Abstract
Microbes play crucial roles in enhancing plant growth by forming symbiotic relationships, promoting nutrient uptake, and stimulating overall plant health in various habitats. The present study aimed to investigate the role of Piriformospora indica, arbuscular mycorrhiza fungi (AMF), and plant growth-promoting bacteria (PGPB) in alleviating drought stress in the Triticum aestivum HD-2967 cultivar. In a completely randomized design experiment, plants were subjected to different water regimes of 75% and 35% field capacity (FC) under greenhouse conditions. Under different water regimes, microbial inoculation significantly enhanced the morphological, physico-biochemical, and ultrastructural characteristics of the wheat plants. Plants inoculated with PGPB, P. indica, and AMF showed increased shoot and root length, shoot and root biomass, leaf area, photosynthetic rate, transpiration rate, stomatal conductance, and internal CO2 as compared to uninoculated plants under all water regimes. The PGPB, P. indica, and AMF-inoculated wheat plants accumulated higher content of glycine betaine, total sugars, trehalose, proline, putrescine, spermidine, carotenoids, proteins, α-tocopherol, and a decrease in lipid peroxidation, relative membrane permeability, and lipoxygenase enzyme activity as compared to uninoculated plants. Besides, microbes-inoculated wheat plants showed a higher level of antioxidant enzymes viz., superoxide dismutase, catalase, and ascorbate peroxidase than uninoculated plants. Microbial inoculation helped wheat plants to overcome water stress-induced deficiency of macro- (Ca2+, Mg2+, and K+) and micronutrient (Cu, Mn2+, Fe, and Zn2+), and reduced damage to the cell ultrastructure (plasma membrane and chloroplasts). Comparing the potential of microbial inoculants to increase growth and nutritional, biochemical, physiological, and ultrastructural changes, the PGPB-inoculated wheat plants showed greater drought resilience followed by AMF and P. indica inoculated plants.
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Aalipour H, Nikbakht A, Sabzalian MR (2023) Essential oil composition and total phenolic content in Cupressus arizonica G. In response to microbial inoculation under water stress conditions. Sci Rep 13(1):1–11. https://doi.org/10.1038/s41598-023-28107-z
Abbas SR, Ahmad SD, Sabir SM et al (2014) Detection of drought tolerant sugarcane genotypes (Saccharum officinarum) using lipid peroxidation, antioxidant activity, glycine-betaine and proline contents. J soil sci plant nutr 14(1):233–243
Abbas S, Javed MT, Shahid M et al (2020) Acinetobacter sp. SG-5 inoculation alleviates cadmium toxicity in differentially cd tolerant maize cultivars as deciphered by improved physio-biochemical attributes, antioxidants and nutrient physiology. Plant Physiol Biochem 155:815–827. https://doi.org/10.1016/j.plaphy.2020.08.024
Abobatta WF (2019) Drought adaptive mechanisms of plants—a review. Adv Agric Environ Sci 2(1):42–45. https://doi.org/10.30881/aaeoa.00021
Adejumo SA, Oniosun B, Akpoilih OA et al (2021) Anatomical changes, osmolytes accumulation and distribution in the native plants growing on Pb-contaminated sites. Environ Geochem Health 43:1537–1549. https://doi.org/10.1007/s10653-020-00649-5
Aldesuquy HS, Ibraheem FL, Ghanem HE (2018) Exogenously supplied salicylic acid and trehalose protect growth vigor, chlorophylls and thylakoid membranes of wheat flag leaf from drought-induced damage. J Agric For Meteorol Res 1(1):13–20
Ali R, Hassan S, Shah D et al (2020) Role of polyamines in mitigating abiotic stress. Prot Chem Agents Amelior Plant Abiotic Stress: Biochem Mol Perspect 22:291–305. https://doi.org/10.1002/9781119552154.ch13
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Aslani Z, Hassani A, Mandoulakani BA et al (2023) Effect of drought stress and inoculation treatments on nutrient uptake, essential oil and expression of genes related to monoterpenes in sage (Salvia officinalis). Sci Hort 309:111610. https://doi.org/10.1016/j.scienta.2022.111610
Azizi M, Fard EM, Ghabooli M (2021) Piriformospora indica affect drought tolerance by regulation of genes expression and some morphophysiological parameters in tomato (Solanum lycopersicum L). Sci Hort 287:110260. https://doi.org/10.1016/j.scienta.2021.110260
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Begum N, Wang L, Ahmad H et al (2022) Co-inoculation of arbuscular mycorrhizal fungi and the plant growth-promoting rhizobacteria improve growth and photosynthesis in tobacco under drought stress by up-regulating antioxidant and mineral nutrition metabolism. Microb Ecol 83:971–988. https://doi.org/10.1007/s00248-021-01815-7
Bhagat N, Raghav M, Dubey S et al (2021) Bacterial exopolysaccharides: insight into their role in plant abiotic stress tolerance. J Microbiol Biotechnol 31(8):1045–1059. https://doi.org/10.4014/jmb.2105.05009
Bhardwaj AK, Chandra KK, Kumar R (2023) Water stress changes on AMF colonization, stomatal conductance and photosynthesis of Dalbergia sissoo seedlings grown in entisol soil under nursery condition. For Sci Technol 19:1–11. https://doi.org/10.1080/21580103.2023.2167873
Bidalia A, Okram Z, Hanief M et al (2018) Assessment of tolerances in Mitragyna parvifolia (Roxb.) Korth. and Syzygium cumini Keels. seedlings to waterlogging. Photosynthetica 56(2):707–717. https://doi.org/10.1007/s11099-017-0724-1
Birhane E, Bongers F, Damtew A et al (2023) Arbuscular mycorrhizal fungi improve nutrient status of Commiphora myrrha seedlings under drought. J Arid Environ 209:104877. https://doi.org/10.1016/j.jaridenv.2022.104877
Boutasknit A, Baslam M, Ait-El-Mokhtar M et al (2020) Arbuscular mycorrhizal fungi mediate drought tolerance and recovery in two contrasting carob (Ceratonia siliqua L.) ecotypes by regulating stomatal, water relations, and (in) organic adjustments. Plants 9(1):80. https://doi.org/10.3390/plants9010080
Brehelin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266. https://doi.org/10.1016/j.tplants.2007.04.003
Caesar J, Tamm A, Ruckteschler N et al (2018) Revisiting chlorophyll extraction methods in biological soil crusts–methodology for determination of chlorophyll a and chlorophyll a + b as compared to previous methods. Biogeosciences 15(5):1415–1424. https://doi.org/10.5194/bg-15-1415-2018
Cheng H-Q, Giri B, Wu Q-S et al (2022) Arbuscular mycorrhizal fungi mitigate drought stress in citrus by modulating root microenvironment. Arch Agron Soil Sci 68(9):1217–1228. https://doi.org/10.1080/03650340.2021.1878497
Chiappero J, del Rosario Cappellari L, Alderete LG et al (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
de Bang TC, Husted S, Laursen KH et al (2021) The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol 229(5):2446–2469. https://doi.org/10.1111/nph.17074
Devarajan AK, Muthukrishanan G, Truu J et al (2021) The foliar application of rice phyllosphere bacteria induces drought-stress tolerance in Oryza sativa (L.). Plants 10(2):387. https://doi.org/10.3390/plants10020387
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32(1):93–101. https://doi.org/10.1093/jxb/32.1.93
Diatta AA, Min D, Jagadish SK (2021) Drought stress responses in non-transgenic and transgenic alfalfa—current status and future research directions. Adv Agron 170:35–100. https://doi.org/10.1016/bs.agron.2021.06.002
Doderer A, Kokkelink I, Van Der Veen S et al (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 1120(1):97–104. https://doi.org/10.1016/0167-48389290429-h
EN ISO 20483 (2006) AN 300 “the determination of nitrogen according to Kjeldahl. Using block digestion and steam distillation”
Fadiji AE, Santoyo G, Yadav AN et al (2022) Efforts towards overcoming drought stress in crops: revisiting the mechanisms employed by plant growth-promoting bacteria. Front Microbiol 13:962427. https://doi.org/10.3389/fmicb.2022.962427
Farooq MA, Kobayashi WN, Fujita D et al (2009) Plant drought stress: effects, mechanisms and management. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Berlin, pp 153–188
Ferreira JC, Paschoalin VMF, Panek AD et al (1997) Comparison of three different methods for trehalose determination in yeast extract. Food Chem 60(2):251–254. https://doi.org/10.1016/S0308-81469600330-5
Fresno DH, Solé-Corbatón H, Munné‐Bosch S (2023) Water stress protection by the arbuscular mycorrhizal fungus rhizoglomus irregulare involves physiological and hormonal responses in an organ‐specific manner. Physiol Plant 175(1):e13854. https://doi.org/10.1111/ppl.13854
Ghabooli M, Kaboosi E (2022) Alleviation of the adverse effects of drought stress using a desert adapted endophytic fungus and glucose in tomato. Rhizosphere 21:100481. https://doi.org/10.1016/j.rhisph.2022.100481
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70(2):303–307. https://doi.org/10.1007/BF02374789
Gunasekera D, Ratnasekera D (2023) Advancement in mitigating the effects of drought stress in wheat. In: Khan MK, Pandey A, Gezgin S (eds) Abiotic stresses in wheat. Academic Press, Cambridge, pp 297–311
Guo H, Cui YN, Pan YQ et al (2020) Sodium chloride facilitates the secretohalophyte Atriplex canescens adaptation to drought stress. Plant Physiol Biochem 150:99–108. https://doi.org/10.1016/j.plaphy.2020.02.018
Haghighi TM, Saharkhiz MJ, Kavoosi G et al (2023) Adaptation of Glycyrrhiza glabra L. to water deficiency based on carbohydrate and fatty acid quantity and quality. Sci Rep 13(1):1766. https://doi.org/10.1038/s41598-023-28807-6
Harada D, Nagamachi S, Aso K et al (2019) Oral administration of l-ornithine increases the content of both collagen constituting amino acids and polyamines in mouse skin. Biochem Biophys Res Commun 512(4):712–715. https://doi.org/10.1016/j.bbrc.2019.03.147
Hasanuzzaman M, Bhuyan MB, Nahar K et al (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8(3):31. https://doi.org/10.3390/agronomy8030031
Hashem A, Abd-Allah EF, Alqarawi AA et al (2016) Bioremediation of adverse impact of cadmium toxicity on Cassia italica Mill by arbuscular mycorrhizal fungi. Saudi J Biol Sci 23(1):39–47. https://doi.org/10.1016/j.sjbs.2015.11.007
Hashemi M, Behboodian B, Karimi E et al (2022) Azotobacter chroococcum inoculation under low drought stress condition improves Trachyspermum ammi seeds’ essential oil bioactivity. Biochem Syst Ecol 105:104537. https://doi.org/10.1016/j.bse.2022.104537
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198. https://doi.org/10.1016/0003-98616890654-1
Hiscox JD, Israelstam GFA (1979) Method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334. https://doi.org/10.1139/b79-163
Ilyas N, Mumtaz K, Akhtar N et al (2020) Exopolysaccharides producing bacteria for the amelioration of drought stress in wheat. Sustainability 12(21):76–88. https://doi.org/10.3390/su12218876
Inbaraj MP (2021) Plant-microbe interactions in alleviating abiotic stress—a mini review. Front Agron. https://doi.org/10.3389/fagro.2021.667903
Israel A, Langrand J, Fontaine J et al (2022) Significance of arbuscular mycorrhizal fungi in mitigating abiotic environmental stress in medicinal and aromatic plants: a review. Foods 11(17):2591. https://doi.org/10.3390/foods11172591
Jalili F, Khavazi K, Pazira E et al (2009) Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674. https://doi.org/10.1016/j.jplph.2008.08.004
Jarrett U, Miller S, Mohtadi H (2023) Dry spells and global crop production: a multi-stressor and multi-timescale analysis. Ecol Econ 203:107627. https://doi.org/10.1016/j.ecolecon.2022.107627
Jofre MF, Mammana SB, Lopez Appiolaza M et al (2023) Melatonin production by rhizobacteria native strains: towards sustainable plant growth promotion strategies. Physiol Plant 175(1):e13852
Karim S, Alezzawi M, Garcia-Petit C et al (2014) A novel chloroplast localized Rab GTPase protein CPRabA5e is involved in stress, development, thylakoid biogenesis and vesicle transport in Arabidopsis. Plant Mol Biol 84:675–692. https://doi.org/10.1007/s11103-013-0161-x
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138
Khan SW, Yaseen T, Naz F et al (2019) Influence of arbuscular mycorrhizal fungi (AMF) inoculation on growth and mycorrhizal dependency of (Lens culinaris L.) varieties. Int J Bioorganic Chem 4:47
Khazaei Z, Esmaielpour B, Estaji A (2020) Ameliorative effects of ascorbic acid on tolerance to drought stress on pepper (Capsicum annuum L) plants. Physiol Mol Biology Plants 26(8):1649–1662. https://doi.org/10.1007/s12298-020-00846-7
Kim SE, Lee CJ, Ji CY et al (2019) Transgenic sweetpotato plants overexpressing tocopherol cyclase display enhanced α-tocopherol content and abiotic stress tolerance. Plant Physiol Biochem 144:436–444. https://doi.org/10.1016/j.plaphy.2019.09.046
Kleczkowski LA, Igamberdiev AU (2021) Magnesium signaling in plants. Int J Mol Sci 22(3):1159. https://doi.org/10.3390/ijms22031159
Komatsu KJ, Esch NL, Bloodworth KJ et al (2023) Rhizobial diversity impacts soybean resistance, but not tolerance, to herbivory during drought. Basic Appl Ecol 66:31–39. https://doi.org/10.1016/j.baae.2022.12.004
Kour D, Rana KL, Yadav AN et al (2020) Amelioration of drought stress in Foxtail millet (Setaria italica L.) by P-solubilizing drought-tolerant microbes with multifarious plant growth promoting attributes. Environ Sustain 3(1):23–34. https://doi.org/10.1007/s42398-020-00094-1
Kumar N (2015) Effect of copper mining dust on the soil and vegetation in India: a critical review int. J Mod Sci Eng Technol 2(2):73–76
Kumar S, Kumar S, Mohapatra T (2021) Interaction between macro-and micro-nutrients in plants. Front Plant Sci 12:665583. https://doi.org/10.3389/fpls.2021.665583
Liang D, Ni ZY, Xia H et al (2019) Exogenous melatonin promotes biomass accumulation and photosynthesis of kiwifruit seedlings under drought stress. Sci Hortic 246:34–43. https://doi.org/10.1016/j.scienta.2018.10.058
Liu Y, Wei X (2021) Dark septate endophyte improves the drought-stress resistance of Ormosia hosiei seedlings by altering leaf morphology and photosynthetic characteristics. Plant Ecol 222:761–771. https://doi.org/10.1007/s11258-021-01135-3
Liu Q, Ying SH, Feng MG et al (2009) Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress. Antonie Van Leeuwenhoek 95:65–75. https://doi.org/10.1007/s10482-008-9288-1
Liu Y, Guo Z, Shi H (2022) Rhizobium symbiosis leads to increased drought tolerance in Chinese milk vetch (Astragalus sinicus L). Agronomy 12(3):725. https://doi.org/10.3390/agronomy12030725
Liu CY, Hao Y, Wu XL et al (2023a) Arbuscular mycorrhizal fungi improve drought tolerance of tea plants via modulating root architecture and hormones. Plant Growth Regul 4:1–10. https://doi.org/10.1007/s10725-023-00972-8
Liu F, Ma H, Liu B et al (2023b) Effects of plant growth-promoting rhizobacteria on the physioecological characteristics and growth of walnut seedlings under drought stress. Agronomy 13(2):290. https://doi.org/10.3390/agronomy13020290
Liu Y, Lu J, Cui L et al (2023c) The multifaceted roles of arbuscular mycorrhizal fungi in peanut responses to salt, drought, and cold stress. BMC Plant Biol 23(1):1–19. https://doi.org/10.1186/s12870-023-04053-w
López-Galiano MJ, García-Robles I, González-Hernández AI et al (2019) Expression of miR159 is altered in tomato plants undergoing drought stress. Plants 8(7):201. https://doi.org/10.3390/plants8070201
Ma W-Y, Qin Q-Y, Zou Y-N, Kuca K, Giri B, Wu Q-S, Hashem A, Al-Arjani A-BF, Almutairi KF, AbdAllah EF, Xu YJ (2022) Arbuscular mycorrhiza induces low oxidative burst in drought-stressed walnut through activating antioxidant defense systems and heat shock transcription factor expression. Front Plant Sci 13:1089420. https://doi.org/10.3389/fpls.2022.1089420
Mahreen N, Yasmin S, Asif M et al (2023) Mitigation of water scarcity with sustained growth of rice by plant growth promoting bacteria. Front Plant Sci 14:1081537. https://doi.org/10.3389/fpls.2023.1081537
Marcé M, Brown DS, Capell T et al (1995) Rapid high-performance liquid chromatographic method for the quantification of polyamines as their dansyl derivatives: application to plant and animal tissues. J Chromatogr B 666(2):329–335. https://doi.org/10.1016/0378-43479400586-T
Minocha R, Shortle WC, Long SL et al (1994) A rapid and reliable procedure for extraction of cellular polyamines and inorganic ions from plant tissues. J Plant Growth Regul 13(4):187–193. https://doi.org/10.1007/BF00226036
Miranda V, Silva-Castro GA, Ruiz-Lozano JM et al (2023) Fungal endophytes enhance wheat and tomato drought tolerance in terms of plant growth and biochemical parameters. J Fungi 9(3):384. https://doi.org/10.3390/jof9030384
Mirzabaev A, Kerr RB, Hasegawa T et al (2023) Severe climate change risks to food security and nutrition. Clim Risk Manage 39:100473. https://doi.org/10.1016/j.crm.2022.100473
Moreno-Galván AE, Cortés-Patiño S, Romero-Perdomo F et al (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
Mori Y (2015) Functional polymeric membrane in agriculture. Funct Polym Food Sci : Technol Biol. https://doi.org/10.1002/9781119108580
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22:867–880
Naservafaei S, Sohrabi Y, Moradi P (2023) Effects of exogenous application of 24-epibrassinolide on photosynthesis parameters, grain yield, and protein of dragon’s head (Lallemantia iberica) under drought stress conditions. J Plant Growth Regul 18:1–13. https://doi.org/10.1007/s00344-023-10910-7
Nemeskeri E, Horvath KZ, Andryei B et al (2022) Impact of plant growth-promoting rhizobacteria inoculation on the physiological response and productivity traits of field-grown tomatoes in Hungary. Horticulturae 8(7):641. https://doi.org/10.3390/horticulturae8070641
Niki E (2021) Lipid oxidation that is, and is not, inhibited by vitamin E: consideration about physiological functions of vitamin E. Free Radic Biol Med 176:1–15. https://doi.org/10.1016/j.freeradbiomed.2021.09.001
Oliveira TC, Cabral JS, Santana LR et al (2022) The arbuscular mycorrhizal fungus Rhizophagus clarus improves physiological tolerance to drought stress in soybean plants. Sci Rep 12(1):9044. https://doi.org/10.1038/s41598-022-13059-7
Ortiz N, Armada E, Duque E, Roldan A, Azcon R et al (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
Ostadi A, Javanmard A, Amani Machiani M et al (2022) Co-application of TiO2 nanoparticles and arbuscular mycorrhizal fungi improves essential oil quantity and quality of sage (Salvia officinalis L.) in drought stress conditions. Plants 11(13):1659. https://doi.org/10.3390/plants11131659
Pandey GK, Sanyal SK, Pandey GK et al (2021) Calcium-from nutrition to signaling. Funct dissection Calcium Homeost Transp Mach plants. https://doi.org/10.1007/978-3-030-58502-0_1
Pequeno DNL, Hern´andez-Ochoa IM, Reynolds M et al (2021) Climate impact and adaptation to heat and drought stress of regional and global wheat production. Environ Res Lett 16(5):054070. https://doi.org/10.1088/1748-9326/abd970
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br mycological Soc 55(1):158–IN18. https://doi.org/10.1016/S0007-15367080110-3
Rahmani V, Movahhedi Dehnavi M, Balouchi H et al (2023) Silicon can improve nutrient uptake and performance of black cumin under drought and salinity stresses. Commun Soil Sci Plant Anal 54(3):297–310. https://doi.org/10.1080/00103624.2022.2112590
Rajput S, Sengupta P, Kohli I et al (2022) Role of Piriformospora indica in inducing soil microbial communities and drought stress tolerance in plants. In: Singh H, Vaishnav A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 93–110
Ramakrishna W, Rathore P, Kumari R et al (2020) Brown gold of marginal soil: plant growth promoting bacteria to overcome plant abiotic stress for agriculture, biofuels and carbon sequestration. Sci Total Environ 711:135062. https://doi.org/10.1016/j.scitotenv.2019.135062
Riyazuddin R, Nisha N, Singh K et al (2022) Involvement of dehydrin proteins in mitigating the negative effects of drought stress in plants. Plant Cell Rep 41(3):519–533. https://doi.org/10.1007/s00299-021-02720-6
Ru C, Wang K, Hu X et al (2023) Nitrogen modulates the effects of heat, drought, and combined stresses on photosynthesis, antioxidant capacity, cell osmoregulation, and grain yield in winter wheat. J Plant Growth Regul 42:1681–1703. https://doi.org/10.1007/s00344-022-10650-0
Sadasivam S, Manickam A (2008) Biochemical methods, 3rd edn. New Age International Publishers
Sardans J, Peñuelas J (2021) Potassium control of plant functions: ecological and agricultural implications. Plants 10(2):419. https://doi.org/10.3390/plants10020419
Shah MN, Wright DL, Hussain S et al (2023) Organic fertilizer sources improve the yield and quality attributes of maize (Zea mays L.) hybrids by improving soil properties and nutrient uptake under drought stress. J King Saud University-Science 35(4):102570
Sharma A, Shahzad B, Kumar V et al (2019) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7):285. https://doi.org/10.3390/biom9070285
Shu S, Yuan Y, Chen J et al (2015) The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress. Sci Rep 5(1):1–16. https://doi.org/10.1038/srep14390
Siddique S, Naveed M, Yaseen M et al (2022) Exploring potential of seed endophytic bacteria for enhancing drought stress resilience in maize (Zea mays L). Sustainability 14(2):673. https://doi.org/10.3390/su14020673
Silva S, Santos C, Serodio J et al (2018) Physiological performance of drought-stressed olive plants when exposed to a combined heat–UV-B shock and after stress relief. Funct Plant Biol 45(12):1233–1240. https://doi.org/10.1071/FP18026
Silva S, Dias MC, Silva A (2023) Potential of MgO and MgCO3 nanoparticles in modulating lettuce physiology to drought. Acta Physiol Plant 45(2):1–9. https://doi.org/10.1007/s11738-022-03507-2
Teranishi Y, Tanaka A, Osumi M et al (1974) Catalase activities of hydrocarbon-utilizing Candida yeasts. Agric Biol Chem 38(6):1213–1220. https://doi.org/10.1080/00021369.1974.10861301
Timmusk S, Abd El-Daim IA, Copolovici L et al (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 9(5):e96086. https://doi.org/10.1371/journal.pone.0096086
Tsai HJ, Shao KH, Chan MT et al (2020) Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal Behav 15(2):1722447. https://doi.org/10.1080/15592324.2020.1722447
Tyagi J, Shrivastava N, Sharma AK et al (2021) Effect of Rhizophagus intraradices on growth and physiological performance of finger millet (Eleusine coracana L.) under drought stress. Plant Sci Today 8(4):912–923. https://doi.org/10.14719/pst.2021.8.4.1240
Tyagi J, Mishra A, Kumari S et al (2023) Deploying a microbial consortium of Serendipita indica, Rhizophagus intraradices, and Azotobacter chroococcum to boost drought tolerance in maize. Environ Exp Bot 206:105142. https://doi.org/10.1016/j.envexpbot.2022.105142
Ullah A, Farooq M (2022) The challenge of drought stress for grain legumes and options for improvement. Arch Agron Soil Sci 68(11):1601–1618. https://doi.org/10.1080/03650340.2021.1906413
van Der Heijden MG, Martin FM, Selosse MA et al (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423. https://doi.org/10.1111/nph.13288
Vishnupradeep R, Bruno LB, Taj Z et al (2022) Plant growth promoting bacteria improve growth and phytostabilization potential of Zea mays under chromium and drought stress by altering photosynthetic and antioxidant responses. Environ Technol Innov 25:102154. https://doi.org/10.1016/j.eti.2021.102154
Wang K, Li J, Yi Y et al (2022) Polyamine-activated carbonyl stress strategy for oxidative damage therapy. Nano Today 42:101355. https://doi.org/10.1016/j.nantod.2021.101355
Wang Y, Zou YN, Shu B et al (2023) Deciphering molecular mechanisms regarding enhanced drought tolerance in plants by arbuscular mycorrhizal fungi. Sci Hort 308:111591. https://doi.org/10.1016/j.scienta.2022.111591
Waqar A, Bano A, Ajmal M (2022) Effects of PGPR bioinoculants, hydrogel and biochar on growth and physiology of soybean under drought stress. Commun Soil Sci Plant Anal 53(7):826–847. https://doi.org/10.1080/00103624.2022.2028818
Yadav S, Modi P, Dave A et al (2020) Effect of abiotic stress on crops. Sustainable crop production 3
Yasmeen S, Wahab A, Saleem MH et al (2022) Melatonin as a foliar application and adaptation in lentil (Lens culinaris Medik.) crops under drought stress. Sustainability 14(24):16345. https://doi.org/10.3390/su142416345
Yu J, Fan N, Hao T et al (2023) Ethionine-mitigation of drought stress associated with changes in root viability, antioxidant defense, osmotic adjustment, and endogenous hormones in tall fescue. Plant Growth Regul 21:1–14. https://doi.org/10.1007/s10725-022-00944-4
Zhang K, Zhang Y, Sun J et al (2021) Deterioration of orthodox seeds during ageing: influencing factors, physiological alterations and the role of reactive oxygen species. Plant Physiol Biochem 158:475–485. https://doi.org/10.1016/j.plaphy.2020.11.031
Zhu J, Cai D, Wang J et al (2021) Physiological and anatomical changes in two rapeseed (Brassica napus L.) genotypes under drought stress conditions. Oil Crop Science 6(2):97–104. https://doi.org/10.1016/j.ocsci.2021.04.003
Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21(3):401–404. https://doi.org/10.1139/x91-050
Acknowledgements
MS, JGS, and BG are thankful to Department of Microbiology, IARI, New Delhi for providing PGPBs and AMF inoculum. MS and JGS express their gratitude for the generous financial support provided by Delhi Technological University for the ICPMS and TEM analysis. The authors are also thankful to Professor Ajit Verma, Amity Institute of Microbial Technology, Amity University, Uttar Pradesh, India for providing Piriformospora indica inoculum.
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MS performed the experiments. JGS and BG designed the experiments. MS, BG, and JGS wrote the article and approved the final manuscript.
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Singh, M., Sharma, J.G. & Giri, B. Microbial inoculants alter resilience towards drought stress in wheat plants. Plant Growth Regul 101, 823–843 (2023). https://doi.org/10.1007/s10725-023-01059-0
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DOI: https://doi.org/10.1007/s10725-023-01059-0