Skip to main content
Log in

Regulation of Drought-Responsive Gene Expression in Glycine max L. Merrill is Mediated Through Pseudomonas simiae Strain AU

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Plant growth promoting rhizobacteria (PGPR) have been described for sustainable agriculture practices as being a vital agent for abiotic and biotic stress mitigation and growth promotion in plants. In the present research, the authors emphasize the role of drought tolerant PGPR namely, Pseudomonas simiae strain AU, in protection of soybean plants by modulating the gene expression profile and phytohormone biosynthesis responsible for drought tolerance in plants. The gene expression analysis confirmed the involvement of transcription factors (DREB/EREB), osmoprotectants (P5CS, GOLS), and water transporters (PIP & TIP), as these genes were up-regulated in P. simiae AU-inoculated plants leading to drought tolerance. In addition, enhanced production of abscisic acid (ABA) and salicylic acid (SA) hormones and reduction of ethylene emission, associated with promoting drought tolerance, was observed in bacterial-inoculated plants in comparison to non-inoculated plants. Higher proline and total soluble sugar contents in AU-inoculated soybean plants also contributed to increased tolerance to drought stress. Overall, P. simiae AU mediated drought-induced expression profiles of stress genes and plant hormones were determined in soybean plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  • Almeida Trapp M, De Souza GD, Rodrigues-Filho E, Boland W, Mithöfer A (2014) Validated method for phytohormone quantification in plants. Front Plant Sci 5:417

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A (2017) Plant growth promoting rhizobacteria enhances wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 161:502–514

    Article  CAS  PubMed  Google Scholar 

  • Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Int 27:349–363

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350

    Google Scholar 

  • Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, Sa T (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8:705

    Article  PubMed  PubMed Central  Google Scholar 

  • Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R, 3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Cho SM, Kang BR, Kim JJ, Kim YC (2012) Induced systemic drought and salt tolerance by Pseudomonas chlororaphis O6 root colonization is mediated by ABA-independent stomatal closure. Plant Pathol 28:202–206

    Article  CAS  Google Scholar 

  • Chrispeels MJ, Maurel C (1994) Aquaporins: the molecular basis of facilitated water movement through living plant cells. Plant Physiol 105:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153:79–90

    Article  CAS  PubMed  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  • García JE, Maroniche G, Creus C, Suárez-Rodríguez R, Ramirez-Trujillo JA, Groppa MD (2017) In vitro PGPR properties and osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiol Res 202:21–29

    Article  CAS  Google Scholar 

  • German MA, Burdman S, Okon Y, Kigel J (2000) Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol Fertil Soil 32:259–264

    Article  Google Scholar 

  • Ghosh D, Sen S, Mohapatra S (2017) Modulation of proline metabolic gene expression in Arabidopsis thaliana under water-stressed conditions by a drought-mitigating Pseudomonas putida strain. Ann Microbiol 67:655–668

    Article  CAS  Google Scholar 

  • Gojło E, Pupel P, Lahuta LB, Podliński P, Kucewicz M, Górecki RJ (2015) The acquisition of desiccation tolerance in developing Vicia hirsuta seeds coincides with an increase in galactinol synthase expression and soluble α-d-galactosides accumulation. J Plant Physiol 184:37–48

    Article  CAS  PubMed  Google Scholar 

  • Grobelak A, Napora A, Kacprzak M (2015) Using plant growth-promoting rhizobacteria (PGPR) to improve plant growth. Ecol Eng 84:22–28

    Article  Google Scholar 

  • Gupta S, Seth R, Sharma A (2016) Plant growth-promoting rhizobacteria play a role as phytostimulators for sustainable agriculture. In: Choudhary DK and others (eds) Plant–microbe interaction: an approach to sustainable agriculture. Springer, Singapore. https://doi.org/10.1007/978-981-10-2854-0_22

    Chapter  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  CAS  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293

    Article  CAS  PubMed  Google Scholar 

  • Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682

    Article  CAS  Google Scholar 

  • Kasotia A, Varma A, Choudhary DK (2015) Pseudomonas-mediated mitigation of salt stress and growth promotion in Glycine max. Agri Res 4:31–41

    Article  CAS  Google Scholar 

  • Khan A, Zhao XQ, Javed MT, Khan KS, Bano A, Shen RF, Sajid M (2016) Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited uptake of Na+. Environ Exp Bot 124:120–129

    Article  CAS  Google Scholar 

  • Kishor K, Polavarapu B, Kumari PH, Sunita MSL, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544

    Google Scholar 

  • Kohler J, Hernández JA, Caravaca F, Roldán A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151

    Article  CAS  Google Scholar 

  • Kumar M, Lee SC, Kim JY, Kim SJ, Kim SR (2014) Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). J Plant Biol 57:383–393

    Article  CAS  Google Scholar 

  • Kumari S, Vaishnav A, Jain S, Choudhary DK, Sharma KP (2016) In vitro screening for salinity and drought stress tolerance in plant growth promoting bacterial strains. Int J Agri Life Sci 2:60–66

    Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  CAS  Google Scholar 

  • Li R, Wang J, Li S, Zhang L, Qi C, Weeda S, Zhao B, Ren S, Guo YD (2016) Plasma membrane intrinsic proteins SlPIP2; 1, SlPIP2; 7 and SlPIP2; 5 conferring enhanced drought stress tolerance in tomato. Sci Rep 6:31814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572

    Article  CAS  Google Scholar 

  • Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A and others (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park Y-G, Mun B-G, Kang S-M, Hussain A, Shahzad R, Seo C-W, and others (2017) Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS ONE 12(3):e0173203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel VK, Srivastava R, Sharma A, Srivastava AK, Singh S, Srivastava AK, Kashyap PL, Chakdar H, Pandiyan K, Kalra A, Saxena AK (2018) Halotolerant Exiguobacterium profundum PHM11 tolerate salinity by accumulating L-Proline and fine-tuning gene expression profiles of related metabolic pathways. Front Microbiol 9:423

    Article  PubMed  PubMed Central  Google Scholar 

  • Rajkumar M, Bruno LB, Banu JR (2017) Alleviation of environmental stress in plants: the role of beneficial Pseudomonas spp. Crit Rev Environ Sci Technol 47:372–407

    Article  Google Scholar 

  • Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK, Saikia R (2018) Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 8:3560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvi P, Saxena SC, Petla BP, Kamble NU, Kaur H, Verma P, Rao V, Ghosh S, Majee M (2016) Differentially expressed galactinol synthase(s) in chickpea are implicated in seed vigor and longevity by limiting the age induced ROS accumulation. Sci Rep 6:35088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selvaraj MG, Ishizaki T, Valencia M, Ogawa S, Dedicova B, Ogata T, Yoshiwara K, Maruyama K, Kusano M, Saito K, Takahashi F, Shinozaki K, Nakashima K, Ishitani M (2017) Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field. Plant Biotechnol J 15:1465–1477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swamy PM, Smith BN (1999) Role of abscisic acid in plant stress tolerance. Curr Sci India 76:1220–1227

    CAS  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought and cold inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Timmusk S, Islam A, Abd El D, Lucian C, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 9:1–13

    Article  CAS  Google Scholar 

  • Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Prasad V, Chauhan PS, Lata C (2017) Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 8:1510

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaishnav A, Jain S, Kasotia A, Kumari S, Gaur RK, Choudhary DK (2013) Effect of nitric oxide signaling in bacterial treated soybean plant under salt stress. Arch Microbiol 195:171–177

    Article  CAS  Google Scholar 

  • Vaishnav A, Jain S, Kasotia A, Kumari S, Gaur RK, Choudhary DK (2014) Molecular mechanism of benign microbe-elicited alleviation of biotic and abiotic stresses for plants. In: Gaur RK, et al. (eds) Approaches to plant stress and their management. Springer, Berlin. https://doi.org/10.1007/978-81-322-1620-9_16

    Chapter  Google Scholar 

  • Vaishnav A, Kumari S, Jain S, Varma A, Tuteja N, Choudhary DK (2016) PGPR-mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J Basic Microbiol 56:1–15

    Article  CAS  Google Scholar 

  • Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195

    Article  CAS  PubMed  Google Scholar 

  • Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Int 6:1–14

    CAS  Google Scholar 

  • Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24

    Article  Google Scholar 

  • Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7:1–10

    Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls A and B, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Phys 144:307–313

    Article  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  Google Scholar 

  • Zahir ZA, Munir A, Asghar HN, Arshad M, Shaharoona B (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963

    CAS  Google Scholar 

  • Zerrouk IZ, Benchabane M, Khelifi L, Yokawa K, Ludwig-Müller J, Baluska F (2016) A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J Plant Physiol 191:111–119

    Article  CAS  PubMed  Google Scholar 

  • Zhang DY, Kumar M, Xu L, Wan Q, Huang YH, Xu ZL, He X-L, Ma J-B, Pandey GK, Shao HB (2017) Genome-wide identification of major intrinsic proteins in Glycine soja and characterization of GmTIP2; 1 function under salt and water stress. Sci rep 7:4106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The research was supported by SERB-Grant No. SR/FT/LS-129/2012 to DKC. Some of the research has partially been supported by DBT Grant No. BT/PR1231/AGR/21/340/2011 to DKC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Devendra Kumar Choudhary.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vaishnav, A., Choudhary, D.K. Regulation of Drought-Responsive Gene Expression in Glycine max L. Merrill is Mediated Through Pseudomonas simiae Strain AU. J Plant Growth Regul 38, 333–342 (2019). https://doi.org/10.1007/s00344-018-9846-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-018-9846-3

Keywords

Navigation