1,266
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

Comparative metabolomic profiling reveals molecular mechanisms underlying growth promotion and disease resistance in wheat conferred by Piriformospora indica in the field

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 2213934 | Received 09 Jan 2023, Accepted 20 Feb 2023, Published online: 25 May 2023

References

  • Shewry PR, Hawkesford MJ, Piironen V, Lampi AM, Gebruers K, Boros D, Andersson AA, Aman P, Rakszegi M, Bedo Z, et al. Natural variation in grain composition of wheat and related cereals. J Agric Food Chem. 2013;61(35):8295–11. doi:10.1021/jf3054092.
  • Chapin III F III, Zavaleta E, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE et al, Consequences of changing biodiversity. Nature. 2000;405(6783):234–242. doi:10.1038/35012241.
  • Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421(6918):37–42. doi:10.1038/nature01286.
  • Bleša D, Matušinský P, Sedmíková R, Baláž M. The potential of rhizoctonia-like fungi for the biological protection of cereals against fungal pathogens. Plants (Basel). 2021;10(2):349. doi:10.3390/plants10020349.
  • Serfling A, Wirsel SG, Lind V, Deising HB. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology. 2007;97(4):523–531. doi:10.1094/PHYTO-97-4-0523.
  • Borowicz VA. Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology. 2001;82(11):3057–3068. doi:10.1890/0012-9658(2001)082[3057:DAMFAP]2.0.CO;2.
  • Gernns H, Alten H, Poehling HM. Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen-is a compensation possible? Mycorrhiza. 2001;11(5):237–243. doi:10.1007/s005720100128.
  • Rai J, Pemmasani JK, Voronovsky A, Jensen IS, Manavalan A, Nyengaard JR, Golas MM, Sander B. Strep-tag II and twin-strep based cassettes for protein tagging by homologous recombination and characterization of endogenous macromolecular assemblies in Saccharomyces cerevisiae. Mol Biotechnol. 2014;56(11):992–1003. doi:10.1007/s12033-014-9778-5.
  • Schmidt B, Gaşpar S, Camen D, Ciobanu I, Sumălan R. Arbuscular mycorrhizal fungi in terms of symbiosis-parasitism continuum. Commun Agric Appl Biol Sci. 2011;76:653–659.
  • Weiss M, Selosse M, Rexer K, Urban A, Oberwinkler F. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res. 2004;108(9):1003–1010. doi:10.1017/s0953756204000772.
  • Varma A, Singh A, Sudha,Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D. et al. 2001. Piriformospora indica: an axenically culturable mycorrhiza-like endosymbiotic fungus. The Mycota. Springer: Berlin, Heidelberg; p. 125–150. doi:10.1007/978-3-662-07334-6_8.
  • Atia MAM, Abdeldaym EA, Abdelsattar M, Ibrahim DSS, Saleh I, Elwahab MA, Osman GH, Arif IA, Abdelaziz ME. Piriformospora indica promotes cucumber tolerance against root-knot nematode by modulating photosynthesis and innate responsive genes. Saudi J Biol Sci. 2020;27(1):279–287. doi:10.1016/j.sjbs.2019.09.007.
  • Daneshkhah R, Cabello S, Rozanska E, Sobczak M, Grundler FM, Wieczorek K, Hofmann J. Piriformospora indica antagonizes cyst nematode infection and development in Arabidopsis roots. J Exp Bot. 2013;64(12):3763–3774. doi:10.1093/jxb/ert213.
  • Li L, Li L, Wang X, Zhu P, Wu H, Qi S. Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiol Biochem. 2017;119:211–223. doi:10.1016/j.plaphy.2017.08.029.
  • Xu L, Wang A, Wang J, Qiao W, Zhang W. Piriformospora indica confers drought tolerance on Zea Mays L. through enhancement of antioxidant activity and expression of drought-related genes. null. 2017;5(3):251–258. doi:10.1016/j.cj.2016.10.002.
  • Vahabi K, Dorcheh SK, Monajembashi S, Westermann M, Reichelt M, Falkenberg D, Hemmerich P, Sherameti I, Oelmüller R. Stress promotes Arabidopsis-Piriformospora indica interaction. Plant Signaling & Behavior. 2016;11(5):e1136763. doi:10.1080/15592324.2015.1136763.
  • Varma A, Verma S, Sahay N, Büttehorn B, Franken P, Franken P. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microb. 1999;65(6):2741–2744. doi:10.1128/AEM.65.6.2741-2744.1999.
  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fisher M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci. 2005;102(38):13386–13391. doi:10.1073/pnas.0504423102.
  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 2008;180(2):501–510. doi:10.1111/j.1469-8137.2008.02583.x.
  • Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, Kogel KH. Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol. 2008;165(1):60–70. doi:10.1016/j.jplph.2007.05.017.
  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R. The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem. 2005;280(28):26241–26247. doi:10.1074/jbc.M500447200.
  • Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Christian M, Scheel D, Lee J, Oelmüller R. A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. The Plant Journal. 2010;59(2):193–206. doi:10.1111/j.1365-313X.2009.03867.x.
  • Venneman J, Audenaert K, Verwaeren J, Baert G, Boeckx P, Moango AM, Dhed’a BD, Vereecke D, Haesaert G. Congolese rhizospheric soils as a rich source of new plant growth-promoting endophytic Piriformospora isolates. Front Microbiol. 2017;8:212. doi:10.3389/fmicb.2017.00212.
  • Stein E, Molitor A, Kogel K, Waller F. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol. 2008;49(11):1747–1751. doi:10.1093/pcp/pcn147.
  • Trzewik A, Maciorowski R, Klocke E, Orlikowska T. The influence of Piriformospora indica on the resistance of two rhododendron cultivars to Phytophthora cinnamomi and P. plurivora. Biol Control. 2020;140:104121. doi:10.1016/j.biocontrol.2019.104121.
  • Wang H, Zheng J, Ren X, Yu T, Varma A, Lou B, Zheng X. Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV. Plant Growth Regul. 2015;76(3):303–313. doi:10.1007/s10725-015-0025-2.
  • Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci. 2006;103(49):18450–18457. doi:10.1073/pnas.0605697103.
  • Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P. The mutualistic fungus piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress–triggered caspase-dependent cell death. Plant Cell. 2012;24(2):794–809. doi:10.1105/tpc.111.093260.
  • Salem R, Arif IA, Salama M, Osman G. Polyclonal antibodies against the recombinantly expressed coat protein of the Citrus psorosis virus. Saudi J Biol Sci. 2018;25(4):733–738. doi:10.1016/j.sjbs.2017.10.018.
  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza. 2010;20(3):191–200. doi:10.1007/s00572-009-0279-5.
  • Sarma MV, Kumar V, Saharan K, Srivastava R, Sharma AK, Prakash A, Sahai V, Bisaria VS. Application of inorganic carrier-based formulations of fluorescent pseudomonads and Piriformospora indica on tomato plants and evaluation of their efficacy. J Appl Microbiol. 2011;111(2):456–466. doi:10.1111/j.1365-2672.2011.05062.x.
  • Sun C, Shao Y, Vahabi K, Lu J, Bhattacharya S, Dong S, Yeh KW, Sherameti I, Lou B, Baldwin IT, et al. The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliae infection by downregulation plant defense responses. BMC Plant Biol. 2014;14(1):268. doi:10.1186/s12870-014-0268-5.
  • Zuccaro A, Basiewicz M, Zurawska M, Biedenkopf D, Kogel K. Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica. Fungal Genet Biol. 2009;46(8):543–550. doi:10.1186/s12870-014-0268-5.
  • Kundu A, Mishra S, Kundu P, Jogawat A, Vadassery J. Piriformospora indica recruits host-derived putrescine for growth promotion in plants. Plant Physiol. 2021;16:kiab536. doi:10.1093/plphys/kiab536.
  • Li Q, Kuo Y, Lin K, Huang W, Deng C, Yeh K, Chen SP. Piriformospora indica colonization increases the growth, development, and herbivory resistance of sweet potato (Ipomoea batatas L.). Plant Cell Rep. 2021;40(2):339–350. doi:10.1007/s00299-020-02636-7.
  • Bertolazi AA, de Souza SB, Ruas KF, Campostrini E, de Rezende CE, Cruz C, Melo J, Colodete CM, Varma A, Ramos AC, et al. Inoculation with Piriformospora indica is more efficient in wild-type rice than in transgenic rice over-expressing the vacuolar H+-ppase. null. 2019;10:1087. doi:10.3389/fmicb.2019.01087.
  • Kumar M, Yadav V, Tuteja N, Johri AK. Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology. 2009;155(3):780–790. doi:10.1099/mic.0.019869-0.
  • Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmüller R, Yeh KW. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant-Microbe Interactions. 2011;24(4):421–431. doi:10.1094/MPMI-05-10-0110.
  • Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K. Piriformospora indica affects plant growth by auxin production. Physiol Plant. 2007;131(4):581–589. doi:10.1111/j.1399-3054.2007.00983.x.
  • Bakshi M, Sherameti I, Meichsner D, Thürich J, Varma A, Johri AK, Yeh KW, Oelmüller R. Piriformospora indica reprograms gene expression in Arabidopsis phosphate metabolism mutants but does not compensate for phosphate limitation. null. 2017;8:1262. doi:10.3389/fmicb.2017.01262.
  • Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 2011;7(10):e1002290. doi:10.1371/journal.ppat.1002290.
  • Achatz B, Kogel KH, Franken P, Waller F. Piriformospora indica mycorrhization increases grain yield by accelerating early development of barley plants. Plant Signal Behav. 2010;5(12):1685–1687. doi:10.4161/psb.5.12.14112.
  • Kundu A, Vadassery J. Molecular mechanisms of Piriformospora indica mediated growth promotion in plants. Plant Signal Behav. 2022;17(1):2096785. doi:10.1080/15592324.2022.2096785.
  • Sun RT, Feng XC, Zhang ZZ, Zhou N, Feng HD, Liu YM, Hashem A, Al-Arjani AF, Abd Allah EF, Wu QS. Root endophytic fungi regulate changes in sugar and medicinal compositions of Polygonum cuspidatum. Front Plant Sci. 2022;13:818909. doi:10.3389/fpls.2022.818909.
  • Liu HC, Senthilkumar R, Ma GY, Zou QC, Zhu KY, Shen XL, Tian DQ, Hua SM, Oelmüller R, Yeh KW. Piriformospora indica-induced phytohormone changes and root colonization strategies are highly host-specific. Plant Signal Behav. 2019;14(9):9, 1632688. doi:10.1080/15592324.2019.1632688.
  • Sherameti I, Tripathi S, Varma A, Oelmüller R. 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 Interactions. 2008;21(6):799–807. doi:10.1094/MPMI-21-6-0799.
  • Das A, Kamal S, Shakil NA, Sherameti I, Oelmüller R, Dua M, Tuteja N, Johri AK, Varma A. The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii. Plant Sign Behav. 2012;7(1):1–10. doi:10.4161/psb.7.1.18472.
  • Pan R, Xu L, Wei Q, Wu C, Tang W, Oelmüller R, Zhang W, Zhou M. Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photoperiod and gibberellin pathways. PLos One. 2017;12(12):e0189791. doi:10.1371/journal.pone.0189791.
  • Hua MS, SenthilKumar R, Shyur LF, Cheng YB, Tian ZH, Oelmuller R, Yeh KW. Metabolomic compounds identified in Piriformospora indica-colonized Chinese cabbage roots delineate symbiotic functions of the interaction. null. 2017;7(1):1. doi:10.1038/s41598-017-08715-2.
  • Tsai HJ, Shao KH, Chan MT, Cheng CP, Wang SJ, Oelmüller R, Wang S-J. Piriformospora indica symbiosis improves water stress tolerance of rice through regulating stomata behavior and ros scavenging systems. Plant Signal Behav. 2020;15(2):1722447. doi:10.1080/15592324.2020.1722447.
  • Davies KM, Landi M, van Klink JW, Schwinn KE, Brummell DA, Albert NW, Chagné D, Jibran R, Kulshrestha S, Zhou Y, et al. Evolution and function of red pigmentation in land plants. Ann Bot. 2022;17(5):613–636. doi:10.1093/aob/mcac109.
  • Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008;54(4):733–749. doi:10.1111/j.1365-313X.2008.03447.x.
  • Liu H, Wang Z, Xu W, Zeng J, Li L, Li S, Gao Z. Bacillus pumilus LZP02 promotes rice root growth by improving carbohydrate metabolism and phenylpropanoid biosynthesis. Mol Plant-Microbe Interactions. 2020;33(10):1222–1231. doi:10.1094/MPMI-04-20-0106-R.
  • Yu G, Wang L, Han Y, He Q. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16(5):284–287. doi:10.1089/omi.2011.0118.