Abstract
The filamentous fungi Trichoderma spp. are widely used for plant growth promotion and disease control. They form stable symbiosis-like relationship with roots. Unlike plant pathogens and mycorrhizae, the molecular events leading to the development of this association is not well understood. Pathogens deploy effector proteins to suppress or evade plant defence. Indirect evidences suggest that Trichoderma spp. can also deploy effector-like proteins to suppress plant defence favouring colonization of roots. Here, using computer simulation, we provide evidence that Trichoderma virens may deploy analogues of host defence proteins to “neutralize” its own effector protein to minimize damage to host tissues, as one of the mechanisms to achieve a stable symbiotic relationship with plants. We provide evidence that T. virens Bys1 protein has a structure similar to plant PR5/thaumatin-like protein and can bind Alt a 1 with a very high affinity, which might lead to the inactivation of its own effector protein. We have, for the first time, predicted a fungal protein that is a competitive inhibitor of a fungal effector protein deployed by many pathogenic fungi to suppress plant defence, and this protein/gene can potentially be used to enhance plant defence through transgenic or other approaches.
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References
Alonso-Ramírez A, Poveda J, Martín I, Hermosa R, Monte E, Nicolás C (2014) Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol Plant Pathol 15:823–831
Amadei A, Linssen AB, Berendsen HJ (1993) Essential dynamics of proteins. Proteins Struct Funct Bioinform 17:412–425
Benkert P, Tosatto SC, Schomburg D (2008) QMEAN: a comprehensive scoring function for model quality assessment. Proteins Struct Funct Bioinform 71:261–277
Burg EF, Smith LH (1994) Cloning and characterization of bys1, a temperature-dependent cDNA specific to the yeast phase of the pathogenic dimorphic fungus Blastomyces dermatitidis. Infect Immun 62:2521–2528
Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: a protein–protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125:1731–1737
Duan Y, Wu C, Chowdhury S et al (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comp Chem 24:1999–2012
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Gómez-Casado C, Murua-García A, Garrido-Arandia M et al (2014) Alt a 1 from Alternaria interacts with PR5 thaumatin-like proteins. FEBS Lett 588:1501–1508
Gorman Z, Christensen SA, Yan Y et al (2020) Green leaf volatiles and jasmonic acid enhance susceptibility to anthracnose diseases caused by Colletotrichum graminicola in maize. Mol Plant Pathol 21:702–715
Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–772
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25
Hess B (2000) Similarities between principal components of protein dynamics and random diffusion. Phys Rev E 62:8438
Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolym Orig Res Biomol 22:2577–2637
Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209
Koiwa H, Kato H, Nakatsu T, Oda JI, Yamada Y, Sato F (1999) Crystal structure of tobacco PR-5d protein at 1.8 Å resolution reveals a conserved acidic cleft structure in antifungal thaumatin-like proteins. J Mol Biol 286:1137–1145
Kozakov D, Hall DR, Xia B et al (2017) The ClusPro web server for protein–protein docking. Nat Prot 12:255
Krajaejun T, Wüthrich M, Gauthier GM, Warner TF, Sullivan TD, Klein BS (2010) Discordant influence of Blastomyces dermatitidis yeast-phase-specific gene BYS1 on morphogenesis and virulence. Infect Immun 78:2522–2528
Kumar R, Mukherjee PK (2020) Trichoderma virens Alt a 1 protein may target maize PR5/thaumatin-like protein to suppress plant defence: an in silico analysis. Physiol Mol Plant Path 112:101551
Kumar R, Saran S (2018) Structure, molecular dynamics simulation, and docking studies of Dictyostelium discoideum and human STRAPs. J Cell Biochem 119:7177–7191
Kumar R, Maurya R, Saran S (2019) Introducing a simple model system for binding studies of known and novel inhibitors of AMPK: a therapeutic target for prostate cancer. J Biomol Struct Dyn 37:781–795
Lamdan NL, Shalaby S, Ziv T, Kenerley CM, Horwitz BA (2015) Secretome of Trichoderma interacting with maize roots: role in induced systemic resistance. Mol Cell Prot 14:1054–1063
Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291
Liao D, Wang S, Cui M, Liu J, Chen A, Xu G (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. Int J Mol Sci 19:3146
Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol 48:395–417
Malinich EA, Wang K, Mukherjee PK, Kolomiets M, Kenerley CM (2019) Differential expression analysis of Trichoderma virens RNA reveals a dynamic transcriptome during colonization of Zea mays roots. BMC Genom 20(1):280
Martínez-Medina A, Appels FV, van Wees SC (2017) Impact of salicylic acid-and jasmonic acid-regulated defences on root colonization by Trichoderma harzianum T-78. Plant Signal Behav 12(8):e1345404
Maurya R, Kumar R, Saran S (2020) AMPKα promotes basal autophagy induction in Dictyostelium discoideum. J Cell Physiol 235:4941–4953
Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R et al (2018) Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fun Biol Rev 32:62–85
Mukherjee PK, Mehetre ST, Sherkhane PD et al (2019) A novel seed-dressing formulation based on an improved mutant strain of Trichoderma virens, and its field evaluation. Front Microbiol 10:1910
Nicolás C, Hermosa R, Rubio B, Mukherjee PK, Monte E (2014) Trichoderma genes in plants for stress tolerance-status and prospects. Plant Sci 228:71–78
Nie HZ, Zhang L, Zhuang HQ et al (2019) The secreted protein MoHrip1 is necessary for the virulence of Magnaporthe oryzae. Int J Mol Sci 20(7):1643
Pachauri S, Sherkhane PD, Kumar V, Mukherjee PK (2020) Whole genome sequencing reveals major deletions in the genome of M7, a gamma ray-induced mutant of Trichoderma virens that is repressed in conidiation, secondary metabolism, and mycoparasitism. Front Microbiol 11:1030
Plett JM, Daguerre Y, Wittulsky S et al (2014a) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci 111:8299–8304
Plett JM, Khachane A, Ouassou M, Sundberg B, Kohler A, Martin F (2014b) Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytol 202:270–286
Rahman TA, Oirdi ME, Gonzalez-Lamothe R, Bouarab K (2012) Necrotrophic pathogens use the salicylic acid signaling pathway to promote disease development in tomato. Mol Plant Microbe Interact 25:1584–1593
Rose PW, Beran B, Bi C et al (2010) The RCSB Protein Data Bank: redesigned web site and web services. Nucl Acids Res 9(suppl_1):D392–D401
Sharpee W, Oh Y, Yi M et al (2017) Identification and characterization of suppressors of plant cell death (SPD) effectors from Magnaporthe oryzae. Mol Plant Pathol 18:850–863
Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ (2005) GROMACS: fast, flexible, and free. J Comp Chem 26:1701–1718
Vizcaíno JA, González FJ, Suárez MB et al (2006) Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. BMC Genom 7(1):193
Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Prot Eng Des Sel 8:127–134
Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucl Acids Res 35(suppl_2):W407–W410
Wiesel L, Newton AC, Elliott I et al (2014) Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front Plant Sci 5:655
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform 9(1):40
Zhang Y, Gao Y, Liang Y, Dong Y, Yang X, Qiu D (2019) Verticillium dahliae PevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection. J Exp Bot 70:613–626
Acknowledgements
P.K.M. thanks Dr. S.K. Ghosh, Associate Director, Bioscience Group, BARC, for encouragement and support.
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The work was supported by institutional funding in the absence of any externally funded projects.
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Kumar, R., Mukherjee, P.K. Trichoderma virens Bys1 may competitively inhibit its own effector protein Alt a 1 to stabilize the symbiotic relationship with plant-evidence from docking and simulation studies. 3 Biotech 11, 144 (2021). https://doi.org/10.1007/s13205-021-02652-8
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DOI: https://doi.org/10.1007/s13205-021-02652-8