Abstract
Drought-induced stress poses a formidable impediment to agricultural productivity, compromising crop growth and yield. While the utilization of arbuscular micorrhizal fungi (AMF) consortium, plant growth promoting bacteria (PGPB) consortium, and Piriformospora indica inoculum shows promise in mitigating drought effects, a rigorous scientific assessment of their relative efficacy is lacking. This study thus investigates the comparative effects of P. indica, AMF consortium, and PGPB consortium inoculation on nutrient assimilation, ultrastructural adjustments, metabolic responses, and antioxidant defenses in drought-exposed maize plants. A completely randomized block design was employed, subjecting plants to varying drought stress levels (75%, 55%, 45%, and 35% of soil field capacity (FC)) in a greenhouse. The study analyzed multiple aspects, including growth parameters, nutrient levels, physiological responses, osmolyte content, antioxidant defense mechanisms, and leaf ultrastructure. Inoculation with AMF, P. indica, and PGPB yielded substantial enhancements in growth metrics like plant height, biomass accrual, leaf area expansion, stomatal conductance, photosynthetic activity, internal CO2 dynamics, and transpiration rate, particularly evident across all drought stress intensities. Notably, microbial treatments counteracted nutrient deficiencies induced by drought, with augmented levels of osmolytes (total sugars, trehalose, glycine betaine), proteins, attenuated lipoxygenase enzyme (LOX) activity, ion leakage, and lipid peroxidation relative to non-inoculated plants. Elevated enzymatic activity of antioxidants, including ascorbate peroxidase (APX), catalase (CAT), and superoxide dismutase (SOD), in addition to elevated non-enzymatic antioxidants (proline, α-tocopherol, polyamines), was evident in microbial-inoculated plants. Furthermore, microbial inoculation ameliorated drought-induced ultrastructural alterations. Noteworthy disparities in drought resilience were observed among inoculants, with PGPB displaying the highest robustness, followed by AMF and P. indica. This research underscores the substantial potential of microbial inoculants in fostering sustainable agriculture practices in drought-challenged contexts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this research have been incorporated into this research article. For any further inquiries, please contact the corresponding author.
References
A Saga of Progress (2012) Compendium of 50 years of achievements. Punjab Agricultural University, Ludhiana, p 230
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 S, Javed MT, Shahid MI, Haider MZ, Chaudhary HJ, Tanwir K, Maqsood A (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
Agnihotri R, Sahni S, Sharma MP, Gupta MM (2022) Facets of AM fungi in sequestering soil carbon and improving soil health. In: Rajpal VR, Singh I, Navi SS (eds) Fungal diversity, ecology and control management, Fungal Biology. Springer, Singapore, pp 327–344. https://doi.org/10.1007/978-981-16-8877-5_15
Akhilesh S, Basandrai AK, Kalia V (2000) Resistance in rabi maize to Fusarium stalk rot (Fusarium moliniformae) and common rust (Puccinia sorghi). Crop Res (Hisar) 20(2):221–225
Alam MZ, Choudhury TR, Mridha MA (2023) Arbuscular mycorrhizal fungi enhance biomass growth, mineral content, and antioxidant activity in tomato plants under drought stress. J Food Qual 2023:2581608. https://doi.org/10.1155/2023/2581608
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, Gul H, Hamayun M, Rauf M, Iqbal A, Hussain A, Lee IJ (2022) Endophytic fungi controls the physicochemical status of maize crop under salt stress. Pol J Environ Stud 31:561–573. https://doi.org/10.15244/pjoes/134540
Ali R, Hassan S, Shah D, Sajjad N, Bhat EA (2020) Role of polyamines in mitigating abiotic stress. Roychoudhury A, Tripathi DK (ed) Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives, vol 22. Wiley, New York, pp 291–305. https://doi.org/10.1002/9781119552154.ch13
Arnon DI (1949) Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1–15
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
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
de Bang TC, Husted S, Laursen KH, Persson DP, Schjoerring JK (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
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, Akhtar K, Roy R, Khan MI, Zhao T (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, Bedi N (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
Bidalia A, Okram Z, Hanief M, Rao KS (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
Bisht A, Gupta MM (2023) Arbuscular Mycorrhiza Fungi Resources for sustainable and climate-smart cultivation of Maize. In: Singh I, Rajpal VR, Nav SS (eds) Fungal resources for sustainable economy: current status and future perspectives. Springer, Singapore, pp 299–317. https://doi.org/10.1007/978-981-19-9103-5_11
Boutasknit A, Baslam M, Ait-El-Mokhtar M, Anli M, Ben-Laouane R, Douira A, El Modafar C, Mitsui T, Wahbi S, Meddich A (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
Cao JL, He WX, Zou YN, Wu QS (2023) An endophytic fungus, Piriformospora indica, enhances drought tolerance of trifoliate orange by modulating the antioxidant defense system and composition of fatty acids. Tree Physiol 43(3):452–466. https://doi.org/10.1093/treephys/tpac126
Chiappero J, del Rosario Cappellari L, Alderete LG, 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
Chourasiya D, Gupta MM, Sahni S, Oehl F, Agnihotri R, Buade R, Maheshwari HS, Prakash A, Sharma MP (2021) Unraveling the AM fungal community for understanding its ecosystem resilience to changed climate in agroecosystems. Symbiosis 84:295–310. https://doi.org/10.1007/s13199-021-00761-9
Devarajan AK, Muthukrishanan G, Truu J, Truu M, Ostonen I, Kizhaeral SS, Panneerselvam P, Kuttalingam Gopalasubramanian S (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, Valk BE, Schram AW, Douma AC (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. The International Organization for Standardization, Geneva
Fadiji AE, Santoyo G, Yadav AN, Babalola OO (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, Basra SM (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29(1):185–212. https://doi.org/10.1051/agro:2008021
Ferreira JC, Paschoalin VMF, Panek AD, Trugo LC (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
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500
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, Hamurcu H, Gupta OP, Gezgin S (eds) Abiotic Stresses in Wheat. Academic Press, Cambridge, pp 297–311. https://doi.org/10.1016/B978-0-323-95368-9.00023-0
Haghighi TM, Saharkhiz MJ, Kavoosi G, Zarei M (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
Hari NS, Jindal J, Malhi NS (2008) Resistance of Cry1Ab maize to spotted stemborer Chilo partellus (Lepidoptera: Crambidae) in India. Int J Trop Insect Sci 27:223–228. https://doi.org/10.1017/S1742758407850983
Hasanuzzaman M, Bhuyan MB, Nahar K, Hossain M, Mahmud J, Hossen M, Masud A, Moumita Fujita M (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, Egamberdieva D (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, Oskoueian E (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
van Der Heijden MG, Martin FM, Selosse MA, Sanders IR (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
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
Inbaraj MP (2021) Plant-microbe interactions in alleviating abiotic stress - a mini review. Front Agron 3:667903. https://doi.org/10.3389/fagro.2021.667903
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, Silva MF, Gomez FJ, Cohen AC (2023) Melatonin production by rhizobacteria native strains: towards sustainable plant growth promotion strategies. Physiol Plant 175(1):e13852
Jyoti K, Ramesh K, Kumar RS, Sain D, Bilal B, Kamboj OP, Usha N, Yadav AK (2013) Response of maize (Zea mays L.) hybrids to excess soil moisture stress at different growth stages. Res Crops 14(2):439–443
Karim S, Alezzawi M, Garcia-Petit C, Solymosi K, Khan NZ, Lindquist E, Dahl P, Hohmann S, Aronsson H (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
Khan SW, Yaseen T, Naz F, Abidullah S, Kamil M (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, Kim HS, Park SU, Lim YH, Park WS, Ahn MJ, Bian X, Xie Y, Guo X, Kwak SS (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
Komatsu KJ, Esch NL, Bloodworth KJ, Burghardt KT, McGurrin K, Pullen JD, Parker JD (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, Sheikh I, Kumar V, Dhaliwal HS, Saxena AK (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 R, Kaul J, Dubey RB, Singode A, Gk C, Manivannan A, Debnath MK (2015) Assessment of drought tolerance in maize (Zea mays L.) based on different indices. SABRAO J Breed Genet 47(3):291–298
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, Xie Y, Lv X, Wang J, Lin L, Deng Q, Luo X (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, 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, Dai F, Abd-Allah EF, Wu Q, Liu S (2023) 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 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
López-Galiano MJ, García-Robles I, González-Hernández AI, Camañes G, Vicedo B, Real MD, Rausell C (2019) Expression of miR159 is altered in tomato plants undergoing drought stress. Plants 8(7):201. https://doi.org/10.3390/plants8070201
Mahreen N, Yasmin S, Asif M, Yahya M, Ejaz K, Mehboob-Ur-Rahman Yousaf S, Amin I, Zulfiqar S, Imran A, Khaliq S, Arif M (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, Figueras X, Tiburcio AF (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, Minocha SC (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
Mirzabaev A, Kerr RB, Hasegawa T, Pradhan P, Wreford A, Cristina T, von der Pahlen M, Gurney-Smith H (2023) Severe climate change risks to food security and nutrition. Clim Risk Manage 39:100473. https://doi.org/10.1016/j.crm.2022.100473
Mori Y (2015) Functional polymeric membrane in agriculture. In: Cirillo G, Spizzirri UG, Iemma F (eds) Functional Polymers in Food Science: From Technology to Biology. John Wiley & Sons, vol 2, pp 33–45. https://doi.org/10.1002/9781119108580.ch3
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, Ilahy R, Takács S, Neményi A, Pék Z, Helyes L (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, Tavares GG, Santos LDS, Paim TP, Müller C, Silva FG, Costa AC, Souchie EL, Mendes GC (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, Roldán A, Azcón R, 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
Ostadi A, Javanmard A, Amani Machiani M, Sadeghpour A, Maggi F, Nouraein M, Morshedloo MR, Hano C, Lorenzo JM (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 (2021) Calcium-from nutrition to signaling. Functional dissection of calcium homeostasis and transport machinery in plants, 1–9. https://doi.org/10.1007/978-3-030-58502-0_1
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, Yadavi A, Hamidian M (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, Varma A, Singh PK, Joshi NC (2022) Role of Piriformospora indica in inducing soil microbial communities and drought stress tolerance in plants. In: Singh H and Vaishnav A (eds) New and future developments in microbial biotechnology and bioengineering, sustainable agriculture: Microorganisms as Biostimulants. Elsevier, Amsterdam, pp 93–110. https://doi.org/10.1016/B978-0-323-85163-3.00003-X
Ramakrishna W, Rathore P, Kumari R, Yadav R (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
Ru C, Wang K, Hu X, Chen D, Wang W, Yang H (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, New Delhi
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, Koutroubas SD, Seepaul R, George S, Ali S, Naveed M, Khan M, Altaf MT, Ghaffor K (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 Univ-Sci 35(4):102570
Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Handa N, Kapoor D, Bhardwaj R, Zheng B (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, Sun J, Zhang W, Tang Y, Zhong M, Guo S (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, Shahbaz M (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, 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
Singh M, Sharma JG, Giri B (2023) Microbial inoculants alter resilience towards drought stress in wheat plants. Plant Growth Regul. https://doi.org/10.1007/s10725-023-01059-0
Sinha SK, Sinha AK, Thakur D, Lakra A, Tripathi AK (2019) Maize research in Chhattisgarh: status and progress. Int J Curr Microbiol Appl Sci 8:2210–2230. https://doi.org/10.20546/ijcmas.2019.803.265
Srinivasa Rao C, Prabhakar M, Maheswari M, Srinivasa Rao M, Sharma KL, Srinivas K, Prasad JVNS, Rama Rao CA, Vanaja M, Ramana DBV, Gopinath KA, Subba Rao AVM, Rejani R, Bhaskar S, Sikka AK, Alagusundaram K (2016) National Innovations in Climate resilient agriculture (NICRA), research highlights 2015-16. Central Research Institute for Dryland Agriculture, Hyderabad, p 112
Tang L, Xiao L, Chen E, Lei X, Ren J, Yang Y, Xiao B, Gong C (2023) Magnesium transporter CsMGT10 of tea plants plays a key role in chlorosis leaf vein greening. Plant Physiol Biochem 17:107842. https://doi.org/10.1016/j.plaphy.2023.107842
Teranishi Y, Tanaka A, Osumi M, Fukui S (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, 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(5):e96086. https://doi.org/10.1371/journal.pone.0096086
Tyagi J, Mishra A, Kumari S, Singh S, Agarwal H, Pudake RN, Varma A, Joshi NC (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
Tyagi J, Shrivastava N, Sharma AK, Varma A, Pudake R (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
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
Vishnupradeep R, Bruno LB, Taj Z, Karthik C, Challabathula D, Kumar A, Freitas H, Rajkumar M (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, Lv B, Wu Y, Wang C, Li H, Li Y, Liu Y, Cai X, Meng X, Jiang X, Zheng X, Zhou Z, Bu W (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, Wu Q (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, Vijapura A, Patel D, Patel M (2020) Effect of abiotic stress on crops. In: Sustainable Crop Production, IntechOpen, London, pp 3–24. https://doi.org/10.5772/intechopen.88434
Yasmeen S, Wahab A, Saleem MH, Ali B, Qureshi KA, Jaremko M (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, Bian Y, Zhuang L, Li Q, Yang Z (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, Meng J, Tao J (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, Cao J, Wen Y, He J, Zhao L, Wang D, Zhang S (2021) Physiological and anatomical changes in two rapeseed (Brassica napus L.) genotypes under drought stress conditions. Oil Crop Sci 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
The authors extend their sincere thanks to Professor Ajit Verma, AIMT, Amity University, Uttar Pradesh, India, for providing the Piriformospora indica inoculum. MS, JGS, and BG would like to express their gratitude to the Department of Microbiology at IARI, New Delhi, for generously providing the PGPB inoculum and AMF inoculum.
Funding
MS and JGS also acknowledge Delhi Technological University for their generous financial support in recording the TEM and ICPMS data.
Author information
Authors and Affiliations
Contributions
MS, JGS and BG formulated the research framework and its conceptual design. MS executed all experimental procedures. MS authored the initial manuscript, which underwent subsequent refinement by JGS and BG. MS, JGS, and BG approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 17.3 MB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Singh, M., Sharma, J.G. & Giri, B. Microbial inoculants improve growth in Zea mays L. under drought stress by up-regulating antioxidant, mineral acquisition, and ultrastructure modulations. Symbiosis 91, 55–77 (2023). https://doi.org/10.1007/s13199-023-00945-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-023-00945-5