Role of Endophytes in Abiotic Stress Tolerance: With Special Emphasis on Serendipita indica

Jaagriti Tyagi1, Parul Chaudhary2, Arti Mishra1, Mahak Khatwani1, Srijita Dey1, Ajit Varma1
1Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Sector 125, Noida Express Way, Noida, Uttar Pradesh, 201313, India
2Department of Microbiology, College of Basic Sciences and Humanities, G. B. Pant University of Agriculture and Technology, Pantnagar, India

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Abadi VAJM, Sepehri M (2016) Effect of Piriformospora indica and Azotobacter chroococcum on mitigation of zinc deficiency stress in wheat (Triticum aestivum L.). Symbiosis 69:9–19

Abadi VAJM, Sepehri M, Khatabi B, Rezaei M (2021) Alleviation of zinc deficiency in wheat inoculated with root endophytic fungus Piriformospora indica and rhizobacterium Pseudomonas putida. Rhizosphere 17:100311

Abdelaziz ME, Abdelsattar M, Abdeldaym EA, Atia MA, Mahmoud AWM, Saad MM, Hirt H (2019) Piriformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic 256:108532

Acosta-Motos J, Ortuño M, Bernal-Vicente A, Diaz-Vivancos P, Sanchez- Blanco M, Hernandez J (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18

Adeleke ARO, Abdul Latiff AA, Daud Z, Mat Daud NF and Aliyu MK (2017) Heavy metal removal from wastewater of palm oil mill using developed activated carbon from coconut shell and cow bones. In: Key engineering materials, vol 737, pp 428–432. Trans Tech Publications Ltd.

Agri U, Chaudhary P, Sharma A (2021) In vitro compatibility evaluation of agriusable nanochitosan on beneficial plant growth-promoting rhizobacteria and maize plant. Natl Acad Sci Lett 44:555–559

Alam P, Albalawi TH, Altalayan FH, Bakht MA, Ahanger MA, Raja V, Ashraf M, Ahmad P (2019) 24-Epibrassinolide (EBR) confers tolerance against NaCl stress in soybean plants by up-regulating antioxidant system, ascorbate-glutathione cycle, and glyoxalase system. Biomolecules 9:640

Al-Arjani ABF, Hashem A, Abd Allah EF (2020) Arbuscular mycorrhizal fungi modulates dynamics tolerance expression to mitigate drought stress in Ephedra foliata Boiss. Saudi J Biol Sci 27:380–394

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signaling transduction. Annu Rev Plant Biol 55:373

Arora M, Saxena P, Abdin MZ, Varma A (2020) Interaction between Piriformospora indica and Azotobacter chroococcum diminish the effect of salt stress in Artemisia annua L. by enhancing enzymatic and non-enzymatic antioxidants. Symbiosis 80:61–73

Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

Aslam MM, Karanja J, Bello SK (2019) Piriformospora indica colonization reprograms plants to improved P-uptake, enhanced crop performance, and biotic/abiotic stress tolerance. Physiol Mol Plant Pathol 106:232–237

Attri MK, Varma A (2018) Bulk production of a potent plant promoter Piriformospora indica (Serendipita indica) in a bioreactor by using Jaggery at optimum environmental conditions. Biochem Cell Arch 18:1495–1501

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 Hortic 287:110260

Babu AG, Reddy MS (2011) Dual inoculation of arbuscular mycorrhizal and phosphate solubilizing fungi contributes in sustainable. maintenance of plant health in fly ash ponds. Water Air Soil Pollut 219:3–10

Bakshi M, Sherameti I, Meichsner D, Thürich J, Varma A, Johri AK, Yeh KW, Oelmüller R (2017) Piriformospora indica reprograms gene expression in Arabidopsis phosphate metabolism mutants but does not compensate for phosphate limitation. Front Microbiol 8:1262

Bamisile BS, Dash CK, Akutse KS, Keppanan R, Wang L (2018) Fungal endophytes: beyond herbivore management. Front Microbiol 9:1–11

Baron NC, Costa NTA, Mochi DA, Rigobelo EC (2018) First report of Aspergillus sydowii and Aspergillus brasiliensis as phosphorus solubilizers in maize. Ann Microbiol 68:863–870

Basu S, Roychoudhury A, Saha PP, Sengupta DN (2010) Differential antioxidative responses of indica rice cultivars to drought stress. Plant Growth Regul 60(1):51–59

Bhattacharya A (2022) Plant growth hormones in plants under low-temperature stress: a review. In: Physiological processes in plants under low temperature stress, pp.517–627

Bilal S, Shahzad R, Imran M, Jan R, Kim KM, Lee I-J (2020) Synergistic association of endophytic fungi enhances Glycine max L. resilience to combined abiotic stresses: heavy metals, high temperature and drought stress. Ind Crops Prod 143:111931

Boeckx T, Webster R, Winters AL, Webb KJ, Gay A, Kingston-Smith AH (2015) Polyphenol oxidase-mediated protection against oxidative stress is not associated with enhanced photosynthetic efficiency. Ann Bot 116:529–540

Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

Card SD, Bastías DA, Caradus JR (2021) Antagonism to plant pathogens by Epichloë fungal endophytes—a review. Plants 11:10–1997

Chandrasekar B, Wanke A, Wawra S, Saake P, Mahdi L, Charura N, Neidert M, Poschmann G, Malisic M, Thiele M, Stühler K (2022) Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses. Plant Cell

Chaudhary P, Sharma A (2019) Response of nanogypsum on the performance of plant growth promotory bacteria recovered from nanocompound infested agriculture field. Environ Ecol 37:363–372

Chaudhary P, Khati P, Chaudhary A, Gangola S, Kumar R, Sharma A (2020) Bioinoculation using indigenous Bacillus spp. improves growth and yield of Zea mays under the influence of nanozeolite. 3 Biot 11(1):11

Chaudhary A, Parveen H, Chaudhary P, Khatoon H, Bhatt P (2021a) Rhizospheric microbes and their mechanism. In: Bhatt P, Gangola S, Udayanga D, Kumar G (eds) Microbial technology for sustainable environment. Springer, Singapore

Chaudhary P, Khati P, Gangola S, Kumar A, Kumar R, Sharma A (2021b) Impact of nanochitosan and Bacillus spp. on health, productivity and defence response in Zea mays under field condition. 3 Biot 11:237

Chaudhary P, Parveen H, Gangola S, Kumar G, Bhatt P, Chaudhary A (2021c) Plant growth-promoting rhizobacteria and their application in sustainable crop production. In: Bhatt P, Gangola S, Udayanga D, Kumar G (eds) Microbial technology for sustainable environment. Springer, Singapore. https://doi.org/10.1007/978-981-16-3840-4_13

Chaudhary P, Chaudhary A, Bhatt P, Kumar G, Khatoon H, Rani A, Kumar S, Sharma A (2022) Assessment of soil health indicators under the influence of nanocompounds and Bacillus spp. in field condition. Front Environ Sci 9:769871

Chen CP, Frank TD, Long SP (2009) Is a short, sharp shock equivalent to long-term punishment? Contrasting the spatial pattern of acute and chronic ozone damage to soybean leaves via chlorophyll fluorescence imaging. Plant Cell Environ 32(4):327–335

Chen W, Lin F, Lin KH, Chen C, Xia C, Liao Q, Kuo YW (2021) Growth promotion and salt-tolerance improvement of Gerbera jamesonii by root colonization of Piriformospora indica. J Plant Growth Reg 21:1–10

Cheng HQ, Ding YE, Shu B, Zou YN, Wu QS, Kuča K (2020) Plant aquaporin responses to mycorrhizal symbiosis under abiotic stress. Int J Agric Biol 23:786–794

Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23681

Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57(3):449–459

Dabral S, Varma A, Choudhary DK, Bahuguna RN, Nath M (2019) Biopriming with Piriformospora indica ameliorates cadmium stress in rice by lowering oxidative stress and cell death in root cells. Ecotoxicol Environ Saf 186:109741

Das MK, Roychoudhury A (2014) ROS and responses of antioxidant as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:1–3

Dastogeer KM (2018) Influence of fungal endophytes on plant physiology is more pronounced under stress than well-watered conditions: a meta-analysis. Planta 248:1403–1416

Dey P, Datta D, Saha D, Parida S, Panda D (2019) Plant-endophyte interaction and its application to abiotic stress management of crop plants. Int J Curr Microbiol App Sci 8:2708–2716

Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox-and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171(3):1541–1550

Dobermann A, Nelson R, Beever D, Bergvinson D, Crowley E, Denning G, Giller K, d’Arros Hughes J, Jahn M, Lynam J, Masters W (2013) Solutions for sustainable agriculture and food systems. In: Sustainable development solutions network

Dolatabadi HK, Goltapeh EM, Moieni A, Varma A (2012) Evaluation of different densities of auxin and endophytic fungi (Piriformospora indica and Sebacina vermifera) on Mentha piperita and Thymus vulgaris growth. Afr J Biotechnol 11(7):1644–1650

Domka AM, Rozpaądek P, Turnau K (2019) Are fungal endophytes merely mycorrhizal copycats? The role of fungal endophytes in the adaptation of plants to metal toxicity. Front Microbiol 10:371

Doni F, Mispan MS, Suhaimi NSM, Ishak N, Uphoff N (2019) Roles of microbes in supporting sustainable rice production using the system of rice intensification. Appl Microbiol Biotechnol 103:5131–5142

Dubey A, Kumar A, Abd Allah EF (2019) Growing more with less: breeding and developing drought resilient soybean to improve food security. Ecol Indic 105:425–437

Eid AM, Salim SS, Hassan SED, Ismail MA, Fouda A (2019) Role of endophytes in plant health and abiotic stress management. Microbiome in plant health and disease. Springer, Singapore, pp 119–144

Elstner EF, Osswald W, Konze JR (1980) Reactive oxygen species: electron donor-hydrogen peroxide complex instead of free OH radicals? FEBS Lett 121(2):219–221

Fan D, Subramanian S, Smith DL (2020) Plant endophytes promote growth and alleviate salt stress in Arabidopsis thaliana. Sci Rep 10:1–18

Fontana DC, de Paula S, Torres AG, de Souza VHM, Pascholati SF, Schmidt D, Dourado Neto D (2021) Endophytic fungi: biological control and induced resistance to phytopathogens and abiotic stresses. Pathogens 10(5):570

Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119(3):355–364

Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17(7):1866–1875

Fridovich I (1997) Superoxide anion radical (O2), superoxide dismutases, and related matters. J Biol Chem 272(30):18515–18517

Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141(2):341–345

Gazara RK, Khan S, Iqrar S, Ashrafi K, Abdin MZ (2020) Comparative transcriptome profiling of rice colonized with beneficial endophyte, Piriformospora indica, under high salinity environment. Mol Biol Rep 47:7655–7673

Ghabooli M, Rezaei E, Movahedi Z, Mohsenifard E (2020) Effect of Piriformospora indica inoculation on some morphophysiological parameters in licorice (Glycyrrhiza glabra L.) under drought stress. Iran J Plant Physiol 10:3379–3389

Ghaffari MR, Mirzaei M, Ghabooli M, Khatabi B, Wu Y, Zabet-Moghaddam M, Salekdeh GH (2019) Root endophytic fungus Piriformospora indica improves drought stress adaptation in barley by metabolic and proteomic reprogramming. Environ Exp Bot 157:197–210

Ghorbani A, Omran VOG, Razavi SM, Pirdashti H, Ranjbar M (2019) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Rep 38:1151–1163

Ghorbani A, Tafteh M, Roudbari N, Pishkar L, Zhang W, Wu C (2021) Piriformospora indica augments arsenic tolerance in rice (Oryza sativa) by immobilizing arsenic in roots and improving iron translocation to shoots. Ecotoxicol Environ Saf 209:111793

Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:332

Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24:867–878

Halliwell B (2006) Reactive species and antioxidants, redox biology is a fundamental theme of aerobic life. Plant Physiol 141(2):312–322

Hasanuzzaman M, Parvin K, Bardhan K, Nahar K, Anee TI, Masud AAC, Fotopoulos V (2021) Biostimulants for the regulation of reactive oxygen species metabolism in plants under abiotic stress. Cells 10:2537

Hashem A, Abd Allah EF, Alqarawi AA, Al-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089

Hassani D, Khalid M, Huang D, Zhang YD (2019) Morphophysiological and molecular evidence supporting the augmentative role of Piriformospora indica in mitigation of salinity in Cucumis melo L. Acta Biochim Biophys Sin 51:301–312

Hill TW, Kafer E (2001) Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet Rep 48:20–21

Honglin H, Ullah F, Zhou D-X, Yi M, Zhao Yu (2019) "Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800

Hosseini F, Mosaddeghi MR, Dexter AR (2017) Effect of the fungus Piriformospora indica on physiological characteristics and root morphology of wheat under combined drought and mechanical stresses. Plant Physiol Biochem 118:107–120

Hu S, Ding Y, Zhu C (2020) Sensitivity and responses of chloroplasts to heat stress in plants. Front Plant Sci 11:375

Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191

Hussin S, Khalifa W, Geissler N, Koyro HW (2017) Influence of the root endophyte Piriformospora indica on the plant water relations, gas exchange and growth of Chenopodium quinoa at limited water availability. J Agron Crop Sci 203:373–384

Ijaz B, Formentin E, Ronci B, Locato V, Barizza E, Hyder MZ, Yasmin T (2019) Salt tolerance in indica rice cell cultures depends on a fine tuning of ROS signalling and homeostasis. PLoS ONE 14(4):e0213986

Ikram M, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A, Hamayun M (2018) IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PLoS ONE 13:0208150

Iqbal Z, Iqbal MS, Hashem A, Abd Allah EF, Ansari MI (2021) Plant defense responses to biotic stress and its interplay with fluctuating dark/light conditions. Front Plant Sci 12:631810

Ismail HM, Hussain A, Iqbal A, Khan SA, Lee IJ (2020) Aspergillus niger boosted heat stress tolerance in sunflower and soybean via regulating their metabolic and antioxidant system. J Plant Interact 15:223–232

Jaagriti T, Prasun B, Neeraj S, Sharma AK, Ajit V, Pudake RN (2017) Effect of inoculum concentrations of Piriformospora indica (Serendipita indica) on phenotypic and biochemical characteristics of finger millet plant under drought stress. Biochem Cell Arch 17:427–434

Jaber LR, Araj SE (2018) Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biol Control 116:53–61

Janků M, Luhová L, Petřivalský M (2019) On the origin and fate of reactive oxygen species in plant cell compartments. Antioxidants 8(4):105

Jiang W, Pan R, Buitrago S, Wu C, Abdelaziz ME, Oelmüller R, Zhang W (2021) Transcriptome analysis of Arabidopsis reveals freezing-tolerance related genes induced by root endophytic fungus Piriformospora indica. Physiol Mol Biol Plants 27(2):189–201

Jisha S, Gouri PR, Anith KN, Sabu KK (2018) Piriformospora indica cell wall extract as the best elicitor for asiaticoside production in Centella asiatica (L.) Urban, evidenced by morphological, physiological and molecular analyses. Plant Physiol Biochem 125:106–115

Jogawat A, Vadassery J, Verma N, Oelmüller R, Dua M, Nevo E, Johri AK (2016) PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Sci Rep 6:1–15

Johnson JM, Thürich J, Petutschnig EK, Altschmied L, Meichsner D, Sherameti I, Dindas J, Mrozinska A, Paetz C, Scholz SS, Furch AC (2018) A poly (A) ribonuclease controls the cellotriose-based interaction between Piriformospora indica and its host Arabidopsis. Plant Physiol 176(3):2496–2514

Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77

Khalid M, Hassani D, Liao J, Xiong X, Bilal M, Huang D (2018) An endosymbiont Piriformospora indica reduces adverse effects of salinity by regulating cation transporter genes, phytohormones, and antioxidants in Brassica campestris ssp. Chinensis. Environ Exp Bot 153:89–99

Khalid M, Kayani SI, Tang K (2020) The ameliorative effects of exogenous inoculation of Piriformospora indica on molecular, biochemical and physiological parameters of Artemisia annua L. under arsenic stress condition. Ecotoxicol Environ Saf 206:111202

Khalvandi M, Amerian M, Pirdashti H, Keramati S (2021) Does co-inoculation of mycorrhiza and Piriformospora indica fungi enhance the efficiency of chlorophyll fluorescence and essential oil composition in peppermint under irrigation with saline water from the Caspian Sea? PLoS ONE 16:0254076

Khan N, Singh SK, Srivastava JP, Siddiqui MZ (2010) Effect of bio fertilizers on production potential and economic feasibility of cauliflower (Brassica oleracea (L.) var. botrytis). Progress Agric 10(2):371–373

Khati P, Parul BP, Nisha KR, Sharma A (2018) Effect of nanozeolite and plant growth promoting rhizobacteria on maize. 3 Biotech 8:141

Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K (2016) Aquaporin-mediated long-distance polyphosphate translocation directed toward the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211:1202–1208

Kord H, Fakheri B, Ghabooli M, Solouki M, Emamjomeh A, Khatabi B, Sepehri M, Salekdeh GH, Ghaffari MR (2019) Salinity-associated microRNAs and their potential roles in mediating salt tolerance in rice colonized by the endophytic root fungus Piriformospora indica. Funct Integr Genomics 19:659–672

Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155(3):780–790

Kumar A, Sharma A, Chaudhary P, Gangola S (2021) Chlorpyrifos degradation using binary fungal strains isolated from industrial waste soil. Biologia 76:3071–3080

Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276

Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8(4):94

Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70(5):831–844

Li WK (2005) Endophytes and natural medicines. Chin J Nat Med 3:193–199

Li X, Cobb CE, Hill KE, Burk RF, May JM (2001) Mitochondrial uptake and recycling of ascorbic acid. Arch Biochem Biophys 387(1):143–153

Li L, Li L, Wang X, Zhu P, Wu H, Qi S (2017) Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiol Biochem 119:211–223

Li D, Mensah RA, Liu F, Tian N, Qi Q, Yeh K, Xuhan X, Cheng C, Lai Z (2019) Effects of Piriformospora indica on rooting and growth of tissue-cultured banana (Musa acuminata cv. Tianbaojiao) seedlings. Sci Hortic 257:108649

Li XM, Li YY, Lj-Wang LL (2021) Effect of endophyte inoculation on the accumulation of mineral elements and organic acids in rice (Oryza sativa L.) under osmotic stress. Appl Ecol Environ Res 19:763–775

Li D, Bodjrenou DM, Zhang S, Wang B, Pan H, Yeh KW, Lai Z, Cheng C (2021) The endophytic fungus Piriformospora indica reprograms banana to cold resistance. Int J Mol Sci 22:4973

Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827

Liu YANG, Jin-Li CAO, Zou YN, Qiang-Sheng WU, Kamil KUČA (2020) Piriformospora indica: a root endophytic fungus and its roles in plants. Not Bot Horti Agrobot Cluj Napoca 48:1–13

Mailloux RJ, Harper ME (2011) Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med 51(6):1106–1115

Malar S, Vikram SS, Favas PJ, Perumal V (2016) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55(1):1–1

Manasa KM, Vasanthakumari MM, Nataraja KN, Shaanker RU (2020) Endophytic fungi of salt adapted Ipomea pes-caprae LR Br: their possible role in inducing salinity tolerance in paddy (Oryza sativa L.). Curr Sci 118(9):00113891

Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A (2017) Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants. Genes 8:360

Mhamdi AG, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models, pp 4197–4220

Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145:164376

Miller GA, Suzuki N, Ciftci-Yilmaz SU, Mittler RO (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498

Mittler R, Vanderauwera S, Suzuki N, Miller GA, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16(6):300–309

Møller IM, Sweetlove LJ (2010) ROS signalling-specificity is required. Trends Plant Sci 15(7):370–374

Morita S, Nakatani S, Koshiba T, Masumura T, Ogihara Y, Tanaka K (2011) Differential expression of two cytosolic ascorbate peroxidases and two superoxide dismutase genes in response to abiotic stress in rice. Rice Sci 18(3):157–166

Nanda R, Agrawal V (2018) Piriformospora indica, an excellent system for heavy metal sequestration and amelioration of oxidative stress and DNA damage in Cassia angustifolia Vahl under copper stress. Ecotoxicol Environ Saf 156:409–419

Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

Nouman W, Basra SM, Yasmeen A, Gull T, Hussain SB, Zubair M, Gul R (2014) Seed priming improves the emergence potential, growth and antioxidant system of Moringa oleifera under saline conditions. Plant Growth Reg 73(3):267–278

Ogbe AA, Finnie JF, Van Staden J (2020) The role of endophytes in secondary metabolites accumulation in medicinal plants under abiotic stress. S Afr J Bot 134:126–134

Omomowo OI, Babalola OO (2019) Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms 7:481

Oyekanmi AA, Latiff AAA, Daud Z, Mohamed RMSR, Aziz NAA, Ismail N, Rafatullah M, Ahmad A, Hossain K (2019) Adsorption of pollutants from palm oil mill effluent using natural adsorbents: optimization and isotherm studies. Desalination Water Treat 169:181–190

Oyekanmi AA, Ahmad A, Mohd Setapar SH, Alshammari MB, Jawaid M, Hanafiah MM, Abdul Khalil HPS, Vaseashta A (2021a) sustainable durio zibethinus-derived biosorbents for congo red removal from aqueous solution: statistical optimization, isotherms and mechanism studies. Sustainability 13(23):13264

Oyekanmi AA, Alshammari MB, Ibrahim MNM, Hanafiah MM, Elnaggar AY, Ahmad A, Oyediran AT, Rosli MA, Mohd Setapar SH, Nik Daud NN, Hussein EE (2021b) Highly effective cow bone based biocomposite for the sequestration of organic pollutant parameter from palm oil mill effluent in a fixed bed column adsorption system. Polymers 14(1):86

Ozyigit II, Filiz E, Vatansever R, Kurtoglu KY, Koc I, Öztürk MX, Anjum NA (2016) Identification and comparative analysis of H2O2-scavenging enzymes (ascorbate peroxidase and glutathione peroxidase) in selected plants employing bioinformatics approaches. Front Plant Sci 7:301

Pal KK, Dey R, Sherathia DN, Devidayal MS, Kumar A, Rupapara RB, Mandaliya M, Rawal P, Bhadania RA, Thomas M, Patel MB, Maida P, Nawade BD, Ahmad S, Dash P, Radhakrishnan T (2021) Alleviation of salinity stress in peanut by application of endophytic bacteria. Front Microbiol 12:650771

Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

Paradiso A, Caretto S, Leone A, Bove A, Nisi R, De Gara L (2016) ROS production and scavenging under anoxia and re-oxygenation in Arabidopsis cells: a balance between redox signaling and impairment. Front Plant Sci 7:1803

Parveen A, Saleem MH, Kamran M, Haider MZ, Chen JT, Malik Z, Rana MS, Hassan A, Hur G, Javed MT, Azeem M (2020) Effect of citric acid on growth, ecophysiology, chloroplast ultrastructure, and phytoremediation potential of jute (Corchorus capsularis L.) seedlings exposed to copper stress. Biomolecules 10(4):592

Passari AK, Mishra VK, Singh G, Singh P, Kumar B, Gupta VK, Sarma RK, Saikia R, Donovan AO, Singh BP (2017) Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7(1):1–17

Pavlo A, Leonid O, Iryna Z, Natalia K, Maria PA (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49

Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397(6720):625–628

Phurailatpam L, Mishra S (2020) Role of plant endophytes in conferring abiotic stress tolerance. In: Plant ecophysiology and adaptation under climate change: mechanisms and perspectives II, pp 603–628. Springer, Singapore

Podgórska A, Burian M, Szal B (2017) Extra-cellular but extra-ordinarily important for cells: apoplastic reactive oxygen species metabolism. Front Plant Sci 8:1353

Prasad D, Verma N, Bakshi M, Narayan OP, Singh AK, Dua M, Johri AK (2019) Functional characterization of a magnesium transporter of root endophytic fungus Piriformospora indica. Front Microbiol 9:3231

Pyngrope S, Bhoomika K, Dubey RS (2013) Reactive oxygen species, ascorbate–glutathione pool, and enzymes of their metabolism in drought-sensitive and tolerant indica rice (Oryza sativa L.) seedlings subjected to progressing levels of water deficit. Protoplasma 250(2):585–600

Quiroga G, Erice G, Ding L, Chaumont F, Aroca R, Ruiz-Lozano JM (2019) The arbuscular mycorrhizal symbiosis regulates aquaporins activity and improves root cell water permeability in maize plants subjected to water stress. Plant Cell Environ 42:2274–2290

Radwan DE, Fayez KA, Younis Mahmoud S, Lu G (2010) Modifications of antioxidant activity and protein composition of bean leaf due to Bean yellow mosaic virus infection and salicylic acid treatments. Acta Physiol Plant 32(5):891–904

Ragasa LRP, Joson SEA IV, Bagay WLR, Perez TR, Velarde MC (2021) Transcriptome analysis reveals involvement of oxidative stress response in a copper-tolerant Fusarium oxysporum strain. Fungal Biol 125:435–446

Rana KL, Kour D, Kaur T, Devi R, Yadav AN, Yadav N, Dhaliwal HS, Saxena AK (2020) Endophytic microbes: biodiversity, plant growth-promoting mechanisms and potential applications for agricultural sustainability. Antonie Van Leeuwenhoek Int J General Mol Microbiol 113:1075–1107

Rosli MA, Daud Z, Ridzuan MB, Abd Aziz N, Awang H, Oyekanmi Adeleke A (2019) Equilibrium isotherm and kinetic study of the adsorption of organic pollutants of leachate by using micro peat-activated carbon composite media. Desalin Water Treat 160:185–192

Roychoudhury A, Ghosh S (2013) Physiological and biochemical responses of mungbean (Vigna radiata L. Wilczek) to varying concentrations of cadmium chloride or sodium chloride. Unique J Pharm Biol Sci 1:11–21

Saddique MAB, Ali Z, Khan AS, Rana IA, Shamsi IH (2018) Inoculation with the endophyte Piriformospora indica significantly affects mechanisms involved in osmotic stress in rice. Rice 11:1–12

Sagonda T, Adil MF, Sehar S, Rasheed A, Joan HI, Ouyang Y, Shamsi IH (2021) Physio-ultrastructural footprints and iTRAQ-based proteomic approach unravel the role of Piriformospora indica-colonization in counteracting cadmium toxicity in rice. Ecotoxicol Environ Saf 220:12390

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

Sallaku G, Sandén H, Babaj I, Kaciu S, Balliu A, Rewald BJ (2019) Specific nutrient absorption rates of transplanted cucumber seedlings are highly related to RGR and influenced by grafting method, AMF inoculation and salinity. Sci Hortic 243:177–188

Sandhya VS, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62(1):21–30

Sepehri M, Khatabi B (2021) Combination of siderophore-producing bacteria and Piriformospora indica provides an efficient approach to improve cadmium tolerance in Alfalfa. Microb Ecol 81:717–730

Serfling A, Wirsel SG, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97(4):523–531

Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:187

Shahabivand S, Parvaneh A, Aliloo AA (2017) Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotoxicol Environ Saf 145:496–502

Sharma V, Anderson D, Dhawan A (2012) Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 17(8):852–870

Sharma K, Gupta S, Thokchom SD, Jangir P, Kapoor R (2021) Arbuscular mycorrhiza-mediated regulation of polyamines and aquaporins during abiotic stress: deep insights on the recondite players. Front Plant Sci 12:642101

Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131

Singh A, Roychoudhury A (2021) Augmenting the abiotic stress tolerance in plants through microbial association. Microbial metatranscriptomics belowground. Springer, Singapore, pp 179–198

Sreedevi S, Krishnan PN (2012) Detoxification of heavy metal induced oxidative stress in plants, enzymatic and non-enzymatic machanisms-a mini review. Oxidative stress in plants: causes, consequences and tolerance. IK International Publishing House, New Delhi, pp 291–307

Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF (2004) Mitochondrial α-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24(36):7779–7788

Su Z, Zeng Y, Li X, Perumal AB, Zhu J, Lu X, Lin F (2021) The endophytic fungus Piriformospora indica-assisted alleviation of cadmium in tobacco. J Fungi 7:675

Suebrasri T, Harada H, Jogloy S, Ekprasert J, Boonlue S (2020) Auxin-producing fungal endophytes promote growth of sunchoke. Rhizosphere 16:100271

Suryanarayanan T (2017) Fungal endophytes: an eclectic review. Kavaka 48:1–9

Swetha S, Padmavathi T (2020) Mitigation of drought stress by Piriformospora indica in Solanum melongena L. cultivars. Proc Natl Acad Sci India Sect B Biol Sci 90:585–593

Taghinasab M, Imani J, Steffens D, Glaeser SP, Kogel KH (2018) The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat. Plant Soil 42:339–348

Thakur M, Bhattacharya S, Khosla PK, Puri S (2019) Improving production of plant secondary metabolites through biotic and abiotic elicitation. J Appl Res Med Aromat Plants 12:1–12

Tiwari M, Kumar R, Min D and Krishna Jagadish SV (2022) Genetic and molecular mechanisms underlying root architecture and function under heat stress‐a hidden story. Plant Cell Environ.

Tsai HJ, Shao KH, Chan MT, Cheng CP, Yeh KW, Oelmüller R, Wang SJ (2020) Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ROS scavenging systems. Plant Signal Behav 15:1722447

Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

Tyagi J, Pudake R N (2017) Spectrophotometric assays to evaluate the rhizospheric microbes mediated drought tolerance in plants. In: Modern tools and techniques to understand microbes. Springer, pp 413–429

Tyagi J, Varma A, Pudake RN (2017a) Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. Eur J Soil Biol 81:1–10

Tyagi J, Sultan E, Mishra A, Kumari M, Pudake RN (2017b) The impact of AMF symbiosis in alleviating drought tolerance in field crops. In: Mycorrhiza-nutrient uptake, biocontrol, ecorestoration. Springer, Cham, pp 211–234

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 8:912–923

Ueda Y, Uehara N, Sasaki H, Kobayashi K, Yamakawa T (2013) Impacts of acute ozone stress on superoxide dismutase (SOD) expression and reactive oxygen species (ROS) formation in rice leaves. Plant Physiol Biochem 70:396–402

Unnikumar KR, Sree KS, Varma A (2013) Piriformospora indica: a versatile root endophytic symbiont. Symbiosis 60:107–113

Vahabi K, Dorcheh SK, Monajembashi S, Westermann M, Reichelt M, Falkenberg D, Hemmerich P, Sherameti I, Oelmüller R (2016) Stress promotes Arabidopsis-Piriformospora indica interaction. Plant Signal Behav 11:1136763

Verma SK, White JF Jr (2019) Seed endophytes: biology and biotechnology. Springer, New York

Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903

Verma H, Kumar D, Kumar V, Kumari M, Singh SK, Sharma VK, Droby S, Santoyo G, White JF, Kumar A (2021a) The potential application of endophytes in management of stress from drought and salinity in crop plants. Microorganisms 9:1729

Verma N, Narayan OP, Prasad D, Jogawat A, Panwar SL, Dua M, Johri AK (2021b) Functional characterization of a high‐affinity iron transporter (PiFTR) from the endophytic fungus Piriformospora indica and its role in plant growth and development. Environ Microbiol

Verma SK, Sahu PK, Kumar K, Pal G, Gond SK, Kharwar RN, White JF (2021c) Endophyte roles in nutrient acquisition, root system architecture development and oxidative stress tolerance. J Appl Microbiol 131(5):2161–2177

Volkov V (2015) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci 15:6–873

Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci 102(38):13386–13391

Wang QL, Chen JH, He NY, Guo FQ (2018a) Metabolic reprogramming in chloroplasts under heat stress in plants. Int J Mol Sci 19:849

Wang Y, Branicky R, Noë A, Hekimi S (2018b) Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 217(6):1915–1928

Wang M, Zhang S, Ding F (2020) Melatonin mitigates chilling-induced oxidative stress and photosynthesis inhibition in tomato plants. Antioxidants 9(3):218

Weiß M, Waller F, Zuccaro A, Selosse MA (2016) Sebacinales—one thousand and one interactions with land plants. New Phytol 211(1):20–40

Wen C, Wu Y, Tian X (2004) Recent advances and issues on the endophyte. Chin J Plant Ecol 2:86–91

Wu QS, Zou YN (2017) Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In: Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 25–41

Xie X, He Z, Chen N, Tang Z, Wang Q, Cai Y (2019) The roles of environmental factors in regulation of oxidative stress in plant. BioMed Res Int

Xu L, Wang A, Wang J, Wei Q, Zhang W (2017) Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes. Crop J 5:251–258

Xu L, Wu C, Oelmueller R, Zhang W (2018) Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plants: more questions than answers. Front Microbiol 9:1646

Xu F, Liao H, Zhang Y, Yao M, Liu J, Sun L, Zhang X, Yang J, Wang K, Wang X, Ding Y (2021) Coordination of root auxin with the fungus Piriformospora indica and bacterium Bacillus cereus enhances rice rhizosheath formation under soil drying. ISME J 21:1–11

Yadav V, Arif N, Singh S, Srivastava PK, Sharma S, Tripathi DK, Dubey NK, Chauhan DK (2016) Exogenous mineral regulation under heavy metal stress: advances and prospects. Biochem Pharmacol 5:2167–2501

Yao YQ, Lan F, Qiao YM, Wei JG, Huang RS, Li LB (2017) Endophytic fungi harbored in the root of Sophora tonkinensis Gapnep: diversity and biocontrol potential against phytopathogens. Microbiol Open 6:e00437

Yun P, Xu L, Wang SS, Shabala L, Shabala S, Zhang WY (2018) Piriformospora indica improves salinity stress tolerance in Zea mays L. plants by regulating Na+ and K+ loading in root and allocating K+ in shoot. Plant Growth Regul 86:323–331

Zézél A, Brou YC, Meddich A, Marty F (2008) Molecular identification of MIP genes expressed in the roots of an arbuscular mycorrhizal Trifolium alexandrium L. under water stress. Afr J Agric Res 3:78–83

Zhang W, Wang J, Xu L, Wang A, Huang L, Du H, Qiu L, Oelmüller R (2018) Drought stress responses in maize are diminished by Piriformospora indica. Plant Signal Behav 13(1):e1414121