Abstract
Increased severity of droughts, due to anthropogenic activities and global warming, has imposed a severe threat on agricultural productivity. This has escalated the need for environmentally sustainable solutions to secure global food security. In this context, the application of plant growth-promoting rhizobacteria (PGPR) can be beneficial. PGPR through various mechanisms viz. osmotic adjustments, increased antioxidant activity, phytohormone production, etc., not only ensure the plant’s survival during drought but also augment its growth. Further, due to recent advances in omics technologies, better insights are emerging for PGPR, which facilitates the exploration of genes that are responsible for plant tissue colonization. This review extensively discusses the various mechanisms of PGPR in drought stress resistance; we have also summarized the recent molecular and omics-based approaches for elucidating the role of drought-responsive genes. The manuscript comprises the in-depth mechanistic approach along with designing the PGPR-based bioinoculants to combat drought stress and a possible flowchart for increasing their efficacy.
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References
Agrawal R, Satlewal A, Varma A (2015) Characterization of plant growth-promoting rhizobacteria (PGPR): a perspective of conventional versus recent techniques. In: Heavy Metal Contamination of Soils. Springer, pp 471–485. https://doi.org/10.1007/978-3-319-14526-6_23
Akhtar N, Ilyas N, Hayat R, Yasmin H, Noureldeen A & Ahmad P (2021) Synergistic effects of plant growth promoting rhizobacteria and silicon dioxide nano-particles for amelioration of drought stress in wheat. Plant Physiol. Biochem.
Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheat show major differences in response to drought stress. Funct Integr Genomics 15:587–598. https://doi.org/10.1007/s10142-015-0453-0
Alavi P, Starcher MR, Zachow C, Muller H, Berg G (2013) Root microbe systems: the effect and mode of interaction of stress protecting agent SPA Stenotrophomonas rhizophila DSM14405T. Front Plant Sci 4:141. https://doi.org/10.3389/fpls.2013.00141
Ali S, Hayat K, Iqbal A, **e L (2020) Implications of abscisic acid in the drought stress tolerance of plants. Agronomy 10:1323. https://doi.org/10.3390/agronomy10091323
Anis M, Zaki MJ, Dawar S (2012) Development of a Na alginate based bioformulation and its use in the management of charcoal rot of sunflower Helianthus annuus L. Pak J Bot 44:1167–1170
Anjum SA, Ashraf U, Tanveer M, Khan I, Hussain S, Shahzad B, Zohaib A, Abbas F, Saleem MF, Ali I (2017) Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front. Plant Sci. 8.https://doi.org/10.3389/fpls.2017.00069
Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric actinomycetes for various in vitro and in vivo plant growth promoting PGP traits and for agroactive compounds. Front Microbiol 7:1334. https://doi.org/10.3389/fmicb.2016.01334
Armada E, Roldan A, Azcon R (2014) Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microb Ecol 67:410–420. https://doi.org/10.1007/s00248-013-0326-9
Arora NK, Mehnaz S, Balestrini R (2016) In Bioformulations: for sustainable agriculture. Springer, Berlin, pp 1–283
Arraes FBM, Beneventi MA, de Sa MEL, Paixao JFR, Albuquerque EVS, Marin SRR, Purgatto E, Nepomuceno AL, Grossi de Sa MF (2015) Implications of ethylene biosynthesis and signaling in soybean drought stress tolerance. BMC Plant Biol 15:1–20. https://doi.org/10.1186/s12870-015-0597-z
Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp containing ACC Deaminase partially eliminates the effects of drought stress on growth yield and ripening of pea Pisum sativum L. Pedosphere 18:611–620. https://doi.org/10.1016/S1002-0160(08)60055-7
Aryal JP, Sapkota TB, Khurana R, Khatri-Chhetri A, Jat ML (2019) Climate change and agriculture in South Asia Adaptation options in small holder production systems. Environ Dev Sustain 22:5045–5075. https://doi.org/10.1007/s10668-019-00414-4
Azmat A, Yasmin H, Hassan MN et al (2020) Co application of bio-fertilizer and salicylic acid improves growth photosynthetic pigments and stress tolerance in wheat under drought stress. PeerJ 8:e9960
Bandurska H (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol Plant 27:379–386. https://doi.org/10.1007/s11738-005-0015-5
Bao G, Ashraf U, Wang C, He L, Wei X, Zheng A, Mo Z, Tang X (2018) Molecular basis for increased 2 acetyl 1 pyrroline contents under alternate wetting and drying AWD conditions in fragrant rice. Plant Physiol Biochem 133:149–157. https://doi.org/10.1016/j.plaphy.2018.10.032
Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A (2017) Plant growth promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 161:502–514. https://doi.org/10.1111/ppl.12614
Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum plant relationships physiological molecular agricultural and environmental advances. Can J Microbiol 50:521–577. https://doi.org/10.1139/w04-035
Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI (2009) Rhizosphere bacteria containing 1-aminocyclopropane 1 carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol 181:413–423. https://doi.org/10.1111/j.1469-8137.2008.02657.x
Bhat MA, Wani IA, Dar FL, Farooq I, Bhatti F, Koser R, Rahman S, Jan AT (2020) Mechanistic insights of the interaction of plant growth-promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front. Microbiol. 11. https://doi.org/10.3389/fmicb.2020.01952
Borlee B, Goldman A, Murakami K, Samudrala R, Wozniak D, Parsek M (2010) Pseudomonas aeruginosa uses a cyclic di GMP regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75:827–842. https://doi.org/10.1111/j.1365-2958.2009.06991.x
Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503. https://doi.org/10.1007/s00253-004-1696-1
Bresson J, Vasseur F, Dauzat M, Labadie M, Varoquax F, Touraine B, Vile D (2014) Interact to survive Phyllobacterium brassicacearum improves Arabidopsis tolerance to severe water deficit and growth recovery. PLoS ONE 7(9):e107607. https://doi.org/10.1371/journal.pone.0107607
Brunetti C, Savi T, Nardini A, Loreto F, Gori A, Centritto M (2020) Changes in abscisic acid content during and after drought are related to carbohydrate mobilization and hydraulic recovery in poplar stems. Tree Physiol 40:1043–1057. https://doi.org/10.1093/treephys/tpaa032
Cardinale M, Ratering S, Suarez C, Zapata Montoya AM, Geissler-Plaum R, Schnell S (2015) Paradox of plant growth promotion potential ofrhizobacteria and their actual promotion effect on growth of barley Hordeum vulgare L under salt stress. Microbiol Res 181:22–32. https://doi.org/10.1016/j.micres.2015.08.002
Cardoso AA, Gori A, Da-Silva CJ, Brunetti C (2020) Abscisic acid biosynthesis and signaling in plants: key targets to improve water use efficiency and drought tolerance. Appl Sci 10:6322. https://doi.org/10.3390/app10186322
Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Hassen AI, Labuschagne N (2020) Rhizobacteria induced systemic tolerance against drought stress in Sorghum bicolor L Moench. Microbiol Res 232:126388. https://doi.org/10.1016/j.micres.2019.126388
Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum Inoculation Mitigates Water Stress Effects in Maize Seedlings. Cereal Res Commun 30:343–350. https://doi.org/10.1007/BF03543428
Chang WS, Van de Mortel M, Nielsen L, de Guzman GN, Li X, Halverson LJ (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water limiting conditions. J Bacteriol 189:8290–8299. https://doi.org/10.1128/jb.00727-07
Chi F, Yang P, Han F, **g Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874
Chiappero J, del Rosario CL, Alderete LGS, Palermo TB, Banchio E (2019) Plant growth promoting rhizobacteria improve the antioxidant status in Mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content. Ind Crops Prod 139:111553. https://doi.org/10.1016/j.indcrop.2019.111553
Cho SM, Kang BR, Kim YC (2013) Transcriptome analysis of induced systemic drought tolerance elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana. Plant Pathol 29:209–220. https://doi.org/10.5423/PPJ.SI.07.2012.0103
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 Microbr Interact 21:1067–1075. https://doi.org/10.1094/MPMI-21-8-1067
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. https://doi.org/10.1111/ppl.12221
Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botanique 87:455–462
Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species production scavenging and signaling. Plant Signal Behav 3:156–165
Dangi S, Tirado Corbalá R, Gerik J, Hanson B (2017) Effect of long term continuous fumigation on soil microbial communities. Agronomy 7:37. https://doi.org/10.3390/agronomy7020037
Danish S, Zafar ulHye M, Mohsin F, Hussain M (2020) ACC deaminase producing plant growth promoting rhizobacteria and biochar mitigate adverse effects of drought stress on maize growth. PLoS ONE 15:e0230615. https://doi.org/10.1371/journal.pone.0250286
Davis RF, Earl HJ, Timper P (2014) Effect of simultaneous water deficit stress and Meloidogyne incognita infection on cotton yield and fiber quality. J. Nematol. 46:108. PMID: 24987162; PMCID: PMC4077171.
Defez R, Andreozzi A, Bianco C (2017) The overproduction of indole 3 acetic acid IAA in endophytes upregulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microb Ecol 74:441–452. https://doi.org/10.1007/s00248-017-0948-4
Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157:361–379. https://doi.org/10.1111/j.1744-7348.2010.00439.x
Durán P, Acuña JJ, Armada E, López Castillo OM, Cornejo P, Mora ML, Azcón R (2016) Inoculation with selenobacteria and arbuscular mycorrhizal fungi to enhance selenium content in lettuce plants and improve tolerance against drought stress. J Soil Sci Plant Nutr 16:201–225. https://doi.org/10.4067/S0718-95162016005000017
El-Beltagi HS, Mohamed HI, Sofy MR (2020) Role of ascorbic acid glutathione and proline applied as singly or in sequence combination in improving chickpea plant through physiological change and antioxidant defense under different levels of irrigation intervals. Molecules 25:1702. https://doi.org/10.3390/molecules25071702
Enebe MC, Babalola OO (2018) The influence of plant growth promoting rhizobacteria in plant tolerance to abiotic stress a survival strategy. Appl Microbiol Biotechnol 102:7821–7835. https://doi.org/10.1007/s00253-018-9214-z
FAO (2021) The impact of disasters and crises on agriculture and food security: 2021. Rome.
Finkel OM, Salas Gonzalez I, Castrillo G, Conway JM, Law TF, Teixeira PJPL, Wilson ED, Fitzpatrick CR, Jones CD, Dangl JL (2020) A single bacterial genus maintains root growth in a complex microbiome. Nature 587:103–108. https://doi.org/10.1038/s41586-020-2778-7
Gadhave KR, Devlin PF, Ebertz A, Ross A, Gange AC (2018) Soil inoculation with Bacillus spp modifies root endophytic bacterial diversity evenness and community composition in a context specific manner. Microb Ecol 76:741–750. https://doi.org/10.1007/s00248-018-1160-x
Glodowska M, Husk B, Schwinghamer T, Smith D (2016) Biochar is a growth promoting alternative to peat moss for the inoculation of corn with a pseudomonad. Agron Sustain Dev 36:21. https://doi.org/10.1007/s13593-016-0356-z
Glodowska M, Schwinghamer T, Husk B, Smith D (2017) Biochar based inoculants improve soybean growth and nodulation. Agric Sci 8:1048–1064. https://doi.org/10.4236/as.2017.89076
Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M, Mirzaei M, Amirkhani A, Jorrin-Novo JV, Salekdeh GH (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J Proteomics 94:289–301. https://doi.org/10.1016/j.jprot.2013.09.017
Ghanbari F, Kordi S (2019) Hardening pretreatment by drought and low temperature enhanced chilling stress tolerance of cucumber seedlings. Acta Sci Pol Hortorum Cultus 18:29–37. https://doi.org/10.24326/asphc.2019.2.4
Ghasemlou F, Amiri H, Karamian R, Mirzaie-asl A (2019) Alleviation of the effects of on drought stress Verbascum nudicuale by methyl jasmonate and titanium dioxide nanoparticles. Iran J Plant Physiol 9:2911–2920
Gorim L, Asch F (2012) Effects of composition and share of seed coatings on the mobilization efficiency of cereal seeds during germination. J Agron Crop Sci 198:81–91. https://doi.org/10.1111/j.1439-037X.2011.00490.x
Guterman, L. Distortions to agricultural incentives in Colombia; Agricultural Distortions Working Paper Series No. 1856–2016–152637; Word Bank, December 2007. Available online: https://ideas.repec.org/p/ags/wbadwp/
48392.html (accessed on 5 September 2020).
Hafez EM, Alsohim AS, Farig M, Omara AE-D, Rashwan E, Kamara MM (2019) Synergistic effect of Biochar and plant growth promoting Rhizobacteria on alleviation of water deficit in rice plants under salt affected soil. Agronomy 9:847. https://doi.org/10.3390/agronomy9120847
Harsanyi E, Bashir B, Alsilibe F et al (2021) Impact of agricultural drought on sunflower production across Hungary. Atmosphere 12:1339
Hasanuzzaman M, Bhuyan MHM, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466
Huang B, DaCosta M, Jiang Y (2014) Research advances in mechanisms of turfgrass tolerance to abiotic stresses from physiology to molecular biology. Crit Rev Plant Sci 33:141–189
Husain T, Fatima A, Suhel M, Singh S, Sharma A, Prasad SM, Singh VP (2020) A brief appraisal of ethylene signaling under abiotic stress in plants. Plant Signal Behav 15:1782051. https://doi.org/10.1080/15592324.2020.1782051
Ilyas N, Mumtaz K, Akhtar N, Yasmin H, Sayyed RZ, Khan W, Enshasy HAE, Dailin DJ, Elsayed EA, Ali Z (2020) Exopolysaccharides producing bacteria for the amelioration of drought stress in wheat. Sustainability 12:8876. https://doi.org/10.3390/su12218876
IPCC (2018) Global warming of 1.5° C: an IPCC special report on the impacts of global warming of 1.5° C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. Intergovernmental Panel on Climate Change,
Kakar KU, Ren XL, Nawaz Z et al (2016) A consortium of rhizobacterial strains and biochemical growth elicitors improve cold and drought stress tolerance in rice Oryza sativa L. Plant Biol 18:471–483
Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH (2019) The inherent conflicts in develo** soil microbial inoculants. Trends Biotechnol 37:140–151. https://doi.org/10.1016/j.tibtech.2018.11.011
Kang SM, Khan AL, Waqas M, You YH, Kim H, Kim J-G, Hamayun M, Lee IJ (2014a) 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. https://doi.org/10.1080/17429145.2014.894587
Kang SM, Radhakrishnan R, Khan AL, Kim MJ, Park JM, Kim BR, Shin DH, Lee IJ (2014b) Gibberellin secreting rhizobacterium Pseudomonas putida H 2 3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84:115–124. https://doi.org/10.1016/j.plaphy.2014.09.001
Karimi N, Goltapeh EM, Amini J, Mehnaz S, Zarea MJ (2020) Effect of Azospirillum zeae and Seed Priming with Zinc Manganese and Auxin on Growth and Yield Parameters of Wheat under Dryland Farming. Agric Res 10:44–55. https://doi.org/10.1007/s40003-020-00480-5
Kaushal M (2019) Microbes in cahoots with plants MIST to hit the jackpot of agricultural productivity during drought. Int J Mol Sci 20:1769. https://doi.org/10.3390/ijms20071769
Khan A, Pan X, Najeeb U, Tan DKY, Fahad S, Zahoor R, Luo H (2018) Co** with drought: stress and adaptive mechanisms, and management through cultural and molecular alternatives in cotton as vital constituents for plant stress resilience and fitness. Biol. Res. 51. https://doi.org/10.1186/s40659-018-0198-z
Khan N, Ali S, Tariq H et al (2020a) Water conservation and plant survival strategies of rhizobacteria under drought stress. Agronomy 10:1683
Khan N, Bano A, Ali S, Babar MA (2020b) Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses. Plant Growth Regul 90:189–203. https://doi.org/10.1007/s10725-020-00571-x
Khan N, Mishra A, Chauhan PS, Nautiyal CS (2011) Induction of Paenibacillus lentimorbus biofilm by sodium alginate and CaCl2 alleviates drought stress in chickpea. Ann Appl Biol 159:372–386. https://doi.org/10.1111/j.1744-7348.2011.00502.x
Khan ZS, Rizwan M, Hafeez M, Ali S, Javed MR, Adrees M (2019) The accumulation of cadmium in wheat Triticum aestivum as influenced by zinc oxide nanoparticles and soil moisture conditions. Environ Sci Pollut Res 26:19859–19870. https://doi.org/10.1007/s11356-019-05333-5
Kumar M, Kesawat MS, Ali A, Lee S-C, Gill SS, Kim HU (2019) Integration of abscisic acid signaling with other signaling pathways in plant stress responses and development. Plants 8:592. https://doi.org/10.3390/plants8120592
Lopez-Galiano MJ, Garcia-Robles I, Gonzalez-Hernandez AI, Camanes G, Vicedo B, Real MD, Rausell C (2019) Expression of miR159 is altered in tomato plants undergoing drought stress. Plants 8:201. https://doi.org/10.3390/plants8070201
Lally RD, Galbally P, Moreira AS, Spink J, Ryan D, Germaine KJ, Dowling DN (2017) Application of endophytic Pseudomonas fluorescens and a bacterial consortium to Brassica napus can increase plant height and biomass under greenhouse and field conditions. Front Plant Sci 8:2193. https://doi.org/10.3389/fpls.2017.02193
Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166. https://doi.org/10.3390/plants4010112
Leinauer B, Serena M, Singh D (2010) Seed coating and seeding rate effects on turfgrass germination and establishment. HortTechnology 20:179–185. https://doi.org/10.21273/HORTTECH.20.1.179
Li S, Zhou L, Addo-Danso SD, Ding G, Sun M, Wu S, Lin S (2020a) Nitrogen supply enhances the physiological resistance of Chinese fir plantlets under polyethylene glycol PEG induced drought stress. Sci Rep 10:1–8. https://doi.org/10.1038/s41598-020-64161-7
Li X, Shi W, Broughton K, Smith R, Sharwood R, Payton P, Bange M, Tissue DT (2020) Impacts of growth temperature water deficit and heat waves on carbon assimilation and growth of cotton plants Gossypium hirsutum L. Environ Exp Bot 179:104204. https://doi.org/10.1016/j.envexpbot.2020.104204
Liang C, Wang W, Wang J, Ma J, Li C, Zhou F, Zhang S, Yu Y, Zhang L, Li W (2017) Identification of differentially expressed genes in sunflower Helianthus annuus leaves and roots under drought stress by RNA sequencing. Bot Stud 58:1–11. https://doi.org/10.1186/s40529-017-0197-3
Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201–208. https://doi.org/10.5423/PPJ.SI.02.2013.0021
Liu P, Xu Z-S, Pan-Pan L, Hu D, Chen M, Li L-C, Ma Y-Z (2013) A wheat PI4K gene whose product possesses threonine autophosphorylation activity confers tolerance to drought and salt in Arabidopsis. J Exp Bot 64:2915–2927. https://doi.org/10.1093/jxb/ert133
Mahmood A, Turgay OC, Farooq M, Hayat R (2016) Seed biopriming with plant growth promoting rhizobacteria: a review. FEMS Microbiol. Ecol. 92. https://doi.org/10.1093/femsec/fiw112
Mai VC (2020) Antioxidative Response of Glycine max L Merr cv Namdan to Drought Stress. Indian J Agric Res 54:656–660. https://doi.org/10.18805/IJARe.A-524
Marasco R, Rolli E, Vigani G, Borin S, Sorlini C, Ouzari H, G Z Daffonchio D (2013) Are drought resistance promoting bacteria cross-compatible with different plant models. Plant Signal Behav 8:e26741. https://doi.org/10.4161/psb.26741
Martinez-Cortes T, Pomar F, Merino F, Novo-Uzal E (2014) A proteomic approach to Physcomitrella patens rhizoid exudates. J Plant Physiol 171:1671–1678. https://doi.org/10.1016/j.jplph.2014.08.004
Marulanda A, Barea JM, Azcon R (2009) Stimulation of plant growth and drought tolerance by native microorganisms AM fungi and bacteria from dry environment. Mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. https://doi.org/10.1007/s00344-009-9079-6
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530. https://doi.org/10.1016/j.plantsci.2003.10.025
Meena M, Swapnil P, Divyanshu K, Kumar S, Tripathi YN, Zehra A, Marwal A, Upadhyay RS (2020) PGPR mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: Current perspectives. J Basic Microbiol 60:828–861. https://doi.org/10.1002/jobm.202000370
Mirzaei M, Ladan Moghadam A, Hakimi L, Danaee E (2020) Plant growth promoting rhizobacteria PGPR improve plant growth antioxidant capacity and essential oil properties of lemongrass Cymbopogon citratus under water stress. Plant Physiol 10:3155–3166
Moreno-Galván AE, Cortés-Patiño S, Romero-Perdomo F, Uribe-Vélez D, Bashan Y, Bonilla RR (2020) Proline accumulation and glutathione reductase activity induced by drought-tolerant rhizobacteria as potential mechanisms to alleviate drought stress in Guinea grass. Appl Soil Ecol 147:103367. https://doi.org/10.1016/j.apsoil.2019.103367
Naylor D, DeGraaf S, Purdom E, Coleman-Derr D (2017) Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J 11:2691–2704. https://doi.org/10.1038/ismej.2017.118
Niu X, Song L, **ao Y, Ge W (2018) Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front Microbiol 8:2580. https://doi.org/10.3389/fmicb.2017.02580
Nordstedt NP, Chapin LJ, Taylor CG, Jones ML (2020) Identification of Pseudomonas Spp that increase ornamental crop quality during abiotic stress. Front Plant Sci 10:1754. https://doi.org/10.3389/fpls.2019.01754
O’ Callaghan M, (2016) Microbial inoculation of seed for improved crop performance issues and opportunities. Appl Microbiol Biotechnol 100:5729–5746. https://doi.org/10.1007/s00253-016-7590-9
Oliveira RS, Rocha I, Ma Y, Vosatka M, Freitas H (2016) Seed coating with arbuscular mycorrhizal fungi as an ecotechnological approach for sustainable agricultural production of common wheat Triticum aestivum L. J Toxicol Environ Health Part A 79:329–337. https://doi.org/10.1080/15287394.2016.1153448
Ortiz-Castro R, Campos-García J, López-Bucio J (2020) Pseudomonas putida and Pseudomonas fluorescens influence Arabidopsis root system architecture through an auxin response mediated by bioactive cyclodipeptides. J Plant Growth Regul 39:254–265. https://doi.org/10.1007/s00344-019-09979-w
Ortiz N, Armada E, Duque E, Roldan A, Azcon R (2015) Contribution of arbuscular mycorrhizal fungi and or bacteria to enhancing plant drought tolerance under natural soil conditions effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96. https://doi.org/10.1016/j.jplph.2014.08.019
Pande V, Pandey SC, Sati D, Pande V, Samant M (2020) Bioremediation: an emerging effective approach towards environment restoration. Environ Sustain 3:91–103. https://doi.org/10.1007/s42398-020-00099-w
Pedrini S, Merritt DJ, Stevens J, Dixon K (2017) Seed coating: science or marketing spin. Trends Plant Sci 22:106–116. https://doi.org/10.1016/j.tplants.2016.11.002
Perdomo JA, Capo-Bauca S, Carmo-Silva E, Galmes J (2017) Rubisco and Rubisco activase play an important role in the biochemical limitations of photosynthesis in rice wheat and maize under high temperature and water deficit. Front Plant Sci 8:490. https://doi.org/10.3389/fpls.2017.00490
Pirasteh-Anosheh H, Saed-Moucheshi A, Pakniyat H & Pessarakli M (2016) Stomatal responses to drought stress. Water stress and crop plants:24–40. doi: https://doi.org/10.1002/9781119054450.ch33
Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208. https://doi.org/10.1016/j.ecoenv.2014.03.014
Quastel JH (1953) Krilium and synthetic soil conditioners. Nature 171:7–10. https://doi.org/10.1038/171007a0
Raheem A, Shaposhnikov A, Belimov AA, Dodd IC, Ali B (2018) Auxin production by rhizobacteria was associated with improved yield of wheat Triticum aestivum L under drought stress. Arch Agron Soil Sci 64:574–587. https://doi.org/10.1080/03650340.2017.1362105
Ramakrishna W, Yadav R, Li K (2019) Plant growth promoting bacteria in agriculture two sides of a coin. Appl Soil Ecol 138:10–18. https://doi.org/10.1016/j.apsoil.2019.02.019
Rani A, Devi P, Jha UC, Sharma KD, Siddique KHM, Nayyar H (2020) Develo** climate-resilient chickpea involving physiological and molecular approaches with a focus on temperature and drought stresses. Front Plant Sci 10:1759
Rashid U, Yasmin H, Hassan MN et al. (2021) Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep.:1–21.
Ravanbakhsh M, Sasidharan R, Voesenek LACJ, Kowalchuk GA, Jousset A (2018) Microbial modulation of plant ethylene signaling ecological and evolutionary consequences. Microbiome 6:1–10. https://doi.org/10.1186/s40168-018-0436-1
Ren Z, Zhang D, Cao L, Zhang W, Zheng H, Liu Z, Han S, Dong Y, Zhu F, Liu H, Su H (2020) Functions and regulatory framework of ZmNST3 in maize under lodging and drought stress. Plant Cell Environ 43:2272–2286. https://doi.org/10.1111/pce.13829
Rivera-Ferre MG (2020) From agriculture to food systems in the IPCC. Glob Change Biol 26:2731–2733
Rocha FR, Papini-Terzi FS, Nishiyama MY et al (2007) Signal transduction-related responses to phytohormones and environmental challenges in sugarcane. BMC Genom 8:1–22
Rocha I, Ma Y, Vosátka M, Freitas H, Oliveira RS (2019) Growth and nutrition of cowpea Vigna unguiculata under water deficit as influenced by microbial inoculation via seed coating. J Agron Crop Sci 205:447–459. https://doi.org/10.1111/jac.12335
Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F (2014) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. https://doi.org/10.1111/1462-2920.12439
Ruiz de La Cruz G, Aguirre Mancilla CL, Godinez Garrido NA, Osornio Flores NM, Torres Castillo JA (2017) Chitosan mixed with beneficial fungal conidia or fungicide for bean Phaseolus vulgaris l seed coating. Interciencia 42:307–312
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 8:1–16. https://doi.org/10.1038/s41598-018-21921-w
Saleem AR, Brunetti C, Khalid A, Della Rocca G, Raio A, Emiliani G, De Carlo A, Mahmood T, Centritto M (2018) Drought response of Mucuna pruriens (L.) DC. inoculated with ACC deaminase and IAA producing rhizobacteria. PLoS One 7: e0191218. https://doi.org/10.1371/journal.pone.0191218
Salehi-Lisar SY, Bakhshayeshan-Agdam H (2016) Drought stress in plants: causes, consequences, and tolerance. In: Drought Stress Tolerance in Plants, Vol 1. Springer, pp 1–16. https://doi.org/10.1007/978-3-319-28899-4_1
Salleh MS, Nordin MS, Puteh AB (2020) Germination performance and biochemical changes under drought stress of primed rice seeds. Seed Sci Technol 48:333–343. https://doi.org/10.15258/sst.2020.48.3.02
Salomon MV, Bottini R, de Souza Filho GA, Cohen AC, Moreno D, Gil M, Piccoli P (2014) Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine. Physiol Plant 151:359–374. https://doi.org/10.1111/ppl.12117
Samant M, Pandey SC, Pandey A (2018) Impact of hazardous waste material on environment and their management strategies. In: Microbial biotechnology in environmental monitoring and cleanup. IGI Global, pp 175–192. doi:https://doi.org/10.4018/978-1-5225-3126-5.ch011
Sati D, Pandey SC, Pande V, Upreti S, Gouri V, Joshi T, Gangola S, Debbarma P, Pandey A, Samant M (2020) Toward an enhanced understanding of plant growth promoting microbes for sustainable agriculture. In: Recent Advancements in Microbial Diversity. Elsevier, pp 87–112. https://doi.org/10.1016/B978-0-12-821265-3.00005-0
Schlauch KA, Grimplet J, Cushman J, Cramer GR (2010) Transcriptomics analysis methods: microarray data processing, analysis and visualization using the Affymetrix Genechip® Vitis Vinifera genome Array. In: Methodologies and results in grapevine research. Springer, pp 317–334. https://doi.org/10.1007/978-90-481-9283-0_22
Seleiman MF, Al Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, Dindaroglu T, Abdul Wajid HH, Battaglia ML (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10:259. https://doi.org/10.3390/plants10020259
Sen S, Ghosh D, Mohapatra S (2018) Modulation of polyamine biosynthesis in Arabidopsis thaliana by a drought mitigating Pseudomonas putida strain. Plant Physiol Biochem 129:180–188. https://doi.org/10.1016/j.plaphy.2018.05.034
Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B (2015) Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. Mbio 6:e00621-e615. https://doi.org/10.1128/mBio.00621-15
Shobana N, Thangappan S, Uthandi S (2020) Plant growth-promoting Bacillus sp. cahoots moisture stress alleviation in rice genotypes by triggering antioxidant defense system. Microbiol. Res.:126518. https://doi.org/10.1016/j.micres.2020.126518
Silva-Sanchez C, Li H, Chen S (2015) Recent advances and challenges in plant phosphoproteomics. Proteomics 15:1127–1141. https://doi.org/10.1002/pmic.201400410
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141. https://doi.org/10.1023/A:1022556103536
Singh M, Tiwari N (2021) Microbial amelioration of salinity stress in HD 2967 wheat cultivar by up-regulating antioxidant defense. Commun. Integr. Biol. (just-accepted). https://doi.org/10.1080/19420889.2021.1937839
Singh TB, Sahai V, Ali A, Prasad M, Yadav A, Shrivastav P, Goyal D, Dantu PK (2020) Screening and evaluation of PGPR strains having multiple PGP traits from hilly terrain. J Appl Biol Biotechnol 8:38–44. https://doi.org/10.7324/JABB.2020.80406
Smith MR, Veneklaas E, Polania J, Rao IM, Beebe SE, Merchant A (2019) Field drought conditions impact yield but not nutritional quality of the seed in common bean Phaseolus vulgaris L. PLoS One 14:e0217099
Sonbarse PP, Kiran K, Sharma P, Parvatam G (2020) Biochemical and molecular insights of PGPR application for the augmentation of carotenoids tocopherols and folate in the foliage of Moringa oleifera. Phytochemistry 179:112506. https://doi.org/10.1016/j.phytochem.2020.112506
Steiner Fb, Zuffo AM, Zoz T, Zoz A, Zoz J (2017) Drought tolerance of wheat and black oat crops at early stages of seedling growth. Rev Cienc Agrar 40:576–586. https://doi.org/10.19084/RCA16118
Stocker T (2014) Climate change 2013: the physical science basis: Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge university press,
Sukweenadhi J, Kim YJ, Choi ES, Koh SC, Lee SW, Kim YJ, Yang DC (2015) Paenibacillus yonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum drought, and salt stress. Microbiol Res 172:7–15. https://doi.org/10.1016/j.micres.2015.01.007
SzablińskaPiernik J, Lahuta LB (2020) Metabolite profiling of semi leafless pea Pisum sativum L under progressive soil drought and subsequent re watering. J Plant Physiol 256:153314. https://doi.org/10.1016/j.jplph.2020.153314
Takahashi F, Kuromori T, Urano K, Yamaguchi-Shinozaki K, Shinozaki K (2020) Drought stress responses and resistance in plants: From cellular responses to long distance intercellular communication. Front Plant Sci 11:1407
Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson A-C (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49. https://doi.org/10.3389/fpls.2017.00049
Tsujimoto T, Sato H, Matsushita S (1999) Hydration of seeds with partially hydrated super absorbent polymer particles. Google Patents.
Ullah A, Manghwar H, Shaban M, Khan AH, Akbar A, Ali U, Ali E, Fahad S (2018) Phytohormones enhanced drought tolerance in plants: a co** strategy. Environ Sci Pollut Res 25:33103–33118. https://doi.org/10.1007/s11356-018-3364-5
Vilchez JI, Garcia Fontana C, Roman Naranjo D, Gonzalez Lopez J, Manzanera M (2016) Plant drought tolerance enhancement by trehalose production of desiccation tolerant microorganisms. Front Microbiol 7:1577. https://doi.org/10.3389/fmicb.2016.01577
Vandana UK, Rajkumari J, Singha LP, Satish L, Alavilli H, Sudheer PDVN, Chauhan S, Ratnala R, Satturu V, Mazumder PB (2021) The endophytic microbiome as a hotspot of synergistic interactions with prospects of plant growth promotion. Biology 10:101. https://doi.org/10.3390/biology10020101
Vandana UK, Singha B, Gulzar ABM, Mazumder PB (2020) Molecular mechanisms in plant growth promoting bacteria (PGPR) to resist environmental stress in plants. In: Molecular Aspects of Plant Beneficial Microbes in Agriculture. Elsevier, pp 221–233. https://doi.org/10.1016/B978-0-12-818469-1.00019-5
Vargas L, de Carvalho TLG, Ferreira PCG, Baldani VLD, Baldani JI, Hemerly AS (2012) Early responses of rice Oryza sativa L seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant Soil 356:127–137. https://doi.org/10.1007/s11104-012-1274-8
Vargas L, Santa Brigida AB, Mota Filho JP, De Carvalho TG, Rojas CA, Vaneechoutte D, Van Bel M, Farrinelli L, Ferreira PCG, Vandepoele K (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus a transcriptomic view of hormone pathways. PLoS ONE 9:e114744. https://doi.org/10.1371/journal.pone.0114744
Verma KK, Wu KC, Singh P, Malviya MK, Singh RK, Song XP, Li YR (2019) The protective role of silicon in sugarcane under water stress photosynthesis and antioxidant enzymes. Biomed J Sci Tech Res 15:002685. https://doi.org/10.26717/BJSTR.2019.15.002685
Vorholt JA, Vogel C, Carlstrom CI, Muller DB (2017) Establishing causality opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22:142–155. https://doi.org/10.1016/j.chom.2017.07.004
Vosatka M, Latr A, Gianinazzi S, Albrechtova J (2012) Development of arbuscular mycorrhizal biotechnology and industry current achievements and bottlenecks. Symbiosis 58:29–37. https://doi.org/10.1007/s13199-012-0208-9
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:25–35. https://doi.org/10.3390/molecules14072535
Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth promoting and biocontrol activity of Streptomyces spp as endophytes. Int J Mol Sci 19:952. https://doi.org/10.3390/ijms19040952
Wang C, Linderholm HW, Song Y, Wang F, Liu Y, Tian J, Xu J, Song Y, Ren G (2020) Impacts of drought on maize and soybean production in northeast China during the past five decades. Int J Environ Res Public Health 17:2459. https://doi.org/10.3390/ijerph17072459
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:e52565. https://doi.org/10.1371/journal.pone.0052565
Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome wide temporal spatial gene expression profiling of drought responsiveness in rice. BMC Genom 12:1–15
Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth promoting rhizobacteria Pseudomonas fluorescens FPT9601 T5 in Arabidopsis. Mol Plant Microbe Interact 18:385–396
Wang Y, Qiu L, Song Q, Wang S, Wang Y, Ge Y (2019) Root proteomics reveals the effects of wood vinegar on wheat growth and subsequent tolerance to drought stress. Int J Mol Sci 20:943. https://doi.org/10.3390/ijms20040943
Wang Z, Gerstein M, Snyder M (2009) RNA Seq a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. https://doi.org/10.1038/nrg2484
Wiegmann M, Maurer A, Pham A et al (2019) Barley yield formation under abiotic stress depends on the interplay between flowering time genes and environmental cues. Sci Rep 9:1–16
Wu Y, Ma L, Liu Q et al (2020) The plant growth promoting bacteria promote cadmium uptake by inducing a hormonal crosstalk and lateral root formation in a hyperaccumulator plant Sedum alfredii. J Hazard Mater 395:122661
Yaseen R, Aziz O, Saleem MH, Riaz M, Zafar ulHye M, Rehman M, Ali S, Rizwan M, Nasser Alyemeni M, El Serehy HA, Al Misned FA (2020) Ameliorating the drought stress for wheat growth through application of ACC deaminase containing rhizobacteria along with biogas slurry. Sustainability 12:6022. https://doi.org/10.3390/su12156022
Yasmin H, Bano A, Wilson NL et al. (2021)a Drought-tolerant Pseudomonas sp. showed differential expression of stress-responsive genes and induced drought tolerance in Arabidopsis thaliana. Physiol. Plant. n/a.
Yasmin H, Nosheen A, Naz R, Bano A, Keyani R (2017) L tryptophan assisted PGPR mediated induction of drought tolerance in maize Zea mays L. J Plant Interact 12:567–578
Yasmin H, Nosheen A, Naz R, Keyani R & Anjum S (2019) Regulatory role of rhizobacteria to induce drought and salt stress tolerance in plants. Field Crops: Sustainable Management by PGPR, pp 279–335. Springer.
Yasmin H, Rashid U, Hassan MN et al (2021b) Volatile organic compounds produced by Pseudomonas pseudoalcaligenes alleviated drought stress by modulating defense system in maize Zea mays L. Physiol Plant 172:896–911
Yi Y, de Jong A, Frenzel E, Kuipers OP (2017) Comparative transcriptomics of Bacillus mycoides strains in response to potato-root exudates reveals different genetic adaptation of endophytic and soil isolates. Front Microbiol 8:1487. https://doi.org/10.3389/fmicb.2017.01487
Yu J, Jiang M, Guo C (2019) Crop pollen development under drought: from the phenotype to the mechanism. Int J Mol Sci 20:1550. https://doi.org/10.3390/ijms20071550
Zaheer MS (2019) Effect of Plant Growth Promoting Rhizobacteria (PGPR) and Cytokinins on the Growth and Yield of Wheat (Triticum aestivum L.) under drought. Islamia University, Bahawalpur. http://173.208.131.244:9060/xmlui/handle/123456789/2261
Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851. https://doi.org/10.1007/s00425-007-0530-2
Zhang J, Zhang S, Cheng M et al (2018) Effect of drought on agronomic traits of rice and wheat A meta analysis. Int J Environ Res Public Health 15:839
Zhong Y, Yang Y, Liu P, Xu R, Rensing C, Fu X, Liao H (2019) Genotype and rhizobium inoculation modulate the assembly of soybean rhizobacterial communities. Plant Cell Environ 42:2028–2044. https://doi.org/10.1111/pce.13519
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The authors are thankful to the Department of Zoology, Kumaun University, SSJ Campus, Almora (Uttarakhand), India, and DST FIST grant SR/FST/LS-I/2018/131 for providing the facility for this research work.
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D.S. and V.P. conceived and designed the study; D.S., V.P., and S.C.P. prepared figures and contributed to writing the manuscript; M.S. reviewed the manuscript.
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Sati, D., Pande, V., Pandey, S.C. et al. Recent Advances in PGPR and Molecular Mechanisms Involved in Drought Stress Resistance. J Soil Sci Plant Nutr 23, 106–124 (2023). https://doi.org/10.1007/s42729-021-00724-5
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DOI: https://doi.org/10.1007/s42729-021-00724-5