Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         44 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  44 

Op e n  Ac c e s s  
F u l l  L e n g t h  A r t i c l e  

Study of the Modulating Interactions of Multitrait 

Rhizobacteria Using Zea Mays L. as the Host Plant  

Sana Shakeel, Ambreen Ahmed*, Ifrah Javaid 

Department of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan 

A B S T R A C T  

Background: Rhizosphere is a soil region closest to roots of the plants inhabiting different types of microorganisms including 

rhizobacteria. Chemical fertilizers which are conventionally used for increasing crop production are dangerous in terms of minimizing 

the nutritional value of crops and may also be hazardous for biological agents. Therefore, the use of Plant Growth Promoting 

Rhizobacteria (PGPR) are favorable for improved crop production over chemical fertilizers. 

Objectives: The current study highlights the growth promoting traits of bacterial isolates through isolation of rhizospheric bacterial 

strains from different plants. 

Methodology: In this study, ten rhizospheric bacterial isolates were used, which were morpho-physiologically characterized and 

then tested for plant growth-promoting traits i.e., HCN production, ammonification and auxin production. Most of the bacterial strains 

gave positive results for these plant growth-promoting traits. To study the beneficial effects of these bacteria on plants, plant-

microbial interaction assay was conducted using Zea mays.  

Results: Results revealed that these bacteria enhanced the growth as compared to control plants. Bacterial isolates Streptomyces 

lydicus (Cn6), Staphylococcus aureus (Cn7) and Bacillus pumilus (PP3) showed strong ammonia producing effects. The isolates 

Bacillus subtilis (Cn2), PP2 and PP5 exhibited strong potential of HCN production whereas only Streptomyces lydicus (Cn6) and 

Bacillus pumilus (PP3) were observed to be auxin producers. A maximum increase in fresh weight of the plants was observed in 

treatment with PP2 showing 94.36% increase over controls. Cn1 showed an increase (26.12%) in shoot length while Cn5 revealed a 

prominent increase (64.95%) in root length compared to the control plant. The isolates Cn5 and Cn4 showed improvement in the 

total chlorophyll content of the treated plants with a percentage increase of 100% and 99.82%, respectively compared to the control. 

Conclusion: In conclusion, these PGPR may be further used in agriculture research for growth improvement. 

Keywords  

Rhizobacteria, PGP, plant-microbial 
interaction assay, PGPR, Zea mays.   

*Address of Correspondence 
ambreenahmed1@hotmail.com 

Article info. 
Received: October 10, 2018 
Accepted: October 30, 2019 

Cite this article: Shakeel S, Ahmed A, Javaid I. Study of the Modulating Interactions of 
Multitrait Rhizobacteria Using Zea Mays L. as the Host Plant. RADS J Biol Res Appl Sci. 2019; 
10(2):44-53. 
This is an Open Access article distributed under the terms of the Creative Commons Attribution License 
(http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in 
any medium, provided the original work is properly cited. 

Funding Source: Nil 
Conflict of Interest: Nil 

I N T R O D U C T I O N  

The relationship between species is frequently defined via 

the influence of associations and interactions among 

species. Plants live in an association with a rich variety of 

microorganisms throughout their development. These 

associations relate to plant-microbe interactions from 

mutualism to parasitism, on account of the role of 

symbionts1. Different groups of bacteria and fungi interact 

with higher plants. While studying plants and microbes, 

rhizosphere is a critical segment of soil. In plants, the 

rhizosphere is a multifarious and diverse environment 

occupied by numerous microbes2. The root colonizing 

bacteria are known as rhizospheric bacteria3. 

Different species of rhizobacteria that flourish in the 

rhizosphere are able to stimulate plant growth by different 

O R I G I N A L  A R T I C L E  



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         45 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  45 

mechanisms and are collectively known as plant growth-

promoting rhizobacteria/rhizospheric bacteria (PGPR)4. In 

the past few years, the number of PGPR that has been 

recognized has shown a significant increase, largely 

because the part of rhizosphere in an ecosystem has 

attained prominence in the working of the biosphere. 

Many species of bacteria like Azospirillum, Azotobacter, 

Pseudomonas, Enterobacter, Serratia, Klebsiella, 

Burkholderia, Alcaligenes, Arthrobacter and Bacillus 

species have been testified to increase plant growth5. 

Whenever the roots are inoculated with a PGPR, reduced 

growth rate of the primary roots and increased number 

and/or length of lateral roots may be observed6. 

Accordingly, through improved uptake of water and 

minerals, the growth of the whole plant can be 

augmented. A number of these effects, including 

augmented root and shoot biomass, are also 

acknowledged for PGPR-inoculated plants growing in 

soil7,8. PGPR amend RSA and the assembly of roots, 

chiefly via their capability to meddle with the plant 

hormonal balance9. 

PGPR utilization meets the current need to lessen 

nitrogen input to achieve better sustainability in the 

production of crops, predominantly cereals10. Maize (Zea 

mays L.) is one of the major crops all over the globe 

reserving the mounting claim for food and cultivated 

animals feed11. Exhaustive corn production requires broad 

consumption of pesticides as well as chemical fertilizers, 

which have harmful effects on the soil, water and on the 

food chain. It has been verified that although chemical 

fertilizers improve the crop yield, they cause toxic effects 

too, for instance soil acidification as well as production of 

the greenhouse gas, nitrous oxide (N2O) by denitrification 

on ecosystems12,13. It has been reported that one possible 

mode to reduce the harmful environmental impacts 

ensuing from continuous utilization of chemical fertilizers 

is inoculation with biofertilizers such as PGPR14. Several 

findings have revealed that PGPR are latent growth 

enhancers in numerous crops15. 

The present study deals with four already isolated and 

identified bacterial strains [Bacillus subtilis (Cn2), 

Streptomyces lydicus (Cn6), Staphylococcus aureus 

(Cn7) and Bacillus pumilus (PP3)] and isolation of six 

rhizospheric bacterial strains from plants Convolvulus 

arvensis and Polygonum plebium collected from 

Balochistan, highlighting the growth promoting traits of 

bacterial isolates. These bacterial isolates were then used 

to inoculate the seeds of Zea mays and various 

parameters of treated and non-treated plants were 

studied regarding plant growth improvement. 

M A T E R I A L S  A N D  M E T H O D S  

Sample Collection 

For the isolation of bacteria, Convolvulus arvensis and 

Polygonum plebeium plants were collected from the Zhob 

district of Balochistan (Table 1).  

Isolation and Characterization of Bacteria  

Six bacterial strains were isolated from the rhizosphere of 

the collected plant using the serial dilution method (Table 

1). The isolates were routinely grown on L-Agar (Luria 

Agar) or L-Broth (Luria Bertani Broth). The cultures were 

purified by repeated streaking on L-Agar medium.  

All the bacterial strains including four already isolated and 

identified strains [Bacillus subtilis (Cn2), Streptomyces 

lydicus (Cn6), Staphylococcus aureus (Cn7) and Bacillus 

pumilus (PP3)] were characterized morphologically and 

physiologically. Culture characteristics as well as cell 

morphology was observed. To examine bacterial 

physiology, growth curve, temperature and pH, the 

studies were conducted following the research of Fatima 

and Ahmed16. 

Plant Growth-Promoting Traits 

To determinate plant growth-promoting traits, tests for 

ammonification, HCN production and auxin production 

were performed following the research of Cappuccino and 

Sherman17; Lorck18 and Ahmed and Hasnain19. 

Plant-Microbe Interactions 

Ten strains were used in the plant-microbe interaction 

experiment and their effect on plant growth was observed 

by recording various growth parameters following the 

study by Fatima and Ahmed16. The experiment was 

repeated thrice. 

Statistical Analysis 

The data obtained were statistically analyzed using the 

software SPSS v. 16. 



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         46 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  46 

R E S U L T S  

Isolation and Characterization of Bacteria 

For rhizospheric soil samples, Convolvulus arvensis and 

Polygonum plebeium plants were collected from the Zhob 

district of Balochistan. Six bacterial strains were isolated 

from the rhizosphere of the selected plants through the 

serial dilution method and were used for further study 

including four already isolated strains [Bacillus subtilis 

(Cn2), Streptomyces lydicus (Cn6), Staphylococcus 

aureus (Cn7) and Bacillus pumilus (PP3)]. Different 

bacterial isolates showed different colony size, shape, 

color, texture, elevation, margin and growth. Bacterial 

isolates Cn1, Bacillus subtilis (Cn2), Cn4, Staphylococcus 

aureus (Cn7) and PP5 showed irregular shape; Cn5, 

Streptomyces lydicus (Cn6), PP2 and Bacillus pumilus 

(PP3) were round in shape, while only PP4 possessed 

filamentous shape. All the bacterial isolates were gram 

+ve and except for Cn1, Bacillus pumilus (PP3), PP4 and 

PP5, all were cocci (Table 1). 

For physiological characterization, growth curve, 

temperature test and pH studies were performed. The 

growth curve revealed that all the strains gave optimal 

growth after 24 and 48 hours of incubation whereas a 

significant decline was observed after 72 and 96 hours of 

incubation. Bacterial strains Bacillus subtilis (Cn2), Cn5, 

Staphylococcus aureus (Cn7) and PP5 showed maximum 

growth after 24 hours of incubation while maximum 

growth of strains Cn1, Streptomyces lydicus (Cn6), Cn4, 

PP2, Bacillus pumilus (PP3) and PP4 was observed after 

48 hours of incubation (Figure 1). The temperature test 

showed that all the strains gave optimal growth at 37ºC 

temperature while bacterial growth was observed to 

decrease at 25 ºC and 45 ºC, respectively (Figure 2). All 

the strains showed different behavior towards different pH 

ranges from 5, 6, 7, 8 and 9. Optimum pH for growth of 

bacterial isolate PP2 was pH5. On the other hand, the 

bacterial strains Cn1, Bacillus subtilis (Cn2), Cn5 and 

Streptomyces lydicus (Cn6) showed maximum growth at 

pH7, Staphylococcus aureus (Cn7) at pH8, while Cn4 and 

PP5 showed maximum growth at pH9 (Figure 3). 

Plant Growth-Promoting Traits 

All the bacterial isolates showed positive ammonification 

test except for Cn5 and PP4. Only Streptomyces 

lydicus (Cn6) bacterial strain gave negative results for 

HCN production whereas all other strains were HCN 

producers. On the other hand, only bacterial strains 

Streptomyces lydicus (Cn6) and Bacillus pumilus (PP3) 

were auxin producers while rest of the strains showed 

negative results for auxin production (Table 1). 

 

Figure 1. Growth curve of bacterial strains in L-Broth medium for different intervals of time (24, 48, 72 and 96 hours). 



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         47 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  47 

 

Figure 2. Growth of bacterial strains grown in L-Broth medium at different temperatures (25, 37 and 45oC). 

 

Figure 3. Growth of bacterial strains in L-Broth medium with pH range (5, 6, 7, 8 and 9). 



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

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Table 1. Morphological characterization of bacterial isolates. 

 

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Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         49 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  49 

Plant-Microbe Interactions 

To determine beneficial interactions between plants and 

microbes, PMI assay was done. Zea mays seeds were 

inoculated with the bacterial strains (Cn1, Bacillus subtilis 

(Cn2), Cn4, Cn5, Streptomyces lydicus (Cn6), 

Staphylococcus aureus (Cn7), PP2, Bacillus pumilus 

(PP3), PP4 and PP5) and growth parameters of plants 

e.g., fresh weight, shoot length and root length were 

noted to estimate the growth promotional potential of 

these strains. Considerable increase in fresh weight of 

plants was observed in strains PP2, Cn1, Cn5, Cn4 and 

Streptomyces lydicus (Cn6) showing 94.36, 74.50, 74.21, 

70.41, and 65.03% increase respectively as compared to 

control (Figure 4). Treatment with strains namely Cn1, 

Cn5, Bacillus subtilis (Cn2) and PP2 showed significant 

percentage increase in shoot length of up to 26.12, 23.23, 

21.37 and 21.0% respectively over control. But the two 

strains Bacillus pumilus (PP3) and PP5 showed 

percentage decrease in shoot length over control (Figure 

5). A careful study demonstrated that some bacterial 

strains namely Cn5, Streptomyces lydicus (Cn6), Bacillus 

subtilis (Cn2), Cn4 and PP4 showed significant 

percentage increase in root length of upto 64.95, 64.60, 

53.22, 50.74 and 50.39% respectively, compared to 

control (Figure 5). 

Analysis of chlorophyll ‘a’, ‘b’ and total chlorophyll content 

was done. Few strains namely Cn5, Cn4, Streptomyces 

lydicus (Cn6) and PP2 showed significant percentage 

increase in chlorophyll ‘a’ of upto 100, 99.9, 82.80 and 

80.99% respectively, then non-inoculated control plants. 

Four strains namely Cn5, Cn4, Streptomyces 

lydicus (Cn6) and PP2 showed maximum chlorophyll ‘b’ 

concentration in treated plants with percentage increase 

of 100, 99.72, 82.84 and 80.95% respectively over 

control. Bacterial strains namely Cn5, Cn4, Streptomyces 

lydicus (Cn6) and PP2 showed maximum total chlorophyll 

content in treated plants with a percentage increase of 

100, 99.82, 82.81 and 80.96% respectively over control. 

Exceptionally, Bacillus subtilis (Cn2) showed percentage 

decrease in chlorophyll (a, b and total chlorophyll) 

concentration over control (Figure 6). 

 

 

Figure 4. Effect of bacterial inoculations on the fresh weight of Zea mays under laboratory conditions. Data represent 

mean of twelve replicates. Different letters indicate significant differences between treatments using Duncan’s multiple 

range test (P=0.05) (C=Control). 



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

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Figure 5. Effect of bacterial inoculations on shoot/root length of Zea mays under laboratory conditions. Data represent 

mean of twelve replicates. Different letters indicate significant differences between treatments using Duncan’s multiple 

range test (P=0.05) (C=Control). 

 

 

Figure 6. Effect of bacterial inoculations on chlorophyll ‘a’ of Zea mays under laboratory conditions. Data represent the 

mean of three replicates. Different letters indicate significant differences between treatments using Duncan’s multiple 

range test (P=0.05) (C=Control). 



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         51 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  51 

D I S C U S S I O N  

The current study focused on determining the plant 

growth-promoting potential of rhizobacteria isolated from 

the rhizosphere of Convolvulus arvensis and Polygonum 

plebeium collected from mountainous region of the Zhob 

district of Balochistan including four already isolated and 

identified strains. As Balochistan is not an agricultural 

land so our purpose was to develop methods using 

rhizobacteria from Balochistan native plants to enhance 

the productivity of that region.  

In PMI assay, fresh weight, root length and shoot length 

of inoculated and control plants were observed. A 

maximum increase in fresh weight of plants was observed 

in strains PP2 (94.36%), which was observed to be a 

strong HCN producer and ammonia producer, both of 

which directly and indirectly contributed to an increase in 

growth parameters. In addition, all the treated plants 

showed percentage increase in fresh weight relative to 

control plant (Figure 4). This was due to individual or 

synergistic effects of plant growth-promoting traits of 

rhizobacteria, which modified the uptake of minerals by 

plants8. Similarly the inoculation of Zea mays seeds with 

rhizobacterial strains showed a noteworthy increase in 

shoot length and root length. Cn1, Cn5 and few other 

strains showed a significant percentage increase in shoot 

length. PGPR may help plant growth promotion by using 

their hormones producing ability, nitrogen fixation or even 

phosphate solubilization. They may also affect plant 

metabolism to increase water and minerals uptake, by 

suppressing plant pathogens i.e. through HCN production 

or even by collaborating with other beneficial 

microorganisms4. Balseiro-Romero et al. (2017) and 

many other researchers working on the effect of PGPR on 

growth parameters of various plants reported that shoot 

length increased in their experiments20. The present study 

demonstrated that out of the ten bacterial strains, five 

bacterial strains namely Cn5, Streptomyces lydicus (Cn6), 

Bacillus subtilis (Cn2), Cn4 and PP4 showed considerable 

percentage increase of more than 50% in root length over 

control. Cn5 and PP4 neither produced ammonia nor 

auxin but these were HCN producers and showed 

considerable increase in root length because HCN 

provides indirect mechanism of protection by controlling 

other pathogens.  Moreover, the presence of other plant 

growth-promoting traits may be one of the causes, as 

these may also be siderophore producers and phosphate 

solubilizers21 (Figure 5). Zahid et al. (2015) reported 

similar results of increase in root length in Zea mays after 

bacterial treatment22. 

All the bacterial strains showed increased chlorophyll 

content in inoculated plants than control plants except for 

Bacillus subtilis (Cn2). Actually, the bacterial inoculated 

plants which showed a significant increase in fresh 

weight, and shoot/root length were also rich in chlorophyll 

content over control. PGPR inoculated plants showed 

dark greenish leaves, which were due to an increase in 

chlorophyll content23. It can be assumed that the increase 

in chlorophyll content was due to increased leaf area and 

balanced nutritional uptake from the soil24. Uzair et al. 

(2018) worked on 18 different strains of P. aeruginosa 

isolated from Balochistan and tested these for their plant 

growth-promoting potential and obtained significant 

results25. Sarwar et al. (2014) also worked on PGPR 

isolated from rhizosphere of rice plants of Jafferabad 

district of Balochistan and revealed significant increase in 

plant parameters26. Our results are in accordance with the 

findings of Kamran et al. (2016) who worked on PGPR 

strain i.e., Pseudomonas putida and reported significant 

increase in chlorophyll content of Eruca sativa. They 

revealed that plant growth-promoting bacteria supported 

the defense mechanism to produce various enzymes that 

ultimately increase the chlorophyll content of treated 

plants27,28. 

C O N C L U S I O N  

From the so forth experimental work, it is deduced that 

PGPR are beneficial for the growth promotion of plants. 

Our results revealed that bacteria isolated from plant 

samples, collected from unproductive areas of 

Baluchistan were ammonia producing and possessed the 

ability to produce HCN, an important plant growth 

promoter, while only two bacteria were auxin producers. 

These bacteria were then treated with Zea mays L., which 

showed significant enhancement in plant growth 

parameters including chlorophyll content of plants 

exhibiting beneficial behavior of bacteria towards plant 

traits. Hence, the present study gives an idea to enhance 

plant productivity on such barren lands that can be utilized 

for agricultural purposes.  



Study of the Modulating Interactions of Multitrait Rhizobacteria  Vol. 10 (2), December 2019 

ISSN (Print): 2305 – 8722 ISSN (Online): 2521 – 8573                         52 R A D S  J .  B i o l .  R e s .  A p p l .  S c i .  52 

A C K N O W L E D G E M E N T S  

This work was funded by the grant from the University of 

the Punjab, Quaid-e-Azam Campus, Lahore. 

L I S T  O F  A B B R E V I A T I O N S   

PGPR  Plant Growth Promoting Rhizobacteria 

N2O  Nitrous Oxide 

L- Agar  Luria Agar 

L- Broth  Luria Broth 

R E F E R E N C E S  

1. Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat 
EV, Schulze-Lefert P. Structure and functions of the 
bacterial microbiota of plants. Annu Rev Plant Biol. 
2013; 64:807-38. 

2. Haldar S, Sengupta S. Plant-microbe cross-talk in the 
rhizosphere: insight and biotechnological 
potential. Open Microbiol J. 2015; 9:(1):1-7. 

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