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Transgenerational benefits of endophytes on resilience and antioxidant genes expressions in pea (Pisum sativum L.) under osmotic stress

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Abstract

Water shortage adversely affects many vital physiological processes in plants. In this study, we present the benefit of plant endophytic fungi and bacteria on endophyte-free second-generation Pisum sativum L. seeds arising from drought-stressed plants. Germination percentage, root and shoot length, reactive oxygen species (ROS) accumulation, antioxidant gene expression and protein content was examined in the F2 generation of pea (CDC Golden). The IOP-PDA and PEG media increased water stress, osmotic pressure and dehydration, respectively, to plants grown in vitro. The transgenerational endophyte-mediated benefits to pea can be appreciated by improved seed germination and reduced ROS accumulation levels in plant-roots. qPCR of antioxidants in leaves revealed downregulated proline, superoxide dismutase (SOD), and manganese superoxide dismutase (MnSOD) genes under water-deficient conditions. This finding implies that endophytes can improve pea’s resilience to abiotic stresses. The protein content increased in seeds produced from F1 plants colonized by endophytic Penicilium SMCD2206, Paraconiothyrium SMCD2210 and Streptomyces sp. SMCD2215 strains compared to endophyte-free plants. The results provide new insights into understanding leguminous plant–endophyte interactions under stress. The mechanisms by which transgenerational endophyte-mediated resilience in plants merit further studies under natural field conditions.

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Abbreviations

DCFH-DA:

2′,7′-Dichlorofluorescin diacetate

IOP-PDA:

Increased osmotic pressure-potato dextrose agar

MnSOD:

Manganese superoxide dismutase

PEG:

Polyethylene glycol 8000

SMCD:

Saskatchewan Microbial Collection and Database

SOD:

Superoxide dismutase

References

  • Abid G, Mingeot D, Muhovski Y, Mergeai G, Aouida M, Abdelkarim S, Aroua I, Ayed ME, Mhamdi M, Sassi K, Jebara M (2017) Analysis of DNA methylation patterns associated with drought stress response in faba bean (Vicia faba L.) using methylation-sensitive amplification polymorphism (MSAP). Environ Exp Bot 142:34–44

    CAS  Google Scholar 

  • Ahmad P, John R, Sarwat M, Umar S (2008) Responses to proline, lipid peroxidation and antioxidative enzymes in two verities of pisum sativum L. under salt stress. IJPP 2:353–366

    CAS  Google Scholar 

  • Almansouri M, Kinet JM, Lutts S (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant Soil 231:243–254

    CAS  Google Scholar 

  • Angioloni A, Collar C (2013) Impact of high hydrostatic pressure on protein aggregation and rheological properties of legume batters. Food Bioproc Tech 6:3576–3584

    CAS  Google Scholar 

  • Bailly C, El- Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 331:806–814

    CAS  PubMed  Google Scholar 

  • Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68

    CAS  PubMed  Google Scholar 

  • Caverzan A, Casassola A, Brammer SP (2016) Reactive oxygen species and antioxidant enzymes involved in plant tolerance to stress. In: Shanker AK, Shanker C (eds) Abiotic and biotic stress in plants - Recent advances and future perspectives. InTech Inc, Rijeka, Croatia, pp 463–480

    Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    PubMed  Google Scholar 

  • Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA (2013) Root Traits Contributing to Plant Productivity under Drought. Front Plant Sci:442

  • Cousin R (1997) Peas (Pisum sativum L.). Field Crop Res 53:111–130

    Google Scholar 

  • Dhar MK, Vishal P, Sharma R, Kaul S (2014) Epigenetic dynamics: role of epimarks and underlying machinery in plants exposed to abiotic stress. Int J Plant Genomics. https://doi.org/10.1155/2014/187146

    Article  Google Scholar 

  • Elbersen HW, West CP (1996) Growth and water relations of field-grown tall fescue as influenced by drought and endophyte. Grass Forage Sci 51:333–342

    Google Scholar 

  • Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2017) Drought stress in grain legumes during reproduction and grain filling. J Agron Crop Sci 203:81–102

    Google Scholar 

  • Gamze OKCU, Mehmet Demir KAYA, Mehmet ATAK (2005) Effects of salt and drought stresses on germination and seedling growth of pea (Pisum sativum L.). Turk J Agric For 29:237–242

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hamayun M, Khan SA, Kim HY, Chaudhary MF, Hwang YH, Shin DH, Kim IK, Lee BH, Lee IJ (2009) Gibberellin production and plant growth enhancement by newly isolated strain of Scolecobasidium tshawytschae. J Microbiol Biotechnol 19:560–565

    CAS  PubMed  Google Scholar 

  • Harb A, Awada D, Samarahb N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought. J Plant Interact 10:109–116

    CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbard M, Germida JJ, Vujanovic V (2014) Fungal endophyte colonization coincides with altered DNA methylation in drought-stressed wheat seedlings. Can J Plant Sci 94:223–234

    CAS  Google Scholar 

  • Hubbard M, Germida JJ, Vujanovic V (2013) Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability. J Appl Microbiol 116:109–122

    PubMed  Google Scholar 

  • Hubbard M, Germida J, Vujanovic V (2012) Fungal endophytes improve wheat seed germination under heat and drought stress. Botany 90:137–149

    Google Scholar 

  • Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants 4:393–411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jerry B (1994) A role of endophytic fungi in regulating nutrients and energy in plants with in a desert ecosystem. International Symposium and Workshop on Desertification in Developed Countries: Why Can't We Control It? https://jornada.nmsu.edu/biblio/role-endophytic-fungi-regulating-nutrients-and-energy-plants-within-desert-ecosystem. Cited 25 Oct 2011

  • Karataş İ, Öztürk L, Demir Y, Ünlükara A, Kurunç A, Düzdemir O (2014) Alterations in antioxidant enzyme activities and proline content in pea leaves under long-term drought stress. Toxicol Ind Health 30:693–700

    PubMed  Google Scholar 

  • Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (2012a) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth potential in abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AL, Shinwari ZK, Kim YH, Waqas M, Hamayun M, Kamran M, IEEE J (2012b) Role of Chaetomium globosum lk4 in Capsicum annum l. growth by production of gibberellins and IAA. Pak J Bot 44:1601–1607

    Google Scholar 

  • Khan AL, Hamayun M, Radhakrishnan R, Waqas M, Kang SM, Kim YH, Shin JH, Choo YS, Kim JG, Lee IJ (2012c) c) Mutualistic association of endophyte Paecilomyces formosus LHL10 offered thermotolerance to Cucumis sativus. Antonie Van Leeuwenhoek 101:267–279

    PubMed  Google Scholar 

  • Kumari V, Germida J, Vujanovic V (2018) Legume endosymbionts: Drought stress tolerance in second-generation chickpea (Cicer arietinum) seeds. J Agron Crop Sci 204:529–540

    CAS  Google Scholar 

  • Lal RK (1985) Effect of salinity applied at different stages of growth on seed yield and its constituents in field peas (Pisum sativum L. var. arvensis). Ind J Agronomy 30:296–299

    Google Scholar 

  • Magyar-Tábori K, Mendler-Drienyovszki N, Dobránszki J (2011) Models and tools for studying drought stress responses in peas. OMICS 15:829–838

    PubMed  Google Scholar 

  • Muscolo A, Sidari M, Anastasi U, Santonoceto C, Maggio A (2014) Effect of PEG-induced drought stress on seed germination of four lentil genotypes. J Plant Interact 9:354–363

    CAS  Google Scholar 

  • Mus F, Crook MB, Garcia K, Costas AG, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ane JM, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbio 82:3698–3710

    CAS  Google Scholar 

  • Mustafa BM, Coram TE, Pang ECK, Taylor PWJ, Ford R (2009) A cDNA microarray approach to decipher lentil (Lens culinaris) responses to Ascochyta lentis. Australas Plant Pathol 38:617–631

    CAS  Google Scholar 

  • Naim-Feil E, Toren M, Aubert G, Rubinstein M, Rosen A, Eshed R, Sherman A, Ophir R, Saranga Y, Abbo S (2017) Drought response and genetic diversity in pisum fulvum, a wild relative of domesticated pea. Crop Sci 57:1145–1159

    Google Scholar 

  • Nakamura N, Marutani M, Sanematsu S, Toyoda K, Inagaki Y-S, Shiraishi T, Ichinose Y (2003) Phylogenetic classification of Dof-type transcription factors in Pea (Pisum sativum). Plant Biotechnol J 20:247–252

    CAS  Google Scholar 

  • Osman HS (2015) Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann Agric Sci 60:389–402

    Google Scholar 

  • Olle M (2017) The yield, height and content of protein of field peas (Pisum sativum L.) in Estonian agro-climatic conditions. Agron Res. https://doi.org/10.15159/ar.17.026

    Article  Google Scholar 

  • Peng H, Cheng H-Y, Chen C, Yu X-W, Yang J-N, Gao W-R, Shi QH, Zhang H, Li JG, Ma H (2009) A NAC transcription factor gene of chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. J Plant Physiol 166:1934–1945

    CAS  PubMed  Google Scholar 

  • Qawasmeh A, Objed HK, Raman A, Wheatley W (2012) Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: interaction between Lolium perenne and different strains of Neotyphodium lolii. J Agric Food Chem 60:3381–3388

    CAS  PubMed  Google Scholar 

  • Ravikanth G, Kumari MMV, Nataraja KN, Shaanker RM (2017) Enhancing climate resilience of crop plants: an approach using endophytes. Mysore J Agric Sci 51:63–71

    Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716

    PubMed  Google Scholar 

  • Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114

    CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101

    CAS  PubMed  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root colonizing endophyte Pirifomospora indica confers drought tolerance in arabidopsis by stimulating the expression of drought stress–related genes in leaves. Mol Plant Microbe Interact 21:799–807

    CAS  PubMed  Google Scholar 

  • Shukla N, Awasthi RP, Rawat L, Kumar J (2015) Seed biopriming with drought tolerant isolates of Trichoderma harzianum promote growth and drought tolerance in Triticum aestivum. Ann Appl Biol 166:171–182

    CAS  Google Scholar 

  • Singh RK, Malik N, Singh S (2013) Improved nutrient use efficiency increases plant growth of rice with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RRE25. Microb Ecol 66:375–384

    CAS  PubMed  Google Scholar 

  • Tayeh N, Aubert G, Pilet-Nayel ML, Lejeune-Hénaut I, Warkentin TD, Burstin J (2015) Genomic tools in pea breeding programs: status and perspectives. Front Plant Sci 6:1037

    PubMed  PubMed Central  Google Scholar 

  • Toker C, Mutlu N (2011) Breeding for abiotic stress. In: Pratap A, Kumar J (eds) Biology and breeding of food legumes. CAB International, Wallingford, pp 241–260

    Google Scholar 

  • Tuteja N, Gill SS, Tuteja R (2011) Plant responses to abiotic stresses: Shedding light on salt, drought, cold and heavy metal stress. In: Tuteja N, Gill SS, Tuteja R (eds) Omics and plant abiotic stress tolerance. Bentham Science Publishers Ltd., Beijing, pp 39–64

    Google Scholar 

  • Vujanovic V, Germida JJ (2017) Seed endosymbiosis: a vital relationship in providing prenatal care to plants. CJPS 97:1–10

    Google Scholar 

  • Vujanovic V, Islam MN, Daida P (2019a) Transgenerational role of seed mycobiome – an endosymbiotic fungal composition as a prerequisite to stress resilience and adaptive phenotypes in Triticum. Sci Rep 9:18483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vujanovic V, Kim SH, Lahlali R, Karunakaran C (2019b) Spectroscopy and SEM imaging reveal endosymbiont-dependent components changes in germinating kernel through direct and indirect coleorhiza-fungus interactions under stress. Sci Rep 9:1665

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Gao W, Zhang J, Zhang H, Li J, He X, Ma H (2010) Subunit, amino acid composition and in vitro digestibility of protein isolates from Chinese Kabuli and desi chickpea (Cicer arietinum L.) cultivars. Food Res Int 43:567–572

    CAS  Google Scholar 

  • Wang N, Hatcher DW, Gawalko EJ (2008) Effect of variety and processing on nutrients and certain anti-nutrients in field peas (Pisum sativum). Food Chem 111:132–138

    CAS  Google Scholar 

  • Waqas M, Khan AL, Lee IJ (2014) Bioactive chemical constituents produced by endophytes and effects on rice plant growth. J Plant Interact 9:478–487

    CAS  Google Scholar 

  • Williamson CL, Slocum RD (1992) Molecular cloning and evidence for osmoregulation of the delta 1-pyrroline-5-carboxylate reductase (proC) gene in pea (Pisum sativum L.). Plant Physiol 100:1464–1470

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wong-Vega L, John JB, Randy AD (1991) Isolation and sequence analysis of a cDNA that encodes pea manganese superoxide dismutase. Plant Mol Biol 17:1271–1274

    CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by the NSERC discovery research grant (RGPIN-2017-05286) and Genome Canada-Genome Prairie to Dr. V. Vujanovic.

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Correspondence to Vladimir Vujanovic.

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Kumari, V., Vujanovic, V. Transgenerational benefits of endophytes on resilience and antioxidant genes expressions in pea (Pisum sativum L.) under osmotic stress. Acta Physiol Plant 42, 49 (2020). https://doi.org/10.1007/s11738-020-03042-y

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