt to
polygenic resistance. However, the better
durability of horizontal resistance has been
questioned in later studies (Caten 1974,
Parlevliet 1981, Hwang and Heitefuss
1982) which indicate that significant host-
cultivar and pathogen-isolate interactions
have been found. Further, there are a number
of cases of host resistance based on single
major genes which have given relatively long
lasting disease protection (Russell 1978, Fry

1982, Johnson 1983, Parlevliet 1983). Con-
sequently, it is frequently proposed (Hab-
good and Clifford 1981, Parlevliet 1981,
1983) that single genes can give long lasting

protection against many necrotrophic and
soil-borne fungi and some viruses, while the
protection is likely to be short-lived against
biotrophic fungi. However, the durability of
a cultivar’s resistance depends on many fac-
tors, such as the rate of pathogen reproduc-
tion, the number of generations per year, the

Fig. I. The effects of specific and general resistance on progress curves. A, a cultivar with little general and no spe-
cific resistance; B, a cultivar with specific resistance but little general; C, a cultivar with considerable general
but no specific resistance; D, a cultivar combining the specific resistance of B with that of C. (After Van-
DERPLANK 1968).

16



*>

efficiency of genetic recombination in the
pathogen, as well as factors that affect selec-
tion pressures like the intensity of crop pro-
duction and the popularity of the cultivars
in the fields (Jenns et al. 1982). Moreover,
Kiyosawa (1982) and Leonard (1984) have
shown that durability does not depend on the
genetic background of the cultivar only, but
also on weather conditions.

Northern climatic conditions affect the
ecological aspects of host-parasite interac-
tions in several ways (Karjalainen 1985 a).
For example, field crop production in mar-
ginal areas is characterized by a limited num-
ber of pests and diseases because of cold

climate, and severe epidemics of many path-
ogens are comparatively rare. In addition,
short-season field production implies that
many biotrophic pathogens, for example,
powdery mildew of barley, produce a rela-
tively limited number of reproduction gener-
ations because they attack cereals at the later
stages of crop development and thus the ef-
fective time for reproduction is often very
short. Consequently, it has been suggested
(Karjalainen 1985 a) that in northern mar-
ginal areas resistance based on single genes
can in many cases give long lasting disease
protection.

17



3. Septoria nodorum on wheat: a polygenic host-pathogen system

3.1. Description, host range and
distribution of the disease

Description
Septoria nodorum (Berk) Berk, (perfect

stage: Leptosphaeria nodorum Muller) was
first described by Berkeley in 1885. First he
designated it the name Nepazea nodorum,
but later corrected it to belong to the genus
Septoria (Shipton et al. 1971). The identifica-
tion of S. nodorum is most reliably done
according to conidial morphology (Richard-
son and Noble 1970). The conidia have I—31 —3
septa, and they are usually no longer than
25 /un, however, the variability in conidia
size and shape as well as colony morphology
is large and may be affected by environment
(King et al. 1983). Harrower (1976) has de-
tected that S. nodorum can produce through
micropycnidia spores that are smaller than
the normal ones.

The symptoms of S. nodorum disease are
difficult to distinguish and identify, especially
in the early stages of infection when pycnidia,
sporulating bodies, are absent, and it can
easily be confused with natural senescence
(Shipton et al. 1971, Baker 1978). S. nodo-
rum causes lesions on the leaves and stems,
and they appear as linear, light brown spots
with a yellow margin (Figs 2,3). There is a
wide variation in symptom expression and it
depends on isolates, host cultivars, and en-
vironmental factors. Later in summer the
disease also infects the ears on which brown
spots appear (Fig. 4).

Host range
S. nodorum has been demonstrated to in-

fect a number of grasses and cereals (Smede-
gärd-Petersen 1974, Mäkelä 1975, Har-
rower 1977). Isolates from wheat can in-
fect alternative hosts (Shearer and Zadoks
1972 a), and extensive data (Ao and Grif-
fiths 1976, Fitzgerald and Cooke 1982,
Krupinsky 1982) suggest changes in virulence
after passage through an alternative host.
Flowever, studies on physiological specializ-
ation have lead to contradictory results. For
example, Smedegärd-Petersen (1974) and
Confer (1984, Confer and Yoomans 1983)
have demonstrated that isolates from wheat
are characteristically virulent to wheat and
avirulent to barley. However, Holmes and
Colhoon (1971) and Martin and Cooke
(1979) report that in Britain S. nodorum can
be pathogenic to barley and cross infection is
possible between isolates of barley and wheat.
Hitherto, there is no convincing evidence
suggesting significant isolate-cultivar inter-
actions, and thusphysiological specialization
in S. nodorum to wheat appears to be non-
race-specific (Allingham and Jackson 1981,
King et al. 1983).

Distribution
S. nodorum is an important pathogen in

many parts of Europe, North and South
America, Africa, Asia, Australia, and New
Zealand (Shipton et al. 1971, Eyal 1981,
King et al. 1983). Available data of world-
wide crop losses caused by S. nodorum are

18



19

Figs 2—4. Symptoms of the disease caused by Seploria nodorum. Lesions on leaves (Fig. 2), stems (Fig. 3), and
heads (Fig. 4 a, b).



lacking. However, reports from various coun-
tries suggest yield reductions of up to 65 %,

and in most cases of 25 % (Baker 1978,
Eyal 1981, King et al. 1983). The disease
has become increasingly important during the
last ten years in many wheat growing areas
of cool damp summers and mild winters.
The reason for this lies in the increasing area
of intensive wheat cultivation with dwarf
cultivars which appear to be susceptible to S.
nodorum (Saari and Wilcoxson 1974, Baker
1978, Eyal 1981). Further, increasing use of
non-ploughing techniques, which results in
less efficient stubble cultivations, can pro-
mote disease build-up (Baker 1978).

3.2. Epidemiology

3.2.1. Primary sources of infection
Infected seed

Seed has been found to be an important
source of inoculum in many wheat-growing
areas (Shipton et al. 1971, Shaner 1981,
King et al. 1983). The role of seedborne
inoculum as the source of infection depends
greatly on the longevity of inoculum on the
seed. Kruger and Hoffman (1978) found
that the amount of S. nodorum on seeds
depends on storage temperatures so that the
rate of decline increased with increasing tem-
perature. Further, they noted that the seed
was free of S. nodorum after two year’s
storage. However, recent studies (Confer
1981, Babadoost and Hebert 1984) indicate
that S. nodorum can survive and remain
virulent in storage for more than two years.

The seedborne Septoria first infects the
growing coleoptile from hyphae growing up
its outer surface (Baker 1971). Pycnidia on
the coleoptile may provide secondary inocu-
lum for infection of the leaves (Cooke and
Fozzard 1973, Hewett 1975). Coleoptile in-
fection appears to be more severe in soil with
a high moisture holding capacity (Holmes
and Colhoun 1975). Recent studies by Baba-
doost and Hebert (1984) suggest that there
is not necessarily a clear correlation between
percent seed infection and percent germina-

tion. In addition, high seed infection is not
always directly correlated with the severity
of disease symptoms (Cunfer and Johnson
1981).

Plant debris
S. nodorum is known to survive for con-

siderable lengths of time on plant debris
from previous wheat crops, and it can also
overwinter there (Brokenshire 1975, Holmes
and Colhoun 1975, Harris 1979). Survival
of the fungus depends on the temperature and
humidity of the debris so that if the debris
is alternatively wet and dry, new pycnidia
form abundantly (Scharen 1964, Harrower
1974). Spores are released from pycnidia in
wheat debris during rain and dispersed by
splash (Faulkner and Colhoun 1976). Under
favourable conditions, pycnidiospore produc-
tion may continuefor several months. Limit-
ed data concerning herbicide experiments
(Harris 1979) suggest that herbicides do not
seem to affect the survival of Septoria on
treated straw. The perfect stages, which oc-
cur rarely, can also be important sources of
inoculum (Sanderson and Hampton 1978).
Perithecia of L. nodorum develope on straw
and release ascospores during the season
(King et al. 1983). Alternative hosts such as
grasses and other cereals on which S. nodo-
rum can overwinter may also provide inocu-
lum reserves for disease build-up (Harrower
1977).

3.2.2. Factors affecting infection and
symptom expression

Environmental factors such as humidity
and temperature greatly effect the whole life-
cycle of S. nodorum (Shaner 1981). Release
of pycnidiospores occurs when free water
is present on the infected tissue or when
atmospheric humidity is nearly saturated
(Shaner 1981, King et al. 1983). Dispersal of
spores is connected with periods of rainfall.
It is evident (Jeger et al. 1981 a, King et al.
1983) that only a little amount of rain and a

short period is required to cause dispersal of

20



spores. Humidity affects symptom express-
ion to a great extent. For example, the rate
of symptom development and the overall
severity is closely correlated with high hu-
midity (Scharen 1964, Holmes and Colhoun
1974, Eyal et al. 1977). The duration of
latent period of S. nodorum (Shearer and
Zadoks 1972 b, Aust and Hau 1981) is also
shorter under more humid conditions com-
pared with other moisture treatments. Spores
of S. nodorum will germinate in temperatures
of s—37°C,5 —37°C, but the optimum is 20—25°C
(King et al. 1983). However, the optimum
temperature for infection is 18—25°C (Ship-
ton et al. 1971). Some data suggest (Shipton
et al. 1971) that at lower light intensities
plants seem to be more susceptible than at
higher intensities. Furthermore, it is well
known (Cooke and Jones 1970) that light
quality, for example the amount of near-
ultraviolet (NUV) light, can promote pyc-
nidium formation in leaves.

The growth stage of the host plant has
evidently some influence on symptom ex-
pression (Pirson 1960, Shipton et al. 1971),
but the results are so far contradictory. Evi-
dence is accumulating (Fried and Brönni-
mann 1982, J. Jönsson 1983, pers. comm.)
which suggests that wheat is more susceptible
at the later stage of development than at the
seedling stage.

Fertilization may also have some influence
on symptom expression, but very little is
known at present. Brönnimann (1968) has
found that high nitrogen fertilization and
Confer et al. (1980) excessive phosphorous
and potassium levels in soils make wheat
more susceptible to S. nodorum. Fertilizers
as well as chlorcholinchloride (CCC) (Brön-
nimann 1969) can affect tissue susceptibility
directly or indirectly by changing the micro-
climatic conditions more favourable to dis-
ease development.

3.3. Control measures

Several strategies can be used to control
the disease caused by S. nodorum: crop rota-

tion, resistant varieties, seed treatments, and
fungicide sprays (King et al. 1983). The ef-
fect of crop rotation on reducing the develop-
ment of S. nodorum is not well understood.
Some data (Luke et al. 1983) suggest that
one year rotation did not reduce the amount
of disease when uninfected seed was used. In
addition, Luke et al. (1983) found that two
year’s rotation did not significantly reduce
the amount of disease when infected seed
was used. Thus it seems evident that one or
two year’s rotation has limited value when
the percentage of seed infected is high and
weather conditions favour disease build-up.
However, long term rotations (Eyal 1981)
probably have great value in limiting inocu-
lum potential. In addition, ploughing-in of
infected stubble (Harrower 1974, Harris
1979) or burning it soon after harvest (Har-
rower 1974) are likely to reduce inoculum
potential for disease development.

Treatment of infected seed with organo-
mercury compounds has been found to be ef-
ficient in controlling seedborne S. nodorum
(Shipton et al. 1971). However, the control
has not always been complete and seed treat-
ment has had only minor effects on the sub-
sequent development of leaf attack (Bate-
man 1977, Obst 1977).

Fungicide sprays are now widely used to
control S. nodorum in many wheat-growing
areas. There are several fungicides available
(King et al. 1983) and many experiments
(Cook 1977, Kucharek 1977, Eyal 1981)
suggest profitable increases in yield. The
benefit of chemical control depends on vari-
ous factors, such as the price of the fungicide,
the price of wheat, the amount of disease,
and cultivar susceptibility. Recently, some
studies (Webster and Cook 1979, Menz and
Webster 1981) have clarified the economic
returns and costs when controlling S. nodo-
rum with fungicides. The proper timing of
fungicide sprays is of crucial importance for
an effective strategy (King et al. 1983). Cook
(1977) found that fungicide application be-
tween flag leaf emergence and ear emergence
resulted in considerable yield benefit. Early

21



sprays seem to give good disease control only
if weather subsequently favours disease de-
velopment (King et al. 1983). Thus, it ap-
pears that forecasting disease incidence is
required for optimal strategies of chemical
control.

The use of cultivar mixtures in cereal pro-
duction has received much attention in re-
cent years. There is a considerable body of
data (Browning and Frey 1969, Ayanru and
Browning 1977, Wolfe and Barrett 1982,
Munk 1983) which shows that using host
populations heterogeneous for resistance
genes can control many fungal parasites ef-

fectively. Recently, Jeger et al. (1981 b, c)
demonstrated theoretically and experimen-
tally that intraspecific mixtures of spring
wheat can reduce the disease development
of S. nodorum. This is supported by my
recent experiments (1985 b) indicating that
the disease level in mixed stand was less than
the arithmetic mean of the disease amount
in pure stands. However, it was found that
although the mixture reduced disease de-
velopment, it did not seem to prevent yield
losses under high disease conditions (Karja-
lainen 1985 b).

22



4. The aim of the present experimental study

Some years ago Mäkelä (1975, 1977)
made extensive surveys of the occurrence
of Septoria species in Finland and found
that S. nodorum was one of the major dis-
eases of wheat. However, no estimates of the
economical importance of this disease are
available, but practical experience suggests
that in rainy years S. nodorum has probably
caused significant yield reduction in wheat
crops. Foreign experience (Krupinsky et al.
1977) suggests that resistant sources are
available of the wheat germplasm, although
cultivars which are immune to S. nodorum
have not been found (Baker 1978).

Despite the polygenic nature of resistance,
significant progress in breeding for S. nodo-
rum resistance has been achieved (Brönni-
mann and Fossati 1977, Scott and Benedikz
1977, Scharen and Eyal 1980) and genetic

resistance appears to be the most feasible
method of controlling the disease in terms
of economic advantage over other control
methods (Doodson 1981).

Although some aspects, notably the epide-
miology, of this host-pathogen interaction
are extensively investigated (e.g. King et al.
1983), little is known about the mechanisms
of resistance, and for example, the ultrastruc-
tural nature of S. nodorum-wheat interac-
tion is largely unknown. Furthermore, rela-
tively little is also known about the value of
seedling plant tests to predict the field reac-
tions of cultivars to S. nodorum at the adult
plant stage. In Finland breeding wheats for
resistance to S. nodorum is just starting,
and practical experience is limited. Hence,
in 1979, a research programme was started

which was mainly aimed at providing relevant
basic information for wheat breeders and to
strengthen breeding work for resistance to S.
nodorum. More specifically, the aims of the
investigation were:

to reveal some ultrastructural interac-
tions between S. nodorum and spring
wheat
to study the effects of S. nodorum on
yield and yield components of spring
wheat
to study the inheritance of resistance with
applications for selection strategies
to evaluate seedling plant and mature
plant screening techniques

This experimental investigation is based
on the data presented in this study and on the
following articles which are referred to by
their Roman numerals.
I Karjalainen, R. & Lounatmaa, K. 1984.

Ultrastructure of pycnidiospore walls and
hyphae of Septoria nodorum. Trans. Br.
mycol. Soc. 83: 239—244.

II Karjalainen, R. & Lounatmaa, K. 1985.
Ultrastructure of penetration by Septoria
nodorum of wheat leaves. Accepted for
Physiol. Plant Pathol.

111 Karjalainen, R. 1985. Ultrastructure of
interactions between Septoria nodorum
and resistant wheat leaves. Submitted
for Trans. Br. mycol. Soc.

IV Karjalainen, R., Laitinen, A. & Juuti, T.
1983. Effects of Septoria nodorum Berk,
on yield and yield components of spring
wheat. J. Scient. Agric. Soc. Finl. 55:
333—344.

23



V Karjalainen, R. 1983. Inheritance of leaf
resistance to Septoria nodorum Berk, in
two crosses of spring wheat. J. Scient.
Agric. Soc. Finl. 55: 525 —530.

VI Karjalainen, R. 1984. Evaluation of de-

tached seedling leaves for use in screening
spring wheat cultivars to Septoria nodo-
rum Berk. Acta Agric. Scand. 34: 386
390.

24



5. Materials and methods

Production of inoculum

S. nodorum isolates were collected from in-
fected wheat leaves in southern Finland. For
mass production the most virulent isolates
were selected and grown on oatmeal agar in
petri dishes under near-ultraviolet irradi-
ation with cool-white fluorescent lamps for
7—lo days at 19—22°C.The NUV-light has
been shown to stimulate the pycnidia forma-
tion of S. nodorum (Cooke and Jones 1970).
In order to obtain densely sporulating cul-
tures some spore transfers were made. How-
ever, old cultures were avoided because of
decreasing aggressivity with increased age
(Scharen and Krupinsky 1973). The plates
were flooded with a small amount of ster-
ile water, and the cirrhi containing pyc-
nidiospores were removed by gently rubbing
the agar surface with a glass rod. The conidial
suspension was filtered through two layers of
cheesecloth, and spore concentration of 106
conidia/ml, but also higher concentrations,
was used, as suggested by earlier investiga-
tions (Krupinsky 1976, Eyal and Scharen
1977). To obtain better adherence of the
conidia to wheat leaves ’Tween 20’ surfacant
was used.

Plant material

Spring wheat breeding lines and cultivars
were kindly supplied by the Hankkija Plant
Breeding Institute (Hyrylä), Institute of Plant
Breeding, Agricultural Research Centre (Jo-
kioinen), S. G. Nieminen Oy (Helsinki), Sva-
löf AB (Sweden), Departments of Farm
Crops, Agricultural University of Norway
(Norway), Swiss Federal Station for Agrono-

my (Switzerland), Plant Breeding Institute
(England), and USDA (Maryland, USA).

Electron microscopy
For scanning electron microscopy, two

days after inoculation, sections of infected
leaves of about 5 mm were dehydrated after
ethanol series by critical point method in an
Aminco apparatus before evaporation with
gold in a Balzers apparatus Micro-BA3. The
scanning electron micrographs were taken
with a Jeol JSM-U3 electron microscope
operating at 12 kV.

For thin sections, samples were taken 3,6,
and 9 days after inoculation, and fixed in
2.5 % glutaraldehyde in sodium phosphate
buffer (0.1 M pH 7.2) for 2 h. The samples
were then washed four times with phosphate
buffer and postfixed for 2 h with buffered

1 % osmium tetroxide at room temperature
and dehydrated in a graded ethanol series.
Thin sections were obtained from ’Epon 812’
-embedded samples and stained with uranyl
acetate and lead citrate.

For freeze-fracturing the samples were
frozen in liquid Freon in the presence of 30 %

(v/v) glycerol and fractured at —l2O°C.
Methods of freeze-etching techniques used in
Septoria studies have been described by Kar-
jalainen and Lounatmaa (1984 I). Trans-
mission electron micrographs were taken
using a Jeol JEM-1008 transmission electron
microscope operating at 80 kV.

Field experiments
The field experiments were carried out at

the University Farm of Viikki, except for ex-
periment IV, which was carried out at the

25



Anttila Field Station of the Hankkija Plant
Breeding Institute. The data of crop loss
studies reported in this paper were based on
trials carried out in 1984. Cultivars Tähti and
Kadett were used in the experiments. In the
first part of the study normal breeding plots
(10 m 2) with three replications arranged in a
randomized block design were used. Standard
fertilization and herbicide treatments were
applied. In the second part of the study large
plots (20 m 2) with four replications arranged
in a randomized block design were used. Only
10 m 2 area was harvested for yield measure-
ments so that edge effects were avoided. The
plots were inoculated with spore suspensions
(106 conidia/ml) of S. nodorum three times,
starting before flag leaf emergence and re-
peating at three days intervals. Yield com-
parisons were made in relation to uninoc-
ulated control plots.

The data of the field screening method
reported in this paper based on the procedure
described by Scott and Benedikz (1977).
Small plots (0.3 m 2) with six replications
arranged in a randomized block design were
used. Inoculum was applied onto plants by
spraying (by a spray gun, 106 conidia/ml)
soon after ear emergence. After inoculation
the plants were kept damp by covering them
with plastic bags for 48 hours, followed by
daily irrigation starting one week after in-
oculation. The assessment of disease severity
was made by estimating the percentage area
covered by lesions 7,9, and 12 days after
inoculation.

The data of inheritance studies reported in
this paper based on the F 2 progenies derived
from crosses Hja 21600 X 80325, Hja 21600
x Cl 12463, Luja X 80325, and Hja 21600
X Cl 12463. The F, generation was grown
in the glasshouse, and it produced, by self-
fertilization, material for F 2 population.
The parents were selected to exhibit a wide
variation in height and resistance, Cl 12463
and 80325 being resistant and tall, Luja and
Hja 21600 very susceptible and short. Small
plots were space-planted with three replica-
tions arranged in a randomized block design.

Standard fertilization and herbicide treat-
ments were used. Inoculum was applied onto
the plants by spraying before flag leaf emer-
gence. After inoculation the plots were kept
damp by covering them with a plastic tent
for 48 hours. Irrigation was not necessary
because of rainy days. The assessment of
disease severity was made by estimating the
percentage area covered by lesions. At the
same time height was measured.

Seedling plant tests

The detached seedling plant tests reported
in this paper based on the method described
by Benedikz et al. (1981). Detached spring
wheat leaves taken from two leaf stage plants
were mounted on benzimidazole agar, and
localized inoculum drops of 3/d (10 7 co-
nidia/ml) were placed on the leaves using
a microsyringe needle. Ten leaves per petri
dishes with three replications were used (the
total range 27—30). The assessment of re-
sistance based on the measurement of lesion
length B—lo days after inoculation.

The second seedling test reported in this
paper based on the simplified attached seed-
ling leaf inoculation method. The seedlings
were grown in small pots (0 10 cm) con-
taining fertilized Finnpeat. Approximately
ten seeds/pot were used with 8 replications
arranged in a randomized block design. The
plants were kept in glasshouses at 18—21°C
with supplementary light (Philips lamps)
providing an 18 h photoperiod. Leaves were
inoculated with a spore suspension (10 7 co-
nidia/ml) containing 0.5 ml ’Tween 20’ sur-
facant per 100 ml of suspension. Inoculum
was applied by a spray gun at the two-leaf
stage. All plants were enclosed within poly-
ethene bags for 5 days to provide high hu-
midity for infection. The measurement of
disease severity according to percent disease
area based on assessing symptoms 7 and 9
days after inoculation.

Statistical analysis
The percentages of diseased leaf area were

transformed using the arc-sin transformation.

26



Variance analysis for comparing the yield Hja 21600 x 80325 (N = 67) and Hja 21600
between treatments was calculated (Karja-
lainen et ai. 1983 IV). Spearman’s rank cor-
relation, regression analysis, and correlation
analysis were computed. In addition, Path-
coefficient analysis was also calculated (IV)
according to Li (1975) in order to clarify the
direct and indirect effects on yield compo-
nents caused by S. nodorum. Statistical dif-
ferences between cultivars are not shown in
order to emphasize the relative values and the
fact that S. nodorum-wheat system is sen-
sitive to genotype-environmental interactions.

The objective of the present inheritance
study was to evaluate the upper limit for
narrow sense heritability of total variation in
symptom expression. Two crosses were used,

x Cl 12463 (N = 106), for calculations of
broad sense heritability estimates using a
general equation (e.g. Griffiths and Lawes
1978):

V
VP. + VP2

F2
~

2K
Vf2

where h£s = heritability in the broad sense
Vp2 = variance of F 2 progenies
V p

= variance of parents

The standard error for heritability estimates
was calculated in the previous study by Kar-
jalainen (1983 V).

27



6. Results and discussion

6.1. Host-pathogen interaction at
the cellular level

6.1.1. Ultrastructural aspects
of Septoria nodorum

Numerous studies have been carried out of
the fine-structural features of many sapro-
phytic fungi (Beckett et al. 1974), but our
knowledge of the ultrastructure of many
important pathogenic fungi is still lacking
(Cole et al. 1979, Griffin 1981). Hitherto,
very little is known about the fine-structure
of S. nodorum despite the fact that it is a
widespread and important pathogen.

Recently, Karjalainen and Lounatmaa
(1984 I) attempted to describe some fine-
structural features of S. nodorum using elec-
tron microscopic techniques. Transmission
electron microscopy (TEM) of thin sections
of hyphae revealed such cell organelles as
the nucleus and mitochondrion (Figs 5,6).
Freeze-etching techniques (Branton 1966)
appear to be a powerful method of revealing
unique features of membrane structures of
bacteria and of fungi (Griffiths 1971, Cole
et al. 1979). In freeze-etch replicas of cross-
fractured spores of S. nodorum (Fig. 7) such
organelles as the nucleus with nuclear pores
and a large lipid body are evident.

Recently, much effort has been concen-
trated on trying to understand cellular in-
teractions between plants and pathogens.
Available data (Keen 1982) suggest that in
many cases the early phases of the interac-
tion between plant and fungi are mediated
through molecules via cell wall contact.
Therefore, the knowledge of cell wall surface

structures of plant pathogenic fungi might
give important information which could help
to clarify the early stages of plant-pathogen
interaction (Rohringer et al. 1982). In con-
nection with the study on the ultrastructure
of the interaction between S. nodorum and
wheat leaves, a preliminary study was made
to clarify some ultrastructural features of the
cell walls of S. nodorum using different elec-
tron microscopic techniques (Karjalainen
and Lounatmaa 1984 I). Thin sections of
hyphae and pycnidiospores suggest the wall
to be composed of similar structures, an outer
electron-dense layer and an inner transparent
layer (I). The freeze-etching technique also
revealed some additional information on the
surface features of the outer cell wall layer.
The etched surface appears to be composed
of thin fibrillar and globular material of dif-
ferent size (I).

The thin material revealed by freeze-etch-
ing is probably fibrillar material, since chi-
tinous residues of fungal walls are often fi-
brillar when examined by electron microsco-
py (Jones and Johnson 1970). Data based
on many conidial fungi (Cole et al. 1979,
Schneider and Wardrop 1979) suggest that
the fibrillar material is often composed of
glycoprotein and chitin polysaccharide. The
precise role of this material is not well under-
stood (Cole et al. 1979). However, it is sug-
gested (I) that it may be important in the
attachment of a hypha to a host cell, but
this remains to be determined after detailed
chemical analyses of surface structures. In
addition, it might be necessary to use genetic
mutants of isolates in trying to find sol-

28



29

Fig. 5. Transmission electron micrograph of a median section through a hypha of S. nodorum showing some cell
organelles: nucleus (N), mitochondrion (m), and endoplasmic reticulum (HR), x 52 000.

Fig. 6. A higher magnification of the mitochondrion (m). x 65 000.

Fig. 7. Freeze-etched pycnidiospores of S. nodorum showing some cell organelles: nucleus (N), nuclear pores (np),
and lipid body (L). x 65 000.



utions to questions of the primary role of cer-
tain surface components in host-pathogen
interactions. Recently, Sequeira (1984) pro-
vided an experimental framework using mu-
tants of Pseudomonas bacteria as a model to
study the role of surface components in early
phases of plant-bacterium interaction.

6.1.2. Penetration

Rapid penetration through the natural
defence barriers of plants during the periods
of moisture that are adequate for germina-
tion and growth is necessary for many fungal
leaf pathogens before infection can be estab-
lished. Various fungi have different strategies
to encounter intact host surfaces. For ex-
ample, highly specialized biotrophic patho-
gens, such as rusts and mildews, have spe-
cialized infection structures, and they usually
penetrate into host plant through natural
openings without producing an extensive
amount of cell wall degrading enzymes (Aist
1976). On the contrary, many necrotrophic
pathogens, including fungi and bacteria,
are capable of producing a wide range of
cell wall degrading enzymes matching the
diverse polymers in plant cell walls (Cooper
and Wood 1980, Bishop and Cooper 1983,
Cooper 1983). There are extensive data of
the ultrastructural aspects of penetration by
biotrophic pathogens (e.g. Ingram et al.
1976, Maclean and Tommerup 1979). How-

ever, the ultrastructural nature of penetra-
tion is known only in a few necrotrophic
interactions (Politis 1976, Wheeler 1977,
Van Caeseele and Grumbles 1979, Bishop

and Cooper 1983, Keon and Hargreaves

1983).
It has been previously shown (Bird and

Ride 1981) that most S. nodorum spores
germinate within 6—B h after inoculation,
and penetration is observed about 10 h after
inoculation. However, there are no detailed
data of the ultrastructure of penetration,
which has partly been explained (Baker and
Smith 1978) by difficulties in staining the
hyphae within the leaf. Karjalainen and

Lounatmaa (1985 II) made an attempt to
clarify the ultrastructural nature of penetra-
tion. Scanning electron microscopic (SEM)
observations on the early stages of S. nodo-
rum infection indicate (Figs 8,9) spore ger-
mination and hyphal ramification over the
surface of wheat leaves. SEM studies (Baker
and Smith 1978) have previously shown that
S. nodorum conidia germinate, produce ap-
pressoria, and penetrate into host epidermal
cells. In order to clarify the penetration
event, it is necessary to make thin sections
after inoculation for transmission electron
microscopic observations. TEM studies (II)
showed that S. nodorum appears to grow in
both the intercellular spaces (Fig. 10) and the
intracellular spaces (II). The hyphae were
often surrounded by amorphous material
(Fig. 11), which seems to affect their attach-
ment to host cell wall. In many cases it was
evident that the hyphae were closely associ-
ated with host cell wall. Penetration appears
to take place directly through intact cell walls
(Figs 12, 13). There were some observations
(II) which suggest that the host cell wall
within the area around the penetration peg
was more diffuse than that of adjacent areas.

The study by Karjalainen and Lounat-
maa (1985 II) clearly indicates that S. nodo-
rum penetrates wheat leaves directly through
the epidermal cell walls. There has been a
long controversy among scientists whether
cuticular penetration is by mechanical force
or by enzymic hydrolysis (Verhoeff 1980,
Cooper 1983, Kolattukudy and Köller
1983). The data presented in our study do
not produce any definite proof for either
way of penetration. However, limited ultra-
structural observations (II) on the electron
lucent dissolution of wall material in front
of the penetration peg as well as observa-
tions that part of the host cell wall in contact
with the penetration peg was more electron-
dense than other parts, provide some clues
for the possible role of enzymic digestion in
penetration, as has been suggested on similar
grounds in some other studies (McKeen 1974,
Wheeler 1977, Bishop and Cooper 1983).

30



31

So far, there is no evidence of such cell wall
degrading enzymes in vivo, although some
data (Baker 1969) show that S. nodorum

produces in culture enzymes such as pectic
methylesterase and polygalacturonase. Thus
attempts using modern immuno-cytochemical

Fig. 8. Scanning electron micrograph of a ramifying hypha over the leaf surface of susceptible cultivar Tähti 2 days
after inoculation with S. nodorum. x 780.

Fig. 9. Scanning electron micrograph of a germinating conidium on the leaf surface of cv. Tähti 2 days after inocu
lation with S. nodorum. x 1 040.

Fig. 10. Transmission electron micrograph of an intercellular hypha (H) 3 days after the inoculation of cv. Tähti
with S. nodorum. x 20 800.



32

Fig. 11. Attachment of a hypha to host cell wall (cv. Tähti) 6 days after inoculation with S. nodorum. Note the
mucilagineous sheet (arrow), x 20 800.

Fig. 12. Penetration of the cell wall of susceptible cv. Tähti by a hypha of S. nodorum 6 days after inoculation.
Note the thin cell wall at the point of penetration (arrow), x 26 000,

Fig. 13. Complete wall penetration of susceptible cv. Tähti by a hypha of S. nodorum 9 days after inoculation,
x 26 000.



3

techniques (Shaykh et al. 1977) to localize
specific enzymes during infection might pro-
vide some evidence for their involvement in
penetration.

6.1.3. Nature of cellular resistance reactions

It is well known that the thickening on
the inner surface of cell walls at the site of
penetration by fungi is a common reaction
of plant cells to fungal invasion (Aist 1977,
Israel et al. 1980, Beckman et al. 1982,
Allen and Fried 1983). This type of de-
fence reaction is probably responsible for
the unsuccessful penetrations of many non-
pathogenic and pathogenic fungi, and it
might explain why only a small number of
micro-organisms are pathogenic. For ex-
ample, in leaves of Gramineae, cell wall
alterations, appositional wall formation, and
papilla formation are frequently associated
with unsuccessful penetration of the epider-
mal cells by pathogenic fungi (Politis 1976,
Ride 1978, Sherwood and Vance 1980), and
hence their important role in resistance has
been proposed (Ride 1978, Sherwood and
Vance 1982).

Previous studies on wheat-S. nodorum
interaction (Baker and Smith 1978, Bird
and Ride 1981) throw some light on the poss-
ible mechanisms of resistance. For example,
Bird and Ride (1981) reported that germ
tubes were shorter on more resistant varieties,
and on this basis cultivar differences can be
detected as early as 6—B h after inoculation.
Using light and stereoscan microscopy Baker
and Smith (1978) were able to demonstrate
differences in hyphal development between
resistant and susceptible varieties. However,
the biochemical basis of these differences is
largely unknown. Furthermore, Baker and
Smith (1977) made experiments in order to
test the role of antifungal compounds in-
volved in resistance, but no convincing evi-
dence has yet been published. Bird and Ride
(1981) demonstrated that lignification can
play an important role in restricting fungal
development. However, Baker and Smith

(1978) did not find evidence which would
support the role of lignin as an essential com-
ponent of resistance.

In order to obtain information on the cel-
lular nature of resistance, thin sections of
highly resistant wheat leaves were made after
inoculation for transmission electron micro-
scopy (Karjalainen 1985 III). The results
suggest that S. nodorum grows slowly and
ramifies over the leaf surface searching for
a suitably thin place for penetration (Figs
12, 14). It appears (III) that the majority of
penetration attempts fails, which seems to
be associated with cell wall alterations and
the formation of electron-dense material
(papillae) beneath the point of penetration
(Figs 15, 16). These observations support the
idea of Bird and Ride (1981) that the failure
of S. nodorum to penetrate epidermal cells is
associated with the deposition of new wall-
like material (papillae) and the alterations in
the upper epidermal walls and adjacent lat-
eral walls. The composition of these apposi-
tions and papillae is not known (Aist 1976),
but there is some evidence for wheat (Ride
and Pearce 1979, Ride 1983) suggesting that
they contain lignin-like material. Thus it is
possible that the depositions and papillae
found in this work (11, III) are lignin-like
material. Bird and Ride (1981) have sug-
gested that lignification is an important fac-
tor preventing hyphal development, and it is
more efficient on resistant cultivars. It was
also apparent from the ultrastructural data
of highly resistant interactions (III) that cell
wall alterations and papilla formation were
frequent, which probably explains why it
was very difficult to find successful penetra-
tions.

Increasing evidence has recently accumu-
lated which suggests that lignification may
play an important role in general defence of
plants against pathogen attacks (Vance et
al. 1980, Hammerschmidt and KuC 1982,
Sherwood and Vance 1982, Hammerschmidt
et al. 1984). Ride (1980, 1983) has listed
several alternative ways how lignification in-
hibits fungal growth. For example, lignifica-

33



34

Fig. 14. Transmission electron micrograph of a hypha 6 days after the inoculation of resistant wheat leaves (Cl
12463) with S. nodorum. Note the disorganization of chloroplast (arrow), x 20 800.

Fig. IS. Transmission electron micrograph of a penetrationattempt 6 days after the inoculation of cv. Tähti with
S. nodorum. Note the formation of penetration peg (arrow), x 15 600.

Fig. 16. Transmission electron micrograph of the blunt penetration peg (pp) 6 days after the inoculation ofcv. Täh-
ti with 5. nodorum. Note the presence of wall apposition (wa) which inhibits penetration, x 20 800.



35

tion might provide a mechanical barrier to
hyphae, restricting the diffusion of water
and nutrients or toxins between host and
parasite, impacting hyphal walls and reducing
their capacity to elongate, or protecting host
wall polymers from enzyme degrading. It
is probable that in the wheat-S. nodorum
interaction lignification might function as
a mechanical barrier to hyphae and thus
restrict their growth. Furthermore, it is also
possible that lignified cells might to some ex-
tent hinder host cell degradation by fungal
cell wall enzymes, assuming that enzymic
hydrolysis has a decisive role in penetration.
In addition, lignification may alter the toxin
sensitivity of the host, since there are some
reports on non-specific toxins isolated from
S. nodorum (Bousquet and Skajennikoff

1974, Kent and Strobel 1976). However, it
is very probable that mechanisms of resis-
tance to S. nodorum are complicated be-
cause this host-pathogen interaction is under
polygenic control and is non-race-specific,
and generally such systems involve sev-
eral mechanisms of resistance (Touzfi and
Esquerre-Tugaye 1982). Hence lignification,
cell wall alterations and papilla formation
may account for some part of the defence
systems, but many other factors may be in-
volved in resistance as well. Since the mech-
anism is complex, it is also evident that the
expression of different resistance mechan-
isms may be effective at different stages of
the infection process (III).

6.1.4. Pathological alterations in host
ultrastructure

The penetration of the plant by a patho-
gen leads to diverse changes in host physi-
ology, such as increasing rate of respiration
(Uritani and Asahi 1980, Kosuge and Kim-
pel 1981), decreased rate of photosynthesis
(Buchanan et al. 1981), and changes in sec-
ondary metabolism (Friend 1981). It is wide-
ly accepted (Aist 1976, Cooper 1981) that
biotrophic parasites cause minimal changes
in host metabolism in relation to necrotrophs

which frequently cause severe disruption in
host cytoplasm. An important observation
is that necrotrophs are capable of causing
drastic changes in host metabolism, often
in advance or during penetration (Wheeler
1977, Cooper 1981), while biotrophs cause
prominent changes usually at the later stages
of pathogenesis.

Plant pathogens are also known to cause
changes in host ultrastructure (Coffey et al.
1972, White et al. 1973, Heath 1974, Jones

et al. 1975, Cooper 1981). Figures 17 and
18 show that S. nodorum also alters the
ultrastructure of wheat leaves. For example,
deformation and disintegration of chloroplast
grana and lamellae are evident, as well as
an increased number of plastoglobuli (Figs
19, 20). Similar observations of some other
necrotrophic interactions have been found
(Jones and Ayres 1974, Cooper 1981). These
observations fit well the physiological studies
(Scharen and Taylor 1968, Scharen and
Krupinsky 1970, Krupinsky et al. 1973)
which indicate that photosynthesis is strongly
inhibited due to S. nodorum infection. Thus
electron microscopic data can provide addi-
tional evidence for the observation (Scharen
and Taylor 1968) that S. nodorum reduces
wheat photosynthesis and may in this way
reduce grain yield.

6.2. Effects of S. nodorum on wheat yield
and yield components

The impact of plant pathogens as yield
reducing factors has been known for a long
time, but the exact amount of crop losses
caused by them is difficult to determine.
Generally, the amount of pathogen-induced
yield reduction depends on the incidence and
severity of pathogen attacks, on their in-
fluence on plant physiological processes, and
the significance of these processes for yield
development (James and Teng 1979, Gaunt
1980).

Estimates of national crop losses due to
glume blotch disease are few. However, in
England and Wales routine surveys of leaf



36

Fig. 18. Ultrastructure of a chloroplast ofcv. Tähti 3 days after inoculation with S. nodorum. Note the disorgani
zation of grana (arrow), x 52 000.

Fig. 17. Transmission electron micrograph of a healthy wheat leaf (cv. Tähti). Note the well organized chloroplast
ultrastructure, particularly grana (G), x 39 000.

Fig. 19. Ultrastructure of a chloroplast of cv. Tähti 3 days after inoculation with S. nodorum. Note the presence
of plastoglobuli (P) x 52 000.

Fig. 20. Ultrastructure of a chloroplast of cv. Tähti 6 days after inoculation with S. nodorum. Note the presence
of numerous plastoglobuli and the disorganization of chloroplast. x 26 000.



37

diseases have provided some estimates for the
economic importance of crop losses (King
1977). For example, surveys of winter wheat
in 1970 s (King 1977) showed that Septoria is
the second most important leaf disease, and
Doodson (1981) estimated losses over the
ten year period to be about £ 82 300 000.

There are no extensive surveys of glume
blotch disease in Scandinavian countries.
However, it has been known for a long time
(Mäkelä 1975) that S. nodorum is one of
the major wheat diseases in Finland, and re-
ports from Sweden (Leijerstam 1972, Berg-
gren 1981), Norway (O. Elen 1984, pers.
comm.), and Denmark (V. Smedegärd-Pe-

tersen 1983, pers. comm.) suggest that it is
amongst the most prevalent leaf pathogens of
wheat in other Scandinavian countries, too.
As there are no data of crop losses caused by
S. nodorum in Finland, field experiments
were carried out at the Hankkija Plant Breed-
ing Institute (Karjalainen et ai. 1983 IV)
and at the University Farm of Helsinki Uni-
versity to provide a sound basis for the eco-
nomic evaluation of S. nodorum and its sig-
nificance for plant breeding.

The aim of the study carried out at the
Hankkija Plant Breeding Institute was to
clarify how low infection level affects the
yield of the moderately susceptible cultivar
Hankkija’s Taava. Therefore, low concen-
tration S. nodorum spore suspension was
sprayed onto the plots at heading stage, and
the yield response was compared with un-
inoculated control plots (IV). The results in-
dicated that low infection pressure reduced
grain yield by 10 % and 1000-grain weight by
14 % (Table 2). Data of single tillers (IV)
suggest that S. nodorum strongly reduced
grain number per ear and to some extent
spikelet number per ear. Consequently, this
study suggests that even under moderate
level of infection S. nodorum is capable of
markedly reducing yield. However, as Table 2
shows, the yield level in this experiment was
relatively low, which was due to unfavourable
weather conditions (IV), and hence wide
generalizations of these results should be

Table 2. Effects of S. nodorum on grain yield and
1000-grain weight of spring wheat cultivars
Tähti, Kadett and Hankkija’s Taava, in com-
parison with uninoculated control. Experi-
ment of 1981 based on data by Karjalainen
et ai. (1983 IV).

Treatment Grain yield 1000-gw

kg/ha ratio g ratio

EXPERIMENT 1984
Large plots
Tähti

Control 4374 100 39.3 100
Sep/oria-inoculation 2963 68 32.2 82
EXPERIMENT 1984

10 m 2 plots
Tähti

Control 5270 100 38.8 100
Septona-inoculation 3417 65 30.8 79

Kadett
Control 6287 100 41.5 100
Septoria-inoculation 4604 73 33.1 80
EXPERIMENT 1981

10 m 2 plots
Hankkija’s Taava

Control 2610 100 37.5 100
Septoria-inoculation 2350 90 32.3 96

made with caution.
Experiences of wheat growing in southern

Finland suggest that under field conditions
S. nodorum attacks some wheat cultivars
very heavily in rainy years, and particularly
the cultivar Tähti has suffered greatly. There-
fore, field experiments were carried out at
the University Farm of Viikki to clarify how
high level of infection affects wheat yield. In
the year 1984 cultivars Kadett and Tähti,
both common in southern Finland, were
inoculated with high spore concentrations,
and the yield reduction was compared with
uninoculated control. The results indicate
(Table 2) that severe infection in large plot
experiments reduced the grain yield of Tähti
by 32 % and the 1000-grain weight by 18 %.

Crop losses in experiments using normal
breeding plots were 35 % in the grain yield
of Tähti and 27 ®/o of Kadett; the 1000-grain
weight of Tähti was reduced by 21 % and
that of Kadett by 20 %. Consequently, these
experiments strongly suggest that under high



infection conditions S. nodorum has a high
potential to reduce yield.

The data from these studies are in accord
with several previous investigations (Brönni-
mann 1968, Spierz 1973, Nelson et al. 1976)
which indicate that a moderate or high in-
fection level at a later developmental stage
causes severe yield reductions mostly due to
lowered grain weight. It is known (e.g. Evans
1975) that the grain yield of wheat is deter-
mined mainly by carbohydrates produced
after ear emergence by the flag leaf, head
and penduncle, and the development of these
organs also depends on assimilates trans-
located from the leaves below the flag leaf.

Consequently, S. nodorum may affect
yield, for example, indirectly by damaging
lower leaves, thus reducing the number of
sites for assimilate depositions (Scharen
and Taylor 1968) and directly by damaging
the flag leaf with the consequence of reduc-
tion in overall photosynthesis and assimilate
accumulation.

Leaf pathogens are known to reduce the
rate of photosynthesis (Buchanan et al.
1981). There are some data (Scharen and
Taylor 1968, Scharen and Krupinsky 1969)
which show that S. nodorum caused a strong
reduction in the photosynthetic rate, but
the reason for this is not known. Although
there is some evidence (Buchanan et al.
1981) that infection can reduce the number
of chloroplasts, there is no direct evidence
that this has any major effect on the pho-
tosynthetic rate. On the other hand, some
data of physiological studies (Magyarosy
and Malkin 1978) suggest that disease infec-
tion can alter the partial reactions of pho-
tosynthesis, such as photophosphorylation,
electron transport chain, and ribulose-1,5-
bisphosphate carboxylase activity. Very re-
cently, Walters and Ayres (1984) provided
evidence that ribulose-1,5-bisphosphate car-
boxylase (RußPase) of barley, a key enzyme
in photosynthesis, is inhibited due to mildew
infection. However, as there are no data of
similar studies on Septoria infected wheat
leaves, it remains to be shown whether the

reduction in photosynthesis can be explained
on similar grounds.

It has been suggested (Brönnimann 1968)
that yield loss caused by 5. nodorum may be
partly explained by the fact that infection in-
terferes with translocation. S. nodorum in-
fection may enhance translocation because it
appears to accelerate the onset of senescence
(Spierz 1973). However, there is no evidence
that the interference with translocation by
infection might explain any important part
of yield losses. For example, Wafford and
Whitbread (1976) demonstrated that despite
extensive lesions on the leaves, S. nodorum
infection appeared to alter the export of
assimilates from a leaf only to a small extent,
and obviously this also has littleeffect on the
patterns of assimilate distribution. Scharen
et al. (1975) also found that axial lesions by
S. nodorum did not interfere with the trans-
location of assimilates.

Extensive data of cereal foliage diseases
indicate (James and Teng 1979, Teng and
Gaunt 1980—81, Carver and Griffiths
1981) that the disease severity and the timing
of the attack determine which yield com-
ponents are most affected. Generally, early
attacks mainly affect the number of fertile
tillers and grains per ear and to a less extent
grain size, while late attacks mainly reduce
grain size. S. nodorum is capable of attacking
wheat at all stages of growth. It is suggested
(Baker 1978) that early attacks stunt the
plant and thus disturb growth, but very little
is known about the significance of early infec-
tion to yield reduction. A number of studies
have led to the idea that late attacks are
most damaging. The present study confirms
this idea since inoculation at the later phase
of development caused a strong reduction in
yield. Particularly late infection had great
influence on 1000-grain weight (Fig. 21)
(IV), which has been confirmed by a number
of previous studies (Jones and Odebunmi
1971, Jones and Rowling 1976, Wafford
and Whitbread 1978). This can be under-
stood easily because it is known that pho-
tosynthesis after post-anthesis can greatly

38



contribute to grain-filling, and Lupton (1969),
for example, has shown that the ear receives
assimilates almost exclusively from the flag
leaf. Hence damages at the upper leaves have
strong effect on grain weight.

Karjalainen et ai. (1983 IV) demonstrate
that heavy infection seems to reduce all yield
components, but they also suggest that in
some cases the reduction in grain weight can
be compensated by more grains being filled
per ear in some tillers. This observation is in

accord with those of Jones and Rowling

(1976) and Wafford and Whitbread (1978),
who also found compensation effects. How-
ever, the compensatory mechanism might be
too weak after severe infection and cannot
prevent yield reductions.

It has been observed (Brönnimann 1968,
Scharen and Taylor 1968, Obst 1977) that
S. nodorum is capable of causing yield reduc-
tions that are not always correlated with
symptoms on which disease assessments are
based. Karjalainen et ai. (1983 IV) also
found some evidence that disease severity
was not always correlated with yield loss,
and even susceptible cultivars can possess
some tolerance to attacks by S. nodorum
(Brönnimann 1968). It seems, however, dif-
ficult to explain why in some cases lower in-
fection causes comparatively heavy yield re-
ductions. It has been suggested that S. nodo-
rum can cause yield reductions without caus-
ing symptoms (Obst 1977, Bannon 1978).
Further, Brönnimann (1968) and King et al.
(1983) have suggested that yield damages
may be partly due to the effect of a toxin.
There is some information on toxins purified
from S. nodorum cultures. A phytotoxin,
septorin, produced in vitro has been impli-
cated in causing changes in the respiratory
activity of wheat mitochondria (Bousquet et
al. 1980). Ochracine, the other toxin purified
from S. nodorum has been found to inhibit
the net assimilation rate of wheat (Bousquet
et al. 1980). Consequently, it has been sug-
gested (King et al. 1983) that the toxin effect
might to some extent account for yield losses
at low infection levels. However, available
data are too limited to draw any firm con-
clusion about the role of toxins in the yield
losses caused by S. nodorum.

6.3. Genetic nature of resistance

6.3.1. Inheritance of resistance

Genetic progress in plant breeding for dis-
ease resistance depends on several factors,

Fig. 21. Relationship between disease severity and
grain weight on cultivars Kadett and Tähti.
Solid line indicates flag leaf severity and
dotted line ear severity. Data based on Karja-

lainen et al. 1983.

39



such as the availability of resistance sources,
appropriate screening techniques, and the
genetic nature of the host-pathogen interac-
tion. Previous studies (Laubscher et al. 1966,
Nelson 1980, Mullaney et al. 1982, Scott
et al. 1982) provide evidence for polygenic
control of host reaction to S. nodorum both
at the seedling plant stage and at the mature
plant stage. However, Kleuer et al. (1977)
have shown a single dominant gene to give
simply inherited monogenic resistance at the
seedling plant stage. Hitherto, however, there
is not enough evidence for the idea that single
genes alone can give an easily detectable lev-
el of resistance at the mature plant stage
(Scharen and Eyal 1980, Scott et al. 1982).

Efficient selection work on improving
quantitative traits requires information on
heritability values, which indicate the propor-
tions of variation due to genotype and en-
vironment. Wheat breeding for resistance to
S. nodorum as well as to many other diseases
usually starts by the selection of resistant
plants in F 2 populations. In order to clarify
the effects of selection for resistance to S.
nodorum a crossing program was started to
provide material for inheritance studies in
F 2 progenies. In the first investigation (Kar-
jalainen 1983 V) two spring wheat cultivars
were tested in the field at the heading stage
to infection by S. nodorum. The variation in
symptom expression was continuous, pro-
viding no support for the existence of in-
dividually acting major genes. The broad
sense heritability values were moderate at
0.47 and 0.34 with over half of the variation
being of environmental origin. As the broad
sense heritability estimates provide an upper
limit for narrow sense heritability, it can be
concluded that in these particular crosses
genetic variation is rather low and environ-
mental variation accounts for a major part
of the total variation in symptom expression.
Consequently, it follows that reliable selec-
tion in F 2 populations greatly depends on
efficient screening techniques to detect slight
differences between plants.

In the second investigation (Table 3) the

Table 3. Summary of heritability estimates (h 2) of
resistance of wheat to 5. nodorum obtained
from literature and data presented in this
study. Broad sense heritability estimates are
shown in the text by bs.

Crosses Sourceh 2

Hja 21600x80325, F 2 0.62 bs this study
Hja 21600 x Cl 12463, F 2 0.92 bs this study
Tähti xTGS/334/747, F 2 0.34 bs Karjalainen

1983 V
Tähti x Maris Butler, F 2 0.47 bs Karjalainen

1983 V

500 F 6 (or later) lines 0.89 Aastveit 1982
572 F 3 lines leaf 0.63 Rosielle and

head 0.50 Brown 1980
Diallel, tolerance F, 0.66 Brönnimann

1975
F 2 0.65

parents for crosses were selected to exhibit
an extreme range of susceptible and resistant
reactions based on previous information of
cultivar resistance to S. nodorum (Karjalai-
nen et ai. 1983). The results indicate that
crosses between susceptible and highly resis-
tant cultivars lead to quite high broad sense
heritability values of 0.63 and 0.92.

In general, symptom expression was con-
tinuous, but some tall plants exhibited very
low infection. Consequently, it appears that
progenies derived from crosses between sus-
ceptible and highly resistant parents include
segregants which may not give clear single
gene effects, but seem to provide a rather
clear variation on thebasis of whichresistant
and susceptible plants can be rather easily
recognized. The present result supports the
recent observation by Scharen and Eyal

(1983) suggesting that highly resistant cul-
tivars may be governed by major R-genes.
Hence, selection for resistance to S. nodo-
rum in F 2 populations based on crosses in-
volving highly resistant parents is expected to
be rather rapid because the heredity com-
ponent of variation is large enough to permit
efficient selection. Table 3 shows that the
estimates of heritability values vary largely.

40



Most of these studies indicate a moderate
level of heritability, and some reveal very
high levels of genetic variation (Aastveit
1982). On the other hand, Scott et al. (1982)
have suggested that in most of their winter
wheat crosses the heritabilities were low and
the standard errors high. One reason for
this variation may be that the experiments
have been carried out at different growth
stages and under varying environmental con-
ditions using different inoculation techniques.
There is a considerable body of evidence
(Scharen and Eyal 1980, Fried and Brönni-
mann 1982, Mullaney et al. 1982) that this
host-pathogen interaction is not only sensitive
to inoculation differences but also to en-
vironmental changes which may mask genetic
differences.

Available data of genetic studies shed some
light on practical wheat breeding strategies
against S. nodorum. It is obvious from the
results of the present investigation and the
other data (Table 3) that the genetic vari-
ation in symptom expression is large enough
to permit reliable grounds for selection work.
In addition, Mullaney et al. (1982) have
recently shown that the genetic control of
leaf resistance can be mainly explained by
additive gene effects. Similar results have
been obtained from diallel experiments by
Nelson (1980) and Nelson and Gates (1982).
Brönnimann (1975) showed that tolerance,
measured as the loss of 1000-kernel weight is
polygenically determined and controlled by
additive gene action. Nelson (1980) found
that general combining ability effects were
highly significant, but specific combining
ability effects were observed as well, indi-
cating non-additive gene action in some spe-
cific crosses. Thus, increasing data is ac-
cumulating which shows that the resistance
of wheat to S. nodorum is mainly controlled
by additively acting genes, which means that
the breeder may try to improve the level of
resistance by accumulating desired genes into
populations. Thus transgression breeding
may be one way of improving the level of
resistance of wheat to S. nodorum.

6.3.2. Association of resistance
with agronomic traits

Advances in breeding for disease resistance
have sometimes been hampered by the as-
sociation of resistance with agronomically
undesirable characteristics (Simmonds 1979).
There are some reports which suggest that
wheat resistance to S. nodorum is positively
associated with late maturation time (Scott
1973, Eyal 1981, Scott et al. 1982, Karja-

lainen et al. 1983) and tallness (Hope 1957,
Brönnimann 1969, Scott et al. 1982). The
association between tallness and resistance
has been explained (Scharen 1964) by the
idea that infection usually starts at the base
of the plants and moves upwards by splash
dispersal of the conidia. Hence short cultivars
become generally more severely infected
than tall ones because their tissue is nearer to
the source of inoculum (Fried and Brönni-
mann 1982). It is also apparent that the can-
opy of short cultivars remains wet longer
than that of tall ones, which may provide
favourable conditions for disease develop-
ment (Karjalainen 1984).

It is important for wheat breeders toknow
whether this association between tallness and
disease severity is also clear in segregation
generations, since the general aim of wheat
breeding is a moderately short straw which
guarantees a reasonable level of lodging re-
sistance. In order to clarify this question some
crosses between susceptible short cultivars
and lines (Hja 21600 and Luja) and highly
resistant tall lines (80325 and Cl 12463) were
carried out. The results clearly indicate (Fig.
22) that susceptibility is significantly nega-
tively correlated with tallness, the coeffi-
cients ranging from —0.58 to —0.63 (p <

0.001). Consequently, it is evident that in
these crosses a great part of the variation in
leaf resistance was associated with plant
height. Hence wheat breeding for resistance
to S. nodorum is faced with difficult prob-
lems, if short straw, as it normally is, is an
important breeding objective. Rigorous selec-
tion in F 2 populations for resistance is likely

41



to move populations towards increased tall-
ness. The strength of theassociation between
tallness and resistance depends on the genetic
nature of the association. Scott et al. (1982)
carried out extensive studies to clarify the
genetic nature of this association. Their data
suggest that the association between plant
height and resistance is mainly due to pleio-
tropy rather than linkage. Thus, one or more
genes that promote short straw may also
promote susceptibility. However, Scott et

al. (1982) also found that there was an im-
portant part of the variation that was in-
dependent of height. The present data sup-
port this idea since there was a considerable
level of resistance in medium or short straw
plants (Fig. 23).

Significant negative association between
earliness and resistance is evident from the
data based on cultivar trials (Fig. 24) thus
supporting the previous studies (Fig. 25)
Karjalainen et ai. 1983). This association

Fig. 22. Relationship between leaf disease severity and
plant height on F 2 progenies derived from
crosses between resistant tall and susceptible
short spring wheat cultivars and breeding
lines.

42



43

might be more problematic for northern
wheat breeding than the apparent association

1977) which guarantees crop certainty under
northern marginal conditions.

between plant height and resistance since ear-
liness is a major criterium (Mukula et ai.

Although the present study and other data
suggest that resistance to S. nodorum is often

Fig. 23. Relationship between leaf disease severity and plant height on some spring wheat cultivars and breeding
lines.

Fig. 24. Relationship between time of ear emergence and leaf disease severity on some spring wheat cultivars and
breeding lines.



associated with late maturation time and
long straw, there are, however, many devi-
ations. Practical evidence (e.g. Scott et al.
1982) and the present cultivar trials indicate
that moderately short and early cultivars
with a moderate degree of resistance have
been produced. Scott et al. (1982) have also
stated that the success of breeding depends
more on efficient selection than inadequate
sources of resistance.

6.4. Assessment of disease resistance

6.4.1. Detection of resistance at the adult
plant stage under field conditions

Quantitative resistance is characterized by
continuous variation in sympton expression,
and it cannot be separated into clear-cut
classes. Consequently, one of the major
problems in utilizing this type of resistance is
to find sensitive screening techniques in order
to detect genetic differences from environ-
mental factors. Rosielle and Brown (1980)

suggest that there are three mechanisms of
resistance operating in the S. nodorum-wheat
system: escape mechanisms, true resistance,
and tolerance. It is obvious that very of-
ten the resistance to S. nodorum is masked
by different escape mechanisms (Fried and
Brönnimann 1982). For example, under field
conditions late cultivars often appear to be
more resistant than early ones (Karjalainen
et ai. 1983). However, in years with a rainy
late summer susceptible late cultivars may
suffer great losses because their grain filling
process is slow and thus sensitive to late at-
tacks by S. nodorum with the consequence
of heavy reduction in yield.

Several screening techniques are used in
breeding wheat for resistance to S. nodorum,
but often many of these methods have given
different results even though the same lines
or cultivars have been tested (Rufty et al.
1981 a). During the last ten years extensive
work has been focused on improving the
reliability of methods for testing the reactions
of wheat lines and cultivars to S. nodorum.

Fig. 25. Relationship between maturation time and leaf disease severity on some spring wheat cultivars and breed
ing lines. Data based on Karjalainen et ai. 1983.

44



The central idea of the screening method
is based on the fact that the life cycle of
S. nodorum requires humid conditions. The
release and dispersal of conidia and the ger-
mination and growth of germ tubes requires a
wet leaf surface (Shipton et al. 1971, Holmes
and Colhoun 1971, 1974, Eyal et al. 1977,
Jeger et al. 1981 a). Frequent rains associ-
ated with moderate temperatures, that is
12—25°C, provide favourable conditions for
disease build-up in wheat fields (Polley and
Clarkson 1978, Eyal 1981). Furthermore,
S. nodorum is mainly spread by rain-splashed
drops and inoculum sources within a crop
are obviously more important than external
sources (Griffiths and Ao 1976, Jenkyn and
King 1977, Jeger 1983). Thus it follows that
under natural conditions the disease is not
often evenly spread over the experimental
field. Particularly under northern conditions
weather conditions are not favourable every
year for disease incidence, and in order to
meet the requirements for efficient resistance
breeding, it is necessary to use artificial in-
oculations to test breeding lines and popula-
tions.

Breeding lines and cultivars as well as seg-
regation populations can be tested either at the
seedling plant stage or at the mature plant
stage. The advantage of using mature plant
tests is based on the relevant information (e.g.
Brönnimann 1968) that S. nodorum causes
most damages at later growth stages, and sev-
eral other factors, such as height and matura-
tion time, also affect the expression of resis-
tance. Moreover, the evaluation of resistance
at the mature plant stage enables the scrutiniz-
ation of other breeding objectives at the same
time. In the present investigation the validity
of the field screening method developed by
Scott and Benedikz (1977) was tested, and it
was applied to reveal the resistance of Finnish
cultivars and foreign sources to S. nodorum.
The results indicate continuous variation in
sympton expression (Fig. 26), and all cultivars
were infected but to various degrees. This test
seems to easily reveal the most resistant culti-
vars and lines, such as Cl 12463, T. dicoccum,
T. timopheevi, Isepton 64, and Isepton 93. It
is also apparent on the basis of this test that
most Finnish cultivars and breeding lines are
fairly susceptible. The most susceptible ones

Fig. 26. Leaf disease severity (average of two upper leaves) to infection by S. nodorum as revealed by artificial field
inoculation test. The percentage diseased leaf area values were transformed using the arc-sin transforma-
tion.

45



appeared to be Hja 21600, Hja’s Ulla, Jo
8187, Jo 8218, Luja, and Tähti. However,
some cultivars, such as Hja’s Tapio, Hja
21182, Swedish varieties Kadett and Drabant,
and Norwegian Norröna appeared to be only
moderately attacked by the disease.

The field technique developed by Scott
and Benedikz (1977) appears to be a rapid
and reliable way to test breeding lines and
cultivars to S. nodorum. It was apparent that
in order to obtain reliable results one has to
be very careful in spraying inoculum onto
plants. To ensure an even spread of inoculum
and to promote infection, it is useful to make
several successive inoculations. In addition,
it is very important to determine the best
assessment time as the clear differentiation
between cultivars or lines seems to persist for
10—14 days depending on prevailing weather,
after which symptoms are masked by rapidly
increasing senescence. Although this test
reveals easily the most resistant, moderately
resistant, and susceptible cultivars, the detec-
tion of minor differences between cultivars
requires a great number of replications. This
is probably due to the fact that this host-
pathogen system is sensitive to genotype-
environment interaction (Mullaney et al.

1982), which can weaken the separation of
small differences. Particularly environmental
conditions following inoculation affect sub-
sequent disease development to a great ex-
tent. For example, an exceptionally high
temperature after inoculation can mask the
heritable differences of symptom expression
between cultivars (Karjalainen et ai. 1983).
Because of these environmentally induced
changes in cultivar differences, Fried and
Brönnimann (1982) suggest that comparisons
between cultivars should be made only if
they were inoculated on the same day since in
this way the differences caused by changes in
environmental conditions can be avoided.
However, the simultaneous inoculation can
be problematic because it has been recent-
ly shown that tissue susceptibility is also
dependent on the growth stage of the plant
(King et al. 1983, Sharma and Brown 1983,
J. Jönsson 1983, pers. comm.). There are
some data which suggest that tissue suscep-
tibility increases with age so that it is at maxi-
mum at heading/flowering (Brönnimann
1968). In the present study, figures 27 and 28
clearly indicate that late cultivars Kadett and
Tähti are more resistant than the early ones
at early observation times, but at the latter

Fig. 27. Disease progress of S. nodorum on two leaves of five spring wheat cultivars in variety trials at the Hankkija
Plant Breeding Institute in 1981. Data based on Karjalainen et ai. 1983.

46



half of the season susceptible cultivars can be
severely diseased.

The present artificial inoculation method,
followed by covering the plots with plastic
bags, raises some important questions for
wheat breeding. This kind of method is rather
laborious and time consuming, which implies
that only a relatively small number of lines
can be tested on limited resources. The plastic
bags, in particular, cause a lot of extra work.
In addition, under plastic bags the normal
plant growth may be disturbed, which may
make it difficult to evaluate other breeding
objectives at the same time. Recently, these
problems have been solved using fair repeated
irrigation to provide humid conditions and
by making several inoculations to ensure
favourable disease development (P.R. Scott
and P.W. Benedikz 1982, pers. comm.).
This permits efficient evaluation of many
characters simultaneously and reduces the
time needed for plastic bag work.

The data reported in this investigation
reveal some important aspects for practical
resistance breeding. For example, it is evident

that there is a fairly high level of resistance
to S. nodorum in wheat germplasm. How-
ever, the most resistant ones are wild Triticum
species T. timopheevi and T. dicoccum thus
confirming previous studies (Krupinsky et
al. 1972, 1977, Tomerlin et al. 1984), as well
as some other varieties such as Cl 12463,
which was very tall and late maturing under
Finnish conditions. Unfortunately, this kind
of material is difficult to utilize in practical
wheat breeding because the resistance genes
from these sources are likely to be associated
with many agronomically undesirable char-
acters. However, it is clear from this study
that a moderate level of resistance with suit-
able agronomic background is available and
can easily be utilized in Finnish spring wheat
breeding (Fig. 26).

6.4.2. Detection of resistance at the
seedling plant stage under
glasshouse conditions

Screening of wheat lines under field con-
ditions during growing season has many

Fig. 28. Disease progress of S. nodorum on two upper leaves of five spring wheat cultivars in field trials at the Uni
versity Farm of Viikki in 1984. The plots (3 m 2) were inoculated at the five leaf stage.

47



advantages, but it also involves several draw-
backs. For example, in summer breeders are
faced with a number of breeding objectives
which have to be evaluated in a relatively
short time, and any extra character to be
assessed requires extra time meaning that
less time can be devoted to evaluate single
progenies and characters. In addition, the
resistance of wheat to S. nodorum is asso-
ciated with such agronomic traits as height,
maturation time, and growth stage, which
might confuse the detectionof true resistance.
Therefore, in the last few years more atten-
tion has been focused on the possibility of
testing seedlings in the glasshouse or lab-
oratory in order to evaluate cultivars and
breeding lines to S. nodorum (Pirson 1960,
Kietreiber 1962, Eyal and Scharen 1977,
Benedikz et al. 1981).

At present two methods are used in testing
wheat seedlings to infection by S. nodorum.
Seedlings can be inoculated by spraying
them with spore suspension at two—three
leaf stage, or detached seedling leaves can be
mounted on benzimidazole agar with a drop
of inoculum placed on the centre of the
piece. Hitherto, only a few studies have been
carried out (Benedikz et al. 1981, Rufty et
al. 1981 a) to evaluate how seedling tests
predict the field performance of adult plant

resistance. In order to obtain more informa-
tion on this, seedling tests were started in
1982 to provide material for comparisons
between field tests and seedling tests.

In the first investigation, seedlings were
inoculated in glasshouse at two leaf stage
and covered with a plastic tent for providing
high humidity for disease development. The
data suggest that the symptoms were clearly
visible three days after inoculation, and the
best time to differentiate the cultivars for
their reactions to S. nodorum appeared to be
6—B days after inoculation. The results in-
dicated (Fig. 29) that the most resistant lines/
cultivars were T. timopheevi, T. dicoccum,
and Cl 12463, while amongst the most sus-
ceptible ones were Jo 8259, Jo 8292, Jo 8187,
Tähti, Hja 21485, and Hja’s Ulla. The seed-
ling test also revealed that such cultivars and
lines as Kadett, Drabant, Norröna, Hja’s
Tapio, Hja 21182, and 80325 have a moder-
ate level of resistance to S. nodorum. An im-
portant aspect is that this test reveals easily
the most susceptible and the most resistant
ones as indicated the field test (Fig. 30). The
overall correlation between this seedling test
and the field test appears to be very high
(r = 0.82, p < 0.001), and the seedling test
thus seems to predict the field performance
of the cultivars quite well. However, some

Fig. 29. Leaf disease severity (average of two upper leaves) to infection by S. nodorum as revealed by the seedling
test based on inoculation with spore suspension on plants at the two leaf stage in glasshouse. The percenta-
ge diseased leaf area values were transformed using the arc-sin transformation.

48



4

cultivars clearly deviate from this general
pattern (Fig. 30). For example, the cultivar
Calanda appeared more resistant in the field
than at the seedling level.

In the second investigation detached seed-
ling leaves were mounted on benzimidazole
agar according to Benedikz et al. (1981) to
evaluate the seedling reaction of wheat cul-
tivars to S. nodorum. Following drop in-
oculation, the symptoms were clearly visible
four days after inoculation, and the cultivars
were best differentiated to the reaction by
the disease B—lo8 —10 days after inoculation. The
data reveal (Fig. 31) that T. timopheevi,
T. dicoccum, and Cl 12463 were again the
most resistant entries, while Tähti, Hja 21485,
Hja 46592, Hja’s Taava, and Jo 8219 were
among the most susceptible ones. It was also
clear that such cultivars as Kadett, Drabant,
and Norröna, among others, indicate a mod-
erate level of resistance to S. nodorum at the
seedling stage. The overall correlation be-
tween the detached seedling leaf test and the
field test is moderately high (r = 0.63, p <

0.001) indicating that the detached seedling
leaf test predicts the field performance quite

well. However, some cultivars again deviate
greatly from this general pattern (Fig. 32).
For example, Calanda and 80325 were more
resistant in the field test than in the detached
seedling leaf test, while Jo 8187, Jo 8275,
and Hja 21600 appeared more susceptible in
the field test.

The seedling tests evaluated in this study
provide important information on the general
value of seedling tests to predict the field
performance of wheat cultivars to reaction
by S. nodorum. The two seedling tests are
quite well mutually related, as revealed by the
high correlation coefficient (r = 0.79, p <

0.001). However, there were some deviations
which need further clarification. Those devi-
ations may be due to some extent benzim-
idazole agar effect, since benzimidazole is
a fungicide and can somehow affect fun-
gal growth in the leaf, as already noted by
Übels (1979). It is also evident that the de-
velopment of infection is slower in detached
leaves mounted on benzimidazole agar than
on attached leaves, and attached leaves can in
some cases provide a wider range of variation
in sympton expression than the detached

Fig. 30. Relationship between seedling plant test (Fig. 29) and artificial field inoculation test. Data based on arc-sin
transformed values.

49



leaves thus making cultivar comparisons
easier. However, in general the visual assess-
ment of seedling plants appears to be more
liable to estimation errors (Koch and Hau
1980) than the detached seedling leaf test

which is based on quantitative measurement
of lesion length. In addition, uneven spread
of inoculum onto the plants in the attached
seedling test may cause variation in the re-
sults, which is not a problem in the detached

Fig. 31. Susceptibility of spring wheat cultivars and breeding lines to S. nodorum as revealed by detached seedling
leaf test mounted on benzimidazole agar.

Fig. 32. Relationship between detached seedling leaf test and artificial field inoculation test.

50



51

seedling leaf test because the inoculum drop
can be exactly measured and placed on the
centre of leaf pieces. However, there are in-
creasing data (Eyal and Scharen 1977,
Scharen and Eyal 1980) which clearly indi-
cate that the difficulties concerning spraying
techniques can be overcome by using quanti-
tative inoculation methods, and there is every
reason to assume that an experienced re-
searcher can rapidly and reliably visually
evaluate cultivar differences.

The method developed by Eyal and Scha-
ren (1977) provides an efficient technique
to evaluate the reactions of cultivars and
breeding lines to S. nodorum at the seed-
ling stage. Recently, Rufty et al. (1981 a) in-
dicated that seedling tests based on the Eyal

and Scharen (1977) method can predict re-
liably the field reaction of cultivars to S. nodo-

rum. In addition, this quantitative method
and its modifications can be used in screening
segregation populations, and Scharen and
Krupinsky (1978) have been able to improve
significantly the level of resistance to S. nodo-
rum using the above seedling test by Eyal
and Scharen (1977). On the other hand, it
seems evident that the use of detached seed-
ling leaves should be limited to parallel use
with field tests in assessing the reactions of
cultivars and breeding lines to S. nodorum.
The previous data (Karjalainen 1984 VI) as
well as studies by Benedikz et al. (1981) sug-
gest that this technique reveals the field per-
formance of most cultivars quite well. How-
ever, the detached seedling leaf test is not
suitable for evaluating segregation popula-
tions.



7. General discussion perspectives for future wheat breeding
for disease resistance

Plant breeding for cereal improvement has
made outstanding progress during the past
decades. One of the best known examples
of this is English wheat breeding. National
wheat yields have approximately doubled
during the past 35 years, from 2.4 tons/ha
in 1946 to 5.7 tons/ha in 1980 (Bingham
1981 a, Lupton 1982), and comparisons be-
tween old and modern varieties show that
about half of this increase is due to the work
of plant breeders. Major part of yield in-
crease is explained by the increase in harvest
index (Austin et al. 1980). The above yield
comparisons were made under conditions
where disease attacks and lodging were pre-
vented. However, it is evident that plant
breeding has also significantly improved
straw stiffness, baking quality, and disease
resistance. Kivi (1963) showed that Finnish
plant breeding has also made significant con-
tributions by improving cereal yields, and
there is no doubt about the better yielding
ability of current spring wheat varieties com-
pared with the old ones, although such com-
parisons are not available.

Wheat breeding for disease resistance has
also been successful in many countries (Lel-
ley 1976, Bingham 1981 b). Progress has
almost always been faster if the resistance
genes are of large effect and dominant (Day
1984 b) like, for example, the breeding
against rusts and mildew. However, the past
history of using dominant single genes for
disease control also provides examples of
failures when new physiological races capable
of breaking host resistance have emerged

(Kiyosawa 1982). Consequently, we are now
aware of the importance of the structure
and dynamics of pathogen populations for
breeding single gene resistance to achieve
long lasting disease control (Wolfe et al.
1983, Leonard 1984, Wolfe 1984).

Progress in wheat breeding for resistance
to S. nodorum has not been remarkably fast.
The main reason for this is the quantitative
nature of the resistance. Hence the detection
and incorporation of resistance into new
breeding lines is difficult (Brönnimann 1982,
Fried and Brönnimann 1982). Similar prob-
lems are faced in wheat breeding for quanti-
tative resistance to mildew, and Bennett
(1984) concludes that the present methods of
testing quantitative resistance are labour in-
tensive and inappropriate as selection criteria
for breeding programmes. However, practical
plant breeding has succeeded in improving
the level of Septoria resistance (Scott et al.
1982), and Doodson (1981) has shown the
significant economic benefit of cultivating
resistant wheats to control Septoria diseases.

The data presented in this study aimed at
providing relevant information for the in-
tensification of Finnish wheat breeding for
resistance to S. nodorum. The strategy of
wheat breeding is to detect the rare plants
with an improved combination of characters
(Lelley 1976, Bingham 1979). Thus as the
breeder’s task increases in complexity, the
more plants must be grown for selection in
segregation populations (Day 1984 b), and
the more difficult it is to find rare plants
with an improved combination of traits such

52



as yield, quality, straw stiffness, earliness,
and disease resistance. Consequently, it is
necessary to assess the relative economic im-
portance of the diseases likely to be encoun-
tered by a new variety.

The present study suggests that S. nodo-
rum is capable of causing significant yield
reduction even at a moderate level of infec-
tion, and under high disease conditions the
reduction in yield can be very great. It also
seems probable that S. nodorum can reduce
wheat quality because hectolitre weight was
reduced, and the reduction in grain weight
may have some other consequences, for ex-
ample reduced loaf volume. Mäkelä (1975)
indicated that S. nodorum was one of the
major pathogens of wheat, and later studies
(Avikainen and Hollo 1985, Karjalainen

unpublished) suggest that it is frequently
found in the wheat growing areas of Finland.
Thus there is every reason to assume that in
long term S. nodorum reduces yields to such
extent that preventing losses can stabilize
Finnish wheat production. Host resistance
to control damages caused by S. nodorum
seems to be economically the most attractive
method (Doodson 1981).

Seeking sources of resistance is the first
step in incorporating genetic resistance into
crop plants. The present study as well as
other data (Krupinsky et al. 1977, Tomerlin
et al. 1984) suggest that an adequate level of
resistance is available in the wheat germplasm
to enable successful resistance breeding.
However, it appears that the highest level of
resistance is found in wild Triticum species
and a number of lines and cultivars which
are very tall and late maturing. Thus the in-
corporation of high level resistance into well
adapted wheat backgrounds should be one
of the primary objectives of wheat breeding
programmes for resistance to S. nodorum.
It is not reasonable to use these high level
sources in practical wheat breeding unless
their resistance genes have been incorporated
into adapted wheat backgrounds. However,
breeders can currently use a number of lines
and cultivars, for example those Nordic va-

rieties which have a moderate level of Septo-
ria resistance.

The success in breeding for resistance to
S. nodorum depends greatly on efficient
methods of detecting resistant plants during
the various phases of breeding. Following
crossing and F, self-pollination, genetic seg-
regation generates diverse populations in F 2,

where visual selection on a single plant basis
for high heritability characters such as agro-
nomic type and disease resistance is practiced
(Bingham 1979, 1981 b). The present in-
heritance studies suggest that the heredity
component of resistance is high enough to
permit efficient selection work, but also sug-
gest that breeding success depends greatly on
sensitive methods of finding resistant plants
in F 2 populations.

Efficient screening of segregation popula-
tions for resistance to S. nodorum can be
done using alternative techniques. The ad-
vantage on inoculating plants with spore sus-
pension at the seedling plant stage is that in
this way the influence of growth stage on
symptom expression can be avoided. How-
ever, inoculating plants at the mature plant
stage is supported by the idea (Brönnimann
1968, Scott and Benedikz 1977) that host
tissue is most susceptible at heading and
flowering phase, and during this time it is
easy to take other breeding objectives into
account. It seems evident that if inoculations
are made before flag leaf emergence or soon
after that, the genetic differences in symptom
expression will be clear enough to permit
efficient selection. Experience of screening
work suggests that in order to detect resistant
recombinants in progenies derived from mod-
erately resistant crosses, it is particularly
important to make successive inoculations
and to provide humid conditions to ensure
favourable disease development. Assessments
based on visual estimations of percent area of
diseased leaf are most convenient in practical
breeding since such criteria as the number of
lesions or the amount of necrosis (Scharen
and Krupinsky 1978) are too labour intensive
as well as utilizing differences in latent period

53



or other components of partial resistance
(Jeger et al. 1983).

F 3 selections are based on observations
made on separately grown ear-row plots.
Screening for resistance to S. nodorum is
done mainly in fields, but a limited number
of progenies can be tested in glasshouse using
seedling inoculation developed by Eyal and
Scharen (1977). In view of practical breeding
it is important that desired resistant and
agronomically adapted plants can be tested
in this generation for protein quality using,
for example, the sodium dodecyl sulphate
(SDS) precipitation test (Blackman and Gill
1980). This method is very rapid and requires

a small sample size, and it appears to be a
good measure of inherent protein quality
which correlates well with baking quality
(Payne et al. 1979, 1980).

Testing breeding lines and cultivars for
resistance to S. nodorum can be done both in
the field and in the glasshouse. The present
study suggests that the field method devel-
oped by Scott and Benedikz (1977) is ef-
ficient in testing mature plant resistance.
A particularly important piece of informa-
tion from thepresent studies was that seedling
techniques based on detached seedling leaves
mounted on benzimidazole agar and attached
seedling leaves can predict the field reaction
of most cultivars quite well (see also Rufty
et al. 1981), and thus they may considerably
help the testing of breeding lines and cultivars
because the tests can be carried out during
the winter period.

Resistance to S. nodorum appears to be
durable since there are no reports of physio-
logical races capable of breaking host resis-
tance despite the widespread cultivation of
resistant varieties (Scott et al. 1982, King et
al. 1983). However, S. nodorum is a highly
variable pathogen. For example, Scharen
and Krupinsky (1970) and Griffiths and Ao
(1980) found a great variability in spolia-
tion, colony morphology, and aggressiveness
among single conidium isolates taken from a
single pycnidium. The genetic basis of the
variation in S. nodorum is poorly understood

because the sexual stage occurs rarely in
nature and has not been induced in artificial
culture (Griffiths and Ao 1980). Variation
may be due to heterokaryosis, parasexual
recombination (Griffiths and Ao 1980) or
it may be associated with the presence of
mycoviruses or plasmids which have been re-
cently found to cause variation in aggressive-
ness in other fungi (Hollings 1982, Hashiba
et al. 1984). Hitherto, available evidence sug-
gests (Griffiths and Ao 1980, Allingham
and Jackson 1981, Rufty et al. 1981 b, King

et al. 1983) that cultivar resistance to S. nodo-
rum is non-specific and despite the fact that
isolates differ in aggressiveness, they do not
differ in the range of cultivars attacked.

Whether modern research tools such as
recombinant DNA technology can provide
novel avenues for speeding up the develop-
ment of resistant cultivars is a question of
much interest. During the last five years
remarkable progress has been made in de-
veloping transformation systems for plants
(Caplan et al. 1983, Hull 1983, Murai et
al. 1983, Paszkowski et al. 1984). Transform-
ation systems based on Ti plasmids of
Agrobacterium tumefaciens are nearly ready
to introduce purified DNA sequences into
plants (De Block et al. 1984, Herrera-
Estrella et al. 1984, Matzke et al. 1984).
Unfortunately, these systems can be applied
to a limited range of crop plants only, and no
vectors for cereals other than maize are to be
expected in the near future. Thus, it appears
that for many years to come conventional
breeding methods will play a major role in
developing resistant wheat varieties. Further,
since only single gene traits can be improved
by genetic engineering (Comai and Stalker
1984, Day 1984 c), it is probable that its im-
pact on wheat breeding will be marginal be-
cause the most important characters are con-
trolled by many genes.

However, novel avenues for controlling
diseases like S. nodorum may open in the
far future when the nature of disease process
is well understood. For example, current
research (Kolattukudy and Köller 1983,

54



Soliday et ai. 1984) is trying to reveal the
nature of the first step in infection, and the
first molecular interaction between the host
and the pathogen, the outcome of which
determine the disease reaction. The present
ultrastructural observations which have
shown that the penetration by S. nodorum
takes place directly through intact cell sur-
faces may be important for future studies.
Understanding the early phases of infection
and the nature of defence mechanisms could

open novel avenues such as developing anti-
penetrants for disease control (Maiti and
Kolattukudy 1979). So far, new approaches
to control S. nodorum appear to be only
theoretical, and the present knowledge sug-
gests that the best way of controlling the
disease caused by S. nodorum is integrated
control using seed treatment, crop rotation
and resistant cultivars as well as under high
disease conditions sprayings with fungicides.

55



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65



Selostus

Kevätvehnän Septoria nodorum -resistenssi
taudinkestävyysjalostuksen näkökulmasta

Reijo Karjalainen
Helsingin yliopiston kasvipatologian taitos ja
kasvinjalostustieteen laitos
00710 Helsinki 71

Tutkimuksessa tarkastellaan Septoria nodorum Berk,
-sientä, joka aiheuttaa kellanruskeita laikkuja vehnän
lehtiin ja varsiin sekä ruskettaa tähkän kaleita. Viime
vuosina Septoria-tauti on lisääntynyt eri puolilla maail-
maa ja aiheuttanut tuntuvia satotappioita. Suomessa si-
tä esiintyy koko vehnän viljelyalueella, ja sateisina kas-
vukausina sen lisääntyminen on ollut silmiinpistävää.
Tautia voidaan osittain torjua kylvösiemenen peittauk-
sella, vuoroviljelyllä ja fungisidiruiskutuksilla. Ulko-
maiset kokemukset kuitenkin osoittavat, että resistent-
tien lajikkeiden viljely on tehokkain ja halvin torjunta-
muoto. Tämän tutkimuksen tarkoituksena oli selvittää
niitä perusedellytyksiä, joilla vehnän Septorian kestä-
vyysjalostusta voitaisiin tehostaa.

Elektronimikroskoopilla tutkittiin Septorian infektio-
prosessia ja osoitettiin, että sieni tunkeutuu kasviin suo-
raan soluseinän läpi. Sienen tunkeutuminen resistenttiin
kasviin estyy osittain sen vuoksi, että resistentti solukko
muodostaa tunkeutumiskohtaan tiiviin suojakerroksen,
joka estää sienen etenemisen.

Septorian vaikutusta kevätvehnän satoon tutkittiin
useassa kokeessa. Vuoden 1981 kokeessa kohtalainen
infektio alensi Hankkijan Taava-lajikkeen satoa 10 %

ja 1000-siemenen painoa 14 %. Vuonna 1984 voimakas
infektio alensi suurilla koeruuduilla tehdyssä kokeessa
Tähti-lajikkeen satoa 32 % ja 1000-siemenen painoa

18 %. Toisessa vuonna 1984 tehdyssä kokeessa voima-
kas infektio alensi Tähti-lajikkeen satoa 35 % ja 1000-
siemenen painoa 21 % sekä Kadett-lajikkeen satoa
27 % ja 1000-siemenen painoa 20 %. Tulokset osoitta-
vat selvästi, että jo kohtalainen infektio alentaa tuntu-
vasti vehnän satoa.

Septono-taudin resistenssin periytyvyyttä tutkittiin
F 2 -risteytysjälkeläistöstä, joka oli saatu risteyttämällä
alttiita ja kestäviä lajikkeita. Tulokset osoittavat, että
ympäristövaihtelu selitti toisissa risteytyksissä yli puolet
taudin ilmenemisestä, mutta risteytyksissä, joissa toinen
vanhempi oli erittäin kestävä, periytyvien osien määrät
olivat sangen korkeita. Resistenssin havaittiin korreloi-
van positiivisesti kasvin pituuden ja myöhäisyyden
kanssa, mikä vaikeuttaa jalostustyötä. Tämä tutkimus
kuitenkin osoittaa, että kestävyysaineistoissa on kohta-
laisen kestäviä aikaisia linjoja ja lajikkeita, joita voi-
daan hyödyntääpohjoisten alueiden kevätvehnän jalos-
tuksessa.

Kevätvehnälajikkeiden ja jalostuslinjojen Seploria-
taudin kestävyyttä selvitettiin kenttä- ja laboratoriotes-
tein. Kenttätestit osoittivat, että kestävimpiä olivat villit
vehnät ja hyvin myöhäiset sekä pitkät lajikkeet. Eräät
Pohjoismaissa viljellyt lajikkeet kestivät tautia kohtalai-
sesti, mutta suurin osa kotimaisista oli hyvin alttiita.
Kasvihuoneessa testattiin kahdella menetelmällä lajik-
keiden ja linjojen taudinkestävyyttä taimivaiheessa.
Molempien testien avulla kyettiin nopeasti ja luotetta-
vasti seulomaan altteimmat ja kestävimmät lajikkeet.
Taimitestit korreloivat melko hyvin kentlätestien kans-
sa. Tutkimus osoittaa, että taimitestit voivat merkittä-
västi helpottaa jalostuslinjojen testausta, koska testit
voidaan tehdä talvella. Keinotekoiseen saastuntaan pe-
rustuva kenttätesti on luotettava ja tehokas keino seuloa
jalostuslinjoja ja jakautuvia varhaisia populaatioita.

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