Caryologia. International Journal of Cytology, Cytosystematics and Cytogenetics 74(3): 53-63, 2021

Firenze University Press 
www.fupress.com/caryologia

ISSN 0008-7114 (print) | ISSN 2165-5391 (online) | DOI: 10.36253/caryologia-1139

Caryologia
International Journal of Cytology,  

Cytosystematics and Cytogenetics

Citation: Pelin Yilmaz Sancar, Sem-
settin Civelek, Murat Kursat (2021) The 
morphological, karyological and phylo-
genetic analyses of three Artemisia L. 
(Asteraceae) species that around the 
Van Lake in Turkey. Caryologia 74(3): 
53-63. doi: 10.36253/caryologia-1139

Received: November 23, 2020

Accepted: May 26, 2021

Published: December 21, 2021

Copyright: © 2021 Pelin Yilmaz Sancar, 
Semsettin Civelek, Murat Kursat. This 
is an open access, peer-reviewed arti-
cle published by Firenze University 
Press (http://www.fupress.com/caryo-
logia) and distributed under the terms 
of the Creative Commons Attribution 
License, which permits unrestricted 
use, distribution, and reproduction 
in any medium, provided the original 
author and source are credited.

Data Availability Statement: All rel-
evant data are within the paper and its 
Supporting Information files.

Competing Interests: The Author(s) 
declare(s) no conflict of interest.

ORCID
PYS: 0000-0002-6134-622X 
SC: 0000-0003-1398-585X  
MK: 0000-0002-0861-4213

The morphological, karyological and 
phylogenetic analyses of three Artemisia L. 
(Asteraceae) species that around the Van Lake in 
Turkey

Pelin Yilmaz Sancar1,*, Semsettin Civelek1, Murat Kursat2

1Fırat University, Faculty of Sciences, Department of Biology, 23119 Elazıg, Turkey
2Bitlis Eren University, Faculty of Arts and Sciences, Department of Biology, 13000 Bitlis, 
Turkey
*Corresponding author. E-mail: peyilmaz@firat.edu.tr

Abstract. Artemisia is one of the biggest genera in the family Asteraceae, with around 
500-600 taxa at specific and sub-specific levels and organised in five subgenera. Due to 
the high number of taxa, a lot taxonomists are trying to solve the problem of its classi-
fication and phylogeny but its natural classification still has not been achieved. The aim 
of this study is to try to solve the problematic systematic relationship between three dif-
ferent Artemisia species growing in close proximity to each other in the light of mor-
phological, karyological and molecular data. The roots, stems, leaves, flowers structures 
of the plant samples collected from different populations belong to these species were 
investigated within the framework of morphological studies. Additionally, the chromo-
some counts and karyotype analysises of these species were made and idiograms were 
drawn in the karyological studies. In the context of phylogenetic studies, ITS (ITS1-
5.8S-ITS2) and trnT - trnL3’ regions of 22 individuals belonging to 3 taxa were stud-
ied. According to results of phylogenetic anlysis, it has been found that there is com-
pleted speciation genetic isolation mechanism between the species Artemisia spicigera, 
Artemisia taurica and Artemisia fragrans that inhibit gene flow. Also Artemisia fragrans 
and Artemisia spicigera species are very similar to each other in terms of morphological 
characteristics. However, since populations of the species Artemisia fragrans are autopol-
yploid, the dimensional values of their morphological squares are larger than those of 
the species Artemisia spicigera. This study is important as it is the first molecular based 
study relating with some species of Artemisia growing naturally in Turkey.

Keywords: Artemisia, karyology, morphology, phylogeny, cpDNA trnT-trnL3’, r-DNA 
ITS.

INTRODUCTION

Artemisia is one of the biggest genera in the family Asteraceae, with 
around 500-600 taxa at specific and sub-specific levels and organised in five 
subgenera (Vallès et al., 2011). The majority of the members of this genus 
have a high economic value (Chehregani et al., 2010; Hayat et al., 2010). Due 



54 Pelin Yilmaz Sancar, Semsettin Civelek, Murat Kursat

to the high number of taxa, a lot taxonomists are trying 
to solve the problem of its classification and phylogeny 
but its natural classification still has not been achieved 
(Mcarthur et al., 1981; Torrel et al., 1999; Torrell and 
Vallès 2001; Vallès et al., 2003; Kurşat, 2010; Kurşat et 
al., 2011). The genus is currently divided into five main 
groups [Artemisia, Absinthium (Mill.) Less., Dracuncu-
lus (Besser) Rydb., Seriphidium Besser and Tridentatae 
(Rydb.) McArthur] but subgeneric classification is sub-
ject to rearrangements in the light of recent molecular 
studies (Torrell et al., 1999; Vallès et al., 2003). 

Although a lot of investigation have been made of 
the genus Artemisia, enhancing the available morpho-
logic and karyological data (Kawatani and Ohno 1964; 
Vallès 1987a; Torrell et al., 1999; Torrell and Vallès 2001; 
Torrell et al., 2001; Vallès and Mcarthur 2001; Vallès et 
al., 2001; Kreitschitz and Vallès 2003; Inceer and Hay-
irlioglu-Ayaz 2007; Pellicer et al., 2007; Chehregani and 
Hajisadeghian 2009; Nazirzadeh et al., 2009; Chehrega-
ni et al., 2010), still the chromosome numbers of some 
species of the genus remain unknown or doubtful. The 
genus has two basic chromosome numbers, the largely 
predominating x=9 and the less extended x=8. x = 9 is 
not only the most common basic number in the genus 
Artemisia, but in the tribe Anthemideae and the family 
Asteraceae as well (Mcarthur and Sanderson 1999; Oliva 
and Vallès 1994; Schweizer and Ehrendorfer 1983; Sol-
brig 1977; Vallès and Siljak-Yakovlev 1997). A high per-
centage of Artemisia species are polyploid. This phenom-
enon is present in all of the major groups into which the 
genus is divided. Both basic chromosome numbers (x=8 
and x=9) show polyploidy, with levels up to 12x for x=9 
and 6x for x=8 (Vallès and Mcarthur 2001). 

The gene regions that have been used for phylogeo-
graphic and phylogenetic inferences in plants come from 
the single copy portions (LSC and SSC) of the chloroplast 
genome, and internal transcribed spacer (ITS) regions 
of nuclear ribosomal DNA (rDNA). Several molecular 
methods have been used to determine the genetic diver-
sity and relationships among different Artemisia spe-
cies, including karyotyping (Mcarthur and Pope 1979), 
cpDNA restriction site variation analysis (Kornkven et 
al., 1999), polymerase chain reaction restriction fragment 
length polymorphism (PCR–RFLP) analysis of several 
genes (Lee et al., 2009; Mahmood et al., 2011), microsat-
ellite (SSR) polymorphism analysis (Tripathi et al., 2009; 
Shafie et al., 2011) and Random amplified polymorphic 
DNA (RAPD) analysis (Mcarthur et al., 1998a; Mcarthur 
et al., 1998b; Sangwan et al., 1999). Nevertheless, very 
few of Artemisia species have been verified with molec-
ular phylogenetic studies based on nucleotide sequence 
data in Turkey, so far (Koloren et al., 2016).

So, the aim of this study is to try to solve the prob-
lematic systematic relationship between three different 
Artemisia species growing in close proximity to each 
other in the light of morphological, karyological and 
molecular data (using of rDNA ITS and trnT-trnL3’ 
regions sequence data). Additionally, the first molecular 
data for Artemisia spicigera, Artemisia taurica, and Arte-
misia fragrans from Turkey has been submitted to the 
GenBank databases.

MATERIAL AND METHODS

Morphological evaluation

Plant specimens were collected from around the Van 
Lake during the vegetative, flower and seed season in 
2010, collected by M. Kurşat, Ş. Civelek and P.Y. Sancar. 
Morphological examinations consist of instant observa-
tions on the samples in the field and macroscopic and 
microscopic examinations on the samples that have been 
converted into herbarium material in the laboratory. In 
order to determine the minimum and maximum val-
ues of the examined characters, 10 samples were taken 
from each locality and measurements were made. Meas-
urements of small structures were made with a ruler 
under a stereo microscope. Measurements of macro-
scopic structures were made using the ruler again with 
the naked eye. The herbarium materials of the collected 
samples are stored in Firat University Herbarium (FUH). 
The list of the examined specimens, localities, collected 
date and voucher numbers were given in Table 1. 

Karyology

Meristematic cells of root tips are used in the car-
yological studies. The seeds (about 15-20 seeds for each 
type) were germinated on moist filter paper in petri 
dishes between 20-25°C. The actively growing root tips, 
1  cm in length, were excised from the germinating seeds 
and pretreated with aqueous colchicine (0.05%) for 
3-3.5  h at room temperature. Then, the root tips were 
fixed with Farmer (1:3 glacial acetic acid–absolute etha-
nol) for at least 24 h at 4°C, hydrolysed in 0.1 N HCl at 
room temperature for 1 min, and subsequently rinsed in 
tap water for 3–5 min. Then they were stained in Feul-
gen for 1 h and mounted in 45% acetic acid (Gedik et al., 
2014). Digital photographs from at least five well-spread 
metaphase plates from each species were taken using 
an Olympus BX51 microscope (Olympus Optical Co. 
Ltd, Tokyo, Japan), and were recorded with an Olym-
pus Camedia C-4000 digital camera (Olympus Optical 



55The morphological, karyological and phylogenetic analyses of three Artemisia species

Co. Ltd) (Figure 1). The short arm, long arm and total 
lengths of each chromosome were measured and the 
relative lengths (RL), arm ratios (AR), and centromeric 
indices (CI) were determined from images of selected 
cells. Levan et al. (1964) was used for the classification of 
chromosomes. 

The number of somatic chromosomes, ploidy level, 
karyotype formula, morphometric parameters, A1 and 
A2 values (The intrachromosomal asymmetry index - 
A1 and the interchromosomal asymmetry index - A2) 
were determined for each taxa (Romero Zarco 1986)

(Table 2). Idiograms of haploid chromosomes were 
drawn (Figure 2). The examined taxa and characteristics 
of somatic chromosomes are given in the results section.

Genomic DNA isolation, PCR, and Sequencing

Genomic DNA isolation was performed manually 
as described CTAB method by Doyle and Doyle (1987). 
In PCR studies conducted by using trna- trnd primers 
and ITS4-ITS5 primers, trnT - trnL3’ and ITS (ITS1-

Table 1. Information of Artemisia populations location in field.

Taxa Locality Altitude Lat - Lon Date Voucher number

A
. s

pi
ci

ge
ra

Ant valley slope 5.5 km after passing Aktuzla 1555m 39°.21’-42°.15’ 10.10.2010
Yilmaz Sancar, Kurşat and Civelek 

5007,5008,5022
Hınıs - Varto highway, 24 km before Varto 

roadside, slopes
1780m 39°.13’-41°.42’ 10.10.2010

Yilmaz Sancar, Kurşat and Civelek 
5009,5024

Van - Hakkâri road, after 1 km of Gürpınar 
road separation, Çavuştepe locality roadside

1799m 38°.20’-43°.25’ 25.11.2010
Yilmaz Sancar, Kurşat and Civelek 

5013

A
. f

ra
gr

an
s

Kuzgun Koran Pass hills 2142m 38°.23’-42°.47’ 09.10.2010
Yilmaz Sancar, Kurşat and Civelek 

5001,5002,5010,5011
Between Edremit and Gürpınar, 15 km before 

Gürpınar
1714m

38°.19’-43°.14’
09.10.2010

Yilmaz Sancar, Kurşat and Civelek 
5003,5012

Muradiye - Şelale location 1788m 39°.03’-43°.25’ 10.10.2010
Yilmaz Sancar, Kurşat and Civelek 

5005,5016
Between Malazgirt - Aktuzla, around Nurettin 

village roadside slopes
1728m 38°.50’-43°.25’ 26.11.2010

Yilmaz Sancar, Kurşat and Civelek 
5017

After passing Aktuzla 5.5 km, Ant Valley 
slopes (roadside slopes)

1555m 39°.21’-42°.15’ 26.11.2010
Yilmaz Sancar, Kurşat and Civelek 

5006,5019,5020,5021,5023

A
. t

au
ri

ca

Van-hakkari highway, after 1 km of Gürpınar 
crossroads, Çavuştepe area, roadsides

1799m 40°.25’-43°.20’ 25.11.2010
Yilmaz Sancar, Kurşat and Civelek 

5004,5027,5028,

Figure 1. Somatic metaphase in A. spicigera (2n=18), and haploid idiogram (Scale bars: 1 μm).



56 Pelin Yilmaz Sancar, Semsettin Civelek, Murat Kursat

5.8S-ITS2) region for 22 samples has been multiplied 
(Taberlet et al., 1991). The sequence of primers that were 
used to amplified both trnT - trnL3’ region and ITS 
(ITS1-5.8S-ITS2) region were given in Table 3 (Taberlet 
et al., 1991). The following protocol on a BıoRad Ther-
mal Cycler : 2 min 95 °C initial denaturation, 35 cycles 
of 1 min 95 °C denaturation, 40 s 60 °C (for trn region) 

and 55 °C (for ITS region) annealing and 1 min 72 °C 
extension, followed by a 5 min final extension at 72 °C. 
PCR products were monitored in agarose gel with a 1 
% ratio. Two-way reading was applied to the amplifica-
tion products. PCR purification process was realized 
before sequence analysis. The purification and sequenc-
ing process was realized by the Macrogen Company. 

Table 2. Somatic chromosome numbers (2n), ploidy level, karyotype formula, ranges of chromosome length, total karyotype length (TKL), 
and asymmetry indexes (A1, A2) of the studied taxa.

Taxon 2n Ploidy level
Karyotype 

formula

Chromosome 
length range 

(μm)
TKL (μm) A1 A2

A. spicigera 1 18 2x 1M+5m+3sm 4,94-5,56 46,72 0,27 0,04
A. spicigera 2 18 2 x 2M+5m+2sm 4,26-4,81 40,79 0,23 0,02
A. spicigera 3 18 2 x 1M+6m+2sm 4,64-5,14 43,02 0,24 0,04
A. spicigera 4 18 2 x 1M+6m+2sm 4,69-4,97 43,40 0,25 0,02
A. spicigera 5 18 2 x 2M+6m+1sm 4,55-5,50 42,28 0.26 0,03
A. spicigera 6 18 2 x 3M+4m+2sm 4,42-5,25 41,40 0,22 0,03
A. spicigera 7 18 2 x 1M+4m+4sm 4,34-5,33 44,50 0,28 0,04
A. taurica 1 36 4 x 3M+13m+2sm 3,48-4,07 67,31 0,22 0,05
A. taurica 2 36 4 x 4M+12m+2sm 4,57-5,51 92,47 0,25 0,05
A. taurica 3 36 4 x 4M+11m+3sm 4,44-5,50 89,70 0,23 0,06
A. fragrans 1 36 4 x 3M+10m+5sm 4,10-5,35 85,51 0,35 0,08
A. fragrans 2 36 4 x 3M+11m+4sm 3,13-3,53 59,52 0,24 0,01
A. fragrans 3 36 4 x 2M+14m+2sm 3,40-3,94 66,85 0,25 0,05
A. fragrans 4 36 4 x 2M+10m+6sm 4,81-6,29 100,08 0,26 0,07
A. fragrans 5 36 4 x 1M+14m+3sm 3,97-4,65 77,57 0,27 0,05
A. fragrans 6 34 4 x 3M+12m+2sm 3,98-4,89 75,78 0,20 0,07
A. fragrans 7 36 4 x 3M+13m+2sm 3,67-4,14 70,40 0,24 0,04
A. fragrans 8 36 4 x 1M+13m+4sm 3,43-4,75 70,15 0,29 0,08
A. fragrans 9 36 4 x 3M+12m+3sm 3,98-4,99 82,53 0,23 0,07
A. fragrans 10 36 4 x 2M+11m+5sm 3,83-4,79 76,09 0,28 0,07
A. fragrans 11 36 4 x 2M+10m+6sm 3,65-4,51 71,96 0,27 0,06
A. fragrans 12 36 4 x 3M+12m+3sm 3,40-4,49 70,52 0,27 0,08

Figure 2. Somatic metaphase in A. taurica (2n=36), and haploid idiogram (Scale bars: 1 μm).



57The morphological, karyological and phylogenetic analyses of three Artemisia species

The obtained data was uploaded to NCBI and GenBank 
accession numbers were taken. The GenBank accession 
numbers were given in Table 4.

Phylogenetic Analysis

Phylogenetic analysis was conducted using the pro-
gram Molecular Evolutionary Genetics Analysis software 
(MEGA X) (Kumar et al., 2019). In order to evaluate the 
data of chromatograms (sequencing), Finch TV 1.4 ver-
sion is used. DNA sequence alignments of 22 individuals, 
Variable sites, number of parsimony informative sites, 

genetic distance, nucleotide diversity, and divergence 
within species were computed by MEGA X version. DNA 
sequence alignment of all the individuals is made subject 
to statistical analysis within the scope of this program. 
Ultimately, phylogenetic trees were constructed by Maxi-
mum Parsimony Method with 100 bootstrap replicates 
(Nei and Kumar, 2000; Kumar et al., 2019).

RESULTS

Morphological results

It was observed that A. taurica and A. fragrans spe-
cies had a larger size compared to A. spicigera species in 
accordance with the environmental conditions it grows 
and the number of chromosomes and ploidy levels. 
Detailed morphological measurements of the studied 
species are as in Table 5.

Karyological results

A. spicigera K.Koch
This taxa general spread is the Eastern Anatolia 

Region in Turkey. Samples were collected from three 
populations and 6 individuals of three different locali-
ties (Table 1). The samples were labelled “P.Y. 5007-5008-
5009-5013-5022-5024”. The number of chromosomes 
in all the samples examined was 2n=2x=18 and it con-
sists of 4M, 10m and 4sm chromosomes. The metaphase 
chromosome length is 1.46–3.06 μm and longest to 
shortest chromosome ratio is 2.0:1. Chromosome arm 
ratios are 1.28–2.27 μm, the centromeric index is 30.55–
43.83 μm, and relative lengths are 4.20–8.78 μm (Table 
2, Figure 1,). Secondary structures and satellite chromo-
somes (sat-chromosome) were not observed in this spec-
imens.

A. taurica Willd.
The species A. taurica shows the wide distribution in 

the steppes of Central, Eastern and Southeastern Anato-
lia in Turkey. Samples were collected from 6 individuals 
of three different localities (Table 1). The samples were 
labelled “P.Y. 5004-5027-5028”. The number of chromo-
somes in all the samples examined was 2n=4x=36 and it 
consists of 2M, 14m and 2sm chromosomes. The meta-
phase chromosome length is 3.40–3.94 μm. Chromo-
some arm ratios are 1.27–2.57 μm, the centromeric index 
is 33.09–49.20 μm, and relative lengths are 5.08–5.89 μm 
(Table 2, Figure 2). Secondary structures and satellite 
chromosomes (sat-chromosome) were not observed in 
this specimens.

Table 3. The base sequences of the primers used (Taberlet et al., 
1991).

Primers Base sequences (5’ – 3’)

ITS 5 (F): 5’ GAA AGT AAA AGT CGT AAC AAG G 3’
ITS 4 (R): 5’ TCC TCC GCT TAT TGA TAT GC 3’
trn a (F): 5’ CAT TAC AAA TGC GAT GCT CT 3’
trn d (R): 5’ GGG GAT AGA GGA CTT GAA C 3’

Table 4. GenBank accession numbers for the rDNA ITS (ITS1-5.8S-
ITS2) and trnT-trnL3’ regions of the studied samples

Specimens
GenBank Accesion Numbers

ITS region trnT-trnL3’ region

Artemisia fragrans 1 MT159779 MT648006
Artemisia fragrans 2 MT159780 MT648007
Artemisia fragrans 3 MT159781 MT648008
Artemisia fragrans 4 MT159782 MT648009
Artemisia fragrans 5 MT159783 MT648010
Artemisia fragrans 6 MT159784 MT648011
Artemisia fragrans 7 MT159785 MT648012
Artemisia fragrans 8 MT159786 MT648013
Artemisia fragrans 9 MT159787 MT648014
Artemisia fragrans 10 MT159788 MT648015
Artemisia fragrans 11 MT159789 MT648016
Artemisia fragrans 12 MT159790 MT648017
Artemisia spicigera 1 MT159791 MT648018
Artemisia spicigera 2 MT159792 MT648019
Artemisia spicigera 3 MT159793 MT648020
Artemisia spicigera 4 MT159794 MT648021
Artemisia spicigera 5 MT159795 MT648022
Artemisia spicigera 6 MT159796 MT648023
Artemisia spicigera 7 MT159797 MT648024
Artemisia taurica 1 MT159798 MT648025
Artemisia taurica 2 MT159799 MT648026
Artemisia taurica 3 MT159800 MT648027



58 Pelin Yilmaz Sancar, Semsettin Civelek, Murat Kursat

A. fragrans Willd.
This taxa only spread is the Eastern Anatolia Region 

in Turkey and this species a new record for Turkey (Kur-
sat et al., 2014). Samples were collected from five popula-
tions and 14 individuals of four different localities (Table 
1). The samples were labelled “P.Y. 5001-5002-5003-5005-
5006-5010-5011-5012-5016-5017-5019-5020-5021-5023”. 
The number of chromosomes in all the samples exam-
ined was 2n=4x=36 and it consists of 4M, 10m and 4sm 
chromosomes. The metaphase chromosome length is 
1.46–3.06 μm and longest to shortest chromosome ratio 

is 2.0:1. Chromosome arm ratios are 1.28–2.27 μm, 
the centromeric index is 30.55–43.83 μm, and relative 
lengths are 4.20–8.78 μm (Table 2, Figure 3). Secondary 
structures and satellite chromosomes (sat-chromosome) 
were not observed in this specimens.

Phylogenetic results

In this part of the study, a phylogenetic tree display-
ing the phylogenetic position of three Artemisia species 

Table 5. Comparison in terms of key features that distinguish of the species of A. spicigera, A. taurica and A. fragrans 

Characters A. spicigera A. fragrans A. taurica 

Stem length (cm) 20–50 20-75 20–45(–60) 
Dimensions lower leaves (cm) 0.5–2.5 × 0.3–1.5 2.5-4 × 1–2 1–2.5 × 0.5–1.2 
Dimensions of cauline leaves (cm) 0.5–1.5 × 0.3–1.5 1-2.5 × 0.5–1.5 0.5–2.5 × 0.3–1 
Dimensions of floral leaves (cm) 0.1–1 × 0.1–0.2 0.1–1.2 × 0.1–0.8 0.1–1 × 0.1–0.4 
Orientation of synflorescence branches usually horizontal usually ascendant usually horizontal
Capitula length (mm) 1–3 mm long 1–5 mm long (1–) 3–5 mm long, 
Outer phyllaries dimensions (mm) 0.2–0.4 × 0.2–0.4 0.5–0.8 × 0.3–0.5 0.6–0.9 × 0.5–0.8 
Middle phyllaries dimensions (mm) 1.2–2.2 × 0.5–1 1–1.2 × 0.8–1.5 1–2.2 × 1.3–1.7 
Inner phyllaries dimensions (mm) 3–3.4 × 0.5–1 3.3–3.8 × 1–1.2 4–4.2 × 1.2–1.5 
Corolla colour yellow or red yellow or red yellow or pinkish red or purplish red
Corolla dimensions (mm) 2.5–3.2 × 0.5–0.8 1.7–3.5 × 0.2–0.6 2.8–3.3 × 0.5–1 
Pistil length (mm) 1.8–3 2.1–3.2 3.1–3.9 
Ovarium dimensions (mm) 0.4–0.6 × 0.2–0.4 0.5–0.8 × 0.3–0.6 0.7–1 × 0.2–0.7 
Style length (mm) 1.2–1.6 1.5–1.9 1.5–2.2 
Forks length of bifid stigma (mm) 0.2–0.5 0.3–0.7 0.4–0.7 
Stamens length (mm) 2.2–3.2 3–3.5 3–4.2 
Filaments length (mm) 0.8–1.3 1.3–1.6 1–1.5 
Anhters dimensions (mm) 1.4–1.7 × 0.1–0.3 2–2.5 × 0.2–0.5 2–2.7 × 0.1–0.3 
Number of flowers in capitula 3-5 5-8(-10)
Achenes (cypselas) dimensions (mm) 1.2–2.2 × 0.5–1.2 2–2.5 × 0.8–1.4 1.8–2.7 × 0.8–1.4 
Somatic chromosome number 2n=2x=18 2n=4x=36 2n=4x=36 , 2n=6x=54 

Figure 3. Somatic metaphase in A. fragrans (2n=36), and haploid idiogram (Scale bars: 1 μm).



59The morphological, karyological and phylogenetic analyses of three Artemisia species

with respect to each other was constructed (Figure 4). 
Populations of these species were collected from 9 differ-
ent regions cultivated in Van Lake around and 22 indi-
viduals were included in the analyzes. İn addition to, 
the reference base sequences of two individuals belong 
to species A. sieberi (KJ004347.1) and A. maritima 
(NC045093.1) were also included in our analysis to dem-
onstrate the accuracy of the study (Shahzadi et.al., 2020.) 
Haplocarpa scaposa (EU846325.1 and DQ444824) was 
used as an outgroup (McKenzie et.al. 2006; McKenzie 
and Barker 2008). Sequence data of plants used as out-
group and sister group were taken from NCBI. 

Within the scope of the studies, DNA isolation 
of 22 individuals from leaf tissue was made by CTAB 
method, then rDNA ITS (ITS1-5.8S-ITS2) region and 
non-coding trnT-trnL3’ region of cpDNA was ampli-
fied in PCR using specific primers (Table 2). The base 
sequences of the obtained regions were analyzed and 
their genetic characteristics were compared and infor-
mation was obtained about the proximity and distance 
of taxa to each other. For a more accurate visualization 
of the results of the alignment, about 50-100 base from 
the head and the end were not evaluated by us. As a 
result of the research done from NCBI for Artemisia 
genus, the base length of the ITS (ITS1-5.8S-ITS2) region 
was found to be 700-750 bp, trnT-trnL3’ in total and the 
base length was 900-1000 bp in total, and in our study, it 
was found to be of similar length in accordance with the 
literature. 

The analyses were performed with the X version of 
the MEGA program and the method that would give the 
best result for us was selected from the “Find Best DNA 

Models” step of the program. As a result, it was decided 
that Maximum Parsimony method would give the most 
accurate result of the tree drawn with Tamura 3-param-
eter step. In addition, two different DNA regions were 
evaluated at the same time and a complex tree has been 
obtained to achieve a more accurate result (Figure 4).

As a result of the calculations made with the Maxi-
mum Parsimony (MP) method, in both the separate 
and co-evaluations of the sequences of the ITS and trn 
regions of the examined individuals, in total ~1745 base 
pairs were taken into consideration and the number 
of variable regions (V) 204, The number of conserved 
regions (C) was 1507 parsimony number (PI) 34, and 
GC ratio was 41.6%. These calculated values are given in 
Table 6. 

DISCUSSION

Artemisia is one of the most complex genera and it 
is represented by the large number of species, diverse 
morphological types, ploidy and complicated genetic 
relationships (Winward and Mcarthur 1995). Because 
of this, the clarification of the genus’s taxonomy using 
classical botanical tools and morphological characteris-
tics has many difficulties (Torrel et al., 1999). Therefore, 

Table 6. PCR amplified region length and summary statistics from 
the rDNA ITS (ITS1-5.8S-ITS2) and the cpDNA (trnT-trnL3’) data-
set of genus Artemisia.

Molecular 
Diversity 
Parameters

ITS (ITS1-5.8S-
ITS2) Region

trnT-trnL3’ 
Region

Co-evaluated of 
ITS (ITS1-5.8S-
ITS2) and trnT-
trnL3’ Regions

Total Sample 
Count

22 22 22

Total Characters ~725 ~1020 ~1745
GC Ratio (%) 52.7 34.3 41.6
Protected 
Regions (C)

577 930 1507

Regions with 
Variation (V)

142 62 204

Parsimony 
Informative 
Regions (Pi)

14 20 34

Figure 4. Maximum Parsimony tree obtained from the co-eval-
uation of sequences of the ITS (ITS1-5.8S-ITS2) and trnT-trnL3’ 
regions of individuals.



60 Pelin Yilmaz Sancar, Semsettin Civelek, Murat Kursat

usage of molecular markers and caryological data is a 
valuable and promising addition to the traditional mor-
phology-based classification (Turuspekov et al., 2018). In 
this study a phylogenetic systematic study is conducted 
by using the morphological, karyological and phyloge-
netic data of three species in Artemisia that grow around 
the Van Lake in Turkey. 22 individuals of taken from 8 
different populations belong to taxa of the A. spicigera, 
A. taurica and A. fragrans were examined morphologi-
cal measurements, karyotype analysis and analysing the 
base slice of the regions being obtained, it was tried to 
get information about the closeness and distance of taxa 
with each other. This research is important as it is the 
first molecular based study relating with some Artemisia 
species growing naturally that around the Van Lake in 
Turkey. Additionally, the first molecular data about these 
species from Turkey has been submitted to the GenBank 
international databases. 

A lot of research has been carried out to better 
understand the morphological, karyological, anatomical, 
and phylogenetic analysis of the genus Artemisia and its 
relationships to the other (four) subgenera, Absinthium, 
Dracunculus (Besser) Rydb, Seriphidium Besser ex Less. 
and Tridentatae (Rydb), in different parts of the world. 
Polyploidy is currently considered a prominent force in 
plant evolution and represents the most common mode 
of sympatric speciation in plants (Wendel and Doyle 
2005). Polyploids, moreover, may have superior levels 
of adaptability and higher probabilities of survival than 
their diploid relatives (Thompson and Lumaret 1992; 
Soltis and Soltis 2000). Most of the Artemisia that colo-
nize extreme and arid habitats are polyploids. This fact 
supports the hypothesis that polyploids have more tol-
erance of extreme environmental conditions (Pellicer et 
al., 2007).

Chromosome data currently available show poly-
ploidy to be the most significant evolutionary trend in 
chromosome number within Asteraceae (Chehregani et 
al., 2010). Accordig to Chehregani et al. (2010), the high-
est variation in chromosome number was observed in A. 
spicigera. In this species; different chromosome numbers 
(2n=2x=18, 2n=3x=27, 2n=4x=36, 2n=5x=45, 2n=6x=54 
and 2n= 8x= 72) were identified in different populations 
that collected from different parts of Iran. However, in 
our study, the number of chromosomes in all studied 
populations was found to be 2n=2x=18. But Tabur et 
al. (2014), the number of chromosomes in all A. spicig-
era populations they work from Turkey have recorded as 
2n=2x=18. Accordingly, the ploidy level of A. spicigera 
kind in Turkey, we can say that 2x. 

The phylogenetic relationship among the differ-
ent Artemisia species collected from different regions 

of Pakistan based on the chloroplast gene RPS11 was 
investigated by Mahmood et al. (2011). The molecular 
phylogenetic analyses of the Hawaiian Artemisia and its 
worldwide divergence based on nuclear and chloroplast 
DNA markers were reported by Hobbs and Baldwin. 
(2013). As discussed by Haghighi et al. (2014), the phy-
logenetic relationships among Artemisia species based 
on nuclear ITS and chloroplast psbA-trnH DNA mark-
ers using three sections of Artemisia, Dracunculus and 
Serphidium propose that the ITS and cpDNA psbA-trnH 
markers are practicable in the systematic revision of 
troubled taxa at the intra-genus level in plants. Further-
more, Pellicer et al. (2014) performed phylogenetic anal-
ysis of the annual Artemisia within its major lineages 
and suggested that annual Artemisia have been specially 
misidentified at a subgeneric level and verified that they 
are phylogenetically restricted to basal grades. However, 
to date, very few Artemisia species have been verified 
with molecular phylogenetic studies based on the nucle-
otide sequence data in Turkey (Koloren et al., 2016).

Civelek et al. (2010) have carried out a revisionary 
study of the genus Artemisia in Turkey. According to 
results of the revisionary study based on the morpho-
logical features, it was observed that growing around 
the Lake Van that in the populations thought to belong 
to the A. spicigera species, there are some groups show-
ing significant morphological differences from this spe-
cies. These groups were found to be similar to A. spicig-
era and A. taurica in terms of morphological, but it has 
been accepted that they were closer to A. spicigera. In 
these populations, a new variety (A. spicigera var. van-
ensis) belonging to the species A. spicigera was made, 
but the variety was not certain as it was not published 
(nomen nudum). The researchers stated that they are 
not sure about the accuracy of this systematic arrange-
ment and stated that these populations should be stud-
ied in detail. To solve this systematic problems, in Flora 
of Turkey specified to be very close to each other A. spi-
cigera and A. taurica species of, planned to investigate 
detailed morphological and cytogenetic aspects and the 
research was conducted. While these studies continue, 
after literature search and cytogenetic observations in 
these populations, have been identified as belonging to 
the species A. fragrans case a new record for the flora 
of Turkey and published (Kursat et al., 2014). However, 
it has been stated that a molecular study is needed to 
confirm these results. For this purpose, it was decided to 
phylogenetically evaluate the populations of A. spicigera, 
A. taurica and A. fragrans species around the Van Lake 
with various molecular markers. gramer In molecular 
studies, ITS (ITS1-5.8S-ITS2) in rDNA and trn regions 
in cpDNA were amplified with specific primers and ana-



61The morphological, karyological and phylogenetic analyses of three Artemisia species

lyzed with MEGA program. In the phylogenetic family 
tree created after the analysis, it was observed that the 
examined individuals of the species in question were 
completely separated from each other, and the individ-
uals of each species were grouped among themselves. 
According to these results, it has been determined that 
there is no gene flow between the populations of these 
species and they are completely independent from each 
other. According to the morphological and caryological 
data, it has been molecularly proven that the populations 
considered as A. spicigera var. vanensis (nomen nudum) 
are correct to be published as A. fragrans species. 

CONCLUSIONS

According to this study results, it has been found 
that there is complete speciation genetic isolation mech-
anism between the species A. spicigera, A. taurica and A. 
fragrans that inhibit gene flow. Also A.fragrans and A. 
spicigera species are very similar to each other in terms 
of morphological characteristics. However, since popu-
lations of the species A. fragrans are autopolyploid, the 
dimensional values of their morphological squares are 
larger than those of the species A. spicigera.

This study is so important as it is the first molecu-
lar based study relating with some species of Artemisia 
growing naturally in Turkey.

ACKNOWLEDGEMENTS

This work was supported by the Firat University Sci-
entific Research Projects Coordination Unit [grant num-
ber: FF.2090].

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