Triggering the biocontrol of Botrytis cinerea by Trichoderma harzianum through inhibition of pathogenicity and virulence related proteins

Kandasamy SARAVANAKUMAR, Zhixiang LU, Hai XIA, Meng WANG, Jianan SUN, Shaoqing WANG, Qiang-qiang WANG, Yaqian LI, Jie CHEN

PDF(1202 KB)
PDF(1202 KB)
Front. Agr. Sci. Eng. ›› 2018, Vol. 5 ›› Issue (2) : 271-279. DOI: 10.15302/J-FASE-2018214
RESEARCH ARTICLE
RESEARCH ARTICLE

Triggering the biocontrol of Botrytis cinerea by Trichoderma harzianum through inhibition of pathogenicity and virulence related proteins

Author information +
History +

Abstract

This study reports a strain of Trichoderma harzianum CCTCC-SBW0162 with potential to enhance biocontrol activity against gray mold pathogen, Botrytis cinerea, and with a pivotal role in tomato (Solanum esculentum) plant growth enhancement. A total of 254 Trichoderma isolates were screened by in vitro antagonistic assay. Of these, 10 were selected for greenhouse experiments based on their greater inhibition of B. cinerea. The in vitro antagonistic assay and greenhouse experiments indicated that T. harzianum CCTCC-SBW0162 gave the highest inhibition rate (90.6%) and disease reduction (80.7%). Also, to study the possible mechanism associated with antifungal activity of CCTCC-SBW0162 against B. cinerea, molecular docking was used to assess the interactions between CCTCC-SBW0162-derived metabolites, and pathogencity and virulence related proteins of B. cinerea. The molecular docking results indicated that the combination of harzianopyridone, harzianolide and anthraquinone C derived from CCTCC-SBW0162 could synergistically improve antifungal activity against B. cinerea through the inhibition/modification of pathogenicity and virulence related proteins. However, this computerized modeling work emphasized the need for further study in the laboratory to confirm the effect T. harzianum-derived metabolites against the proteins of B. cinerea and their interactions.

Keywords

anthraquinone / Botrytis cinerea / harzianolide / harzianopyridone / molecular docking / Trichoderma harzianum

Cite this article

Download citation ▾
Kandasamy SARAVANAKUMAR, Zhixiang LU, Hai XIA, Meng WANG, Jianan SUN, Shaoqing WANG, Qiang-qiang WANG, Yaqian LI, Jie CHEN. Triggering the biocontrol of Botrytis cinerea by Trichoderma harzianum through inhibition of pathogenicity and virulence related proteins. Front. Agr. Sci. Eng., 2018, 5(2): 271‒279 https://doi.org/10.15302/J-FASE-2018214

References

[1]
Dean R, Van Kan J A, Pretorius Z A, Hammond-Kosack K E, Di Pietro A, Spanu P D, Rudd J J, Dickman M, Kahmann R, Ellis J, Foster G D. The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 2012, 13(4): 414–430
CrossRef Pubmed Google scholar
[2]
Montealegre J R, Herrera R, Velasquez J C, Silva P, Besoain X, Perez L M. Biocontrol of root and crown rot in tomatoes under greenhouse conditions using Trichoderma harzianum and Paenibacillus lentimorbus. Additional effect of solarization. Electronic Biotechnology, 2005, 8(3): 249–257
CrossRef Google scholar
[3]
Srinon W, Chuncheen K, Jirattiwarutkul K, Soytong K, Kanokmedhakul S. Efficacies of antagonistic fungi against Fusarium wilt disease of cucumber and tomato and the assay of its enzyme activity. Agricultural Technology, 2006, 2(2): 191–201
[4]
Talla S G, Raju A S R, Karri S, Kumar Y S. Production and antagonistic effect of Trichoderma spp. on pathogenic microorganisms (Botrytis cinerea, Fusarium oxysporium Macrohomina phasealina and Rhizoctonia solani). African Journal of Biotechnology, 2015, 14(8): 668–675 doi:10.5897/AJB2014.13904
[5]
Parry D W. Diseases of potato. In: Plant pathology in agriculture.Cambridge, UK: Cambridge University Press, 1990
[6]
Weller D M, Raaijmakers J M, Gardener B B M, Thomashow L S. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 2002, 40(1): 309–348
CrossRef Pubmed Google scholar
[7]
Huang H C, Erickson R S, Chang C, Moyer J R, Larney F J, Huang J W. Control of white mold of bean caused by Sclerotinia sclerotiorum using organic soil amendments and biocontrol agents. Plant Pathology Bulletin, 2005, 14(3): 183–190
[8]
Harman G E, Latorre B, Agosin E, Martin R S, Riegel D G, Nielsen P A, Tronsmo A, Pearson R C. Biological and integrated control of Botrytis bunch rot of grape using Trichoderma spp. Biological Control, 1996, 7(3): 259–266
CrossRef Google scholar
[9]
Zimand G, Elad Y, Chet I. Effect of Trichoderma harzianum on Botrytis cinerea pathogenicity. Phytopathology, 1996, 86(11): 1255–1260
CrossRef Google scholar
[10]
Fravel D R, Rhodes D J, Larkin R P. Biological control of diseases: production and commercialization of biocontrol products. In: Clercq P D. Integrated Pest and Disease Management in Greenhouse Crops.Wageningen: Springer Netherlands, 1999, 365–376
[11]
Joshi B B, Bhatt R P, Bahukhandi D. Antagonistic and plant growth activity of Trichoderma isolates of Western Himalayas. Journal of Environmental Biology, 2010, 31(6): 921–928
Pubmed
[12]
Benítez T, Rincón A M, Limón M C, Codón A C. Biocontrol mechanisms of Trichoderma strains. International Microbiology, 2004, 7(4): 249–260
Pubmed
[13]
Soytong K, Srinon W, Rattanacherdchai K, Kanokmedhakul S, Kanokmedhakul K. Application of antagonistic fungi to control anthracnose disease of grape. Journal of Agricultural Biotechnology, 2005, 1: 33–41
[14]
Morsy E M. Role of growth promoting substances producing microorganisms on tomato plant and control of some root rot fungi. Dissertation for the Doctoral Degree. Cairo: Ain shams University, 2005
[15]
Zaghloul R A, Hanafy Ehsan A, Neweigy N A, Khalifa Neamat A. Application of biofertilization and biological control for tomato production. In: 12th Conference of Microbiology 2005, Cairo. Egypt: Factory of Agriculture, Benha University, 2007, 198–212
[16]
Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J. Biodiversity of Trichoderma Community in the Tidal Flats and Wetland of Southeastern China. PLoS One, 2016, 11(12): e0168020
CrossRef Pubmed Google scholar
[17]
Hermosa R, Botella L, Keck E, Jiménez J A, Montero-Barrientos M, Arbona V, Gómez-Cadenas A, Monte E, Nicolás C. The overexpression in Arabidopsis thaliana of a Trichoderma harzianum gene that modulates glucosidase activity, and enhances tolerance to salt and osmotic stresses. Journal of Plant Physiology, 2011, 168(11): 1295–1302
CrossRef Pubmed Google scholar
[18]
Williamson B, Tudzynski B, Tudzynski P, van Kan J A. Botrytis cinerea: the cause of grey mould disease. Molecular Plant Pathology, 2007, 8(5): 561–580
CrossRef Pubmed Google scholar
[19]
Cantu D, Vicente A R, Greve L C, Dewey F M, Bennett A B, Labavitch J M, Powell A L T. The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(3): 859–864
CrossRef Pubmed Google scholar
[20]
González C, Brito N, Sharon A. Infection process. Fungal virulence factors. In: S. Fillinger, Y. Elad, eds. Botrytis—the Fungus, the Pathogen and Its Management in Agricultural Systems. Heidelberg: Springer International Publishing,2015, 229–246
[21]
González M, Brito N, Frías M, González C. Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLoS One, 2013, 8(6): e65924
CrossRef Pubmed Google scholar
[22]
De Groot P W. A genomic inventory of cell wall biosynthesis in the ubiquitous plant pathogen Botrytis cinerea. In: Mora-Montes, eds. The Fungal Cell Wall. Hauppauge: Nova Biomedical, 2013
[23]
González M, Brito N, González C. High abundance of Serine/Threonine-rich regions predicted to be hyper-O-glycosylated in the secretory proteins coded by eight fungal genomes. BMC Microbiology, 2012, 12(1): 213
CrossRef Pubmed Google scholar
[24]
Michielse C B, Becker M, Heller J, Moraga J, Collado I G, Tudzynski P. The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. Molecular Plant-Microbe Interactions, 2011, 24(9): 1074–1085
CrossRef Pubmed Google scholar
[25]
Aguayo C, Riquelme J, Valenzuela P D T, Hahn M, Moreno E S. Bchex virulence gene of Botrytis cinerea: characterization and functional analysis. Journal of General Plant Pathology, 2011, 77(4): 230–238
CrossRef Google scholar
[26]
Giesbert S, Schumacher J, Kupas V, Espino J, Segmüller N, Haeuser-Hahn I, Schreier P H, Tudzynski P. Identification of pathogenesis-associated genes by T-DNA-mediated insertional mutagenesis in Botrytis cinerea: a type 2A phosphoprotein phosphatase and an SPT3 transcription factor have significant impact on virulence. Molecular Plant-Microbe Interactions, 2012, 25(4): 481–495
CrossRef Pubmed Google scholar
[27]
Harren K, Schumacher J, Tudzynski B. The Ca2+/calcineurin-dependent signaling pathway in the gray mold Botrytis cinerea: the role of calcipressin in modulating calcineurin activity. PLoS One, 2012, 7(7): e41761
CrossRef Pubmed Google scholar
[28]
Yang Q, Chen Y, Ma Z. Involvement of BcVeA and BcVelB in regulating conidiation, pigmentation and virulence in Botrytis cinerea. Fungal Genetics and Biology, 2013, 50(1): 63–71
CrossRef Pubmed Google scholar
[29]
Cui Z, Gao N, Wang Q, Ren Y, Wang K, Zhu T. BcMctA, a putative monocarboxylate transporter, is required for pathogenicity in Botrytis cinerea. Current Genetics, 2015, 61(4): 545–553
CrossRef Pubmed Google scholar
[30]
Plaza V, Lagües Y, Carvajal M, Pérez-García L A, Mora-Montes H M, Canessa P, Larrondo L F, Castillo L. bcpmr1 encodes a P-type Ca2+/Mn2+-ATPase mediating cell-wall integrity and virulence in the phytopathogen Botrytis cinerea. Fungal Genetics and Biology, 2015, 76: 36–46
CrossRef Pubmed Google scholar
[31]
Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J. Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. Cucumerinum. Biological Control, 2016, 94: 37–46
CrossRef Google scholar
[32]
Vargas Gil S, Pastor S, March G J. Quantitative isolation of biocontrol agents Trichoderma spp., Gliocladium spp. and actinomycetes from soil with culture media. Microbiological Research, 2009, 164(2): 196–205
CrossRef Pubmed Google scholar
[33]
Dennis C, Webster J. Antagonistic properties of species groups of Trichoderma II. Production of non-volatile antibiotics. Transactions of the British Mycological Society, 1971, 57(1): 41–48 doi:10.1016/S0007-1536(71)80078-5
[34]
Huang X, Zhang N, Yong X, Yang X, Shen Q. Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiological Research, 2012, 167(3): 135–143
CrossRef Pubmed Google scholar
[35]
Vinale F, Sivasithamparam K, Ghisalberti E L, Marra R, Barbetti M J, Li H, Woo S L, Lorito M. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiological and Molecular Plant Pathology, 2008, 72(1): 80–86
CrossRef Google scholar
[36]
Nelson M E, Powelson M L. Biological control of gray mold of snap beans by Trichoderma hamatum. Plant Disease, 1988, 72(8): 727–729
CrossRef Google scholar
[37]
Elad Y. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Protection, 2000, 19(8): 709–714
CrossRef Google scholar
[38]
Vinale F, Marra R, Scala F, Ghisalberti E L, Lorito M, Sivasithamparam K. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Letters in Applied Microbiology, 2006, 43(2): 143–148
CrossRef Pubmed Google scholar
[39]
Inbar J, Abramsky M, Cohen D, Chet I. Plant growth enhancement and disease control by Trichoderma harzianum in vegetable seedlings grown under commercial conditions. European Journal of Plant Pathology, 1994, 100(5): 337–346
CrossRef Google scholar
[40]
Saravanakumar K, Li Y, Yu C, Wang Q Q, Wang M, Sun J, Gao J X, Chen J. Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Scientific Reports, 2017, 7(1): 1771
CrossRef Pubmed Google scholar
[41]
Ferreira L G, Dos Santos R N, Oliva G, Andricopulo A D. Molecular docking and structure-based drug design strategies. Molecules, 2015, 20(7): 13384–13421
CrossRef Pubmed Google scholar
[42]
Rudnitskaya A, Török B, Török M. Molecular docking of enzyme inhibitors: a computational tool for structure-based drug design. Biochemistry and Molecular Biology Education, 2010, 38(4): 261–265
CrossRef Pubmed Google scholar
[43]
Doman T N, McGovern S L, Witherbee B J, Kasten T P, Kurumbail R, Stallings W C, Connolly D T, Shoichet B K. Molecular docking and high-throughput screening for novel inhibitors of protein tyrosine phosphatase-1B. Journal of Medicinal Chemistry, 2002, 45(11): 2213–2221
CrossRef Pubmed Google scholar
[44]
Chaudhary N, Sandhu P, Ahmed M, Akhter Y. Structural basis of transport function in major facilitator superfamily protein from Trichoderma harzianum. International Journal of Biological Macromolecules, 2017, 95: 1091–1100
CrossRef Pubmed Google scholar

Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2018214 contains supplementary materials (Table S1; Fig. S1).
This article does not contain any studies with human or animal subjects performed by any of the authors.

Acknowledgements

This study was supported by the National Key Research and Development Program of China (2017YFD0200400, 2017YFD0201108, SQ2017ZY06102), the National Natural Science Foundation of China (20090073110048), the National Modern Agriculture Industry Technique Systems (CARS-02), Special Project of Basic Work Project for Science and Technology (2014FY120900).

Compliance with ethics guidelines

Kandasamy Saravanakumar, Zhixiang Lu, Hai Xia, Meng Wang, Jianan Sun, Shaoqing Wang, Qiang-qiang Wang, Yaqian Li, and Jie Chen declare that they have no conflicts of interest or financial conflicts to disclose.
This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2018. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
AI Summary AI Mindmap
PDF(1202 KB)

Accesses

Citations

Detail

Sections
Recommended

/