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Journal of Integrative Agriculture  2020, Vol. 19 Issue (11): 2725-2735    DOI: 10.1016/S2095-3119(20)63254-3
Special Issue: 植物细菌真菌合辑Plant Bacteria/Fungus
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
A novel glycoside hydrolase 74 xyloglucanase CvGH74A is a virulence factor in Coniella vitis
QIN Jia-xing, LI Bao-hua, ZHOU Shan-yue
The Key Lab of Integrated Crop Pests Management of Shandong Province/College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, P.R.China
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Grape white rot is a destructive fungal disease occurring worldwide.  Recently, Coniella vitis was identified as the predominant pathogen causing this disease in China.  As the periderms of grape shoots are severely degraded by C. vitis, it was speculated that cell wall-degrading enzymes (CWDEs) might play a key role in the pathogenesis of this disease.  Therefore, this study aimed to examine the hydrolytic activity of the CWDEs of C. vitis.  The results showed that xylanase (Xy) and xyloglucanase (XEG) had high levels of hydrolytic activity both in vitro and in vivo.  Furthermore, a high-virulence fungal strain exhibited higher levels of Xy and XEG activities compared with a low-virulence strain.  The genome of the fungus was found to harbor two XEG-coding genes CvGH74A and CvGH74B, which belonged to the glycoside hydrolase (GH)74 family.  The expression level of CvGH74A was found to be high during pathogen infection.  CvGH74A gene deletion mutants were generated using the split-marker method.  The deletion of CvGH74A decreased both the hydrolytic activities of XEG and Xy and also the ability of the fungus to infect the grape leaves.  No differences in the hyphal growth, morphology of colonies, or conidiation were found between the ΔCvGH74A mutant strains and the wild-type strain.  Together, these results suggested that CvGH74A acted as an important virulence factor, and its enzymatic activity might regulate the virulence of the pathogen.  This study was novel in reporting that GH74 XEG acted as a virulence factor in C. vitis.
Keywords:  Coniella vitis        GH74        grape white rot        virulence        xyloglucanase  
Received: 28 February 2020   Accepted:
Fund: This study was supported by the earmarked fund for China Agriculture Research System (CARS-28).
Corresponding Authors:  Correspondence ZHOU Shan-yue, Tel: +86-532-88030480, E-mail:   

Cite this article: 

QIN Jia-xing, LI Bao-hua, ZHOU Shan-yue. 2020. A novel glycoside hydrolase 74 xyloglucanase CvGH74A is a virulence factor in Coniella vitis. Journal of Integrative Agriculture, 19(11): 2725-2735.

Alvarez L V, Groenewald J Z, Crous P W. 2016. Revising the Schizoparmaceae: Coniella and its synonyms Pilidiella and Schizoparme. Studies in Mycology, 85, 1–34.
Annis S M, Goodwin P H. 1997. Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant fungi. European Journal of Plant Pathology, 103, 1–14.
Attia M A, Brumer H. 2016. Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan. Current Opinion in Structural Biology, 40, 43–53.
Beliën T, Van Campenhout S, Van Acker M, Volckaert G. 2005. Cloning and characterization of two endoxylanases from the cereal phytopathogen Fusarium graminearum and their inhibition profile against endoxylanase inhibitors from wheat. Biochemical and Biophysical Research Communication, 327, 407–414.
Berto P, Comménil P, Belingheri L, Dehorter B. 1999. Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in the infection of cauliflower leaves. FEMS Microbiology, 180, 183–189.
Bisiach M. 1988. White rot. In: Pearson R C, Gohen A C, eds., Compendium of Grape Diseases. American Phytopathological Society Press, St. Paul, MN. pp. 22–23.
Cabello Velasco A, Torres-López F J, Jiménez Lozano M. 1984. Features of an extracellular enzyme extract of Streptomyces species grown on Czapek starch medium. Revista Latinoamericana de Microbiologia, 26, 231–237.
Catlett N L, Lee B, Yoder O C, Turgeon B G. 2003. Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genetics Newsletter, 50, 9–11.
Chethana K W T, Zhou Y, Zhang W, Liu M, Li X, Yan J. 2017. Coniella vitis sp. nov. is the common pathogen of white rot in Chinese vineyards. Plant Disease, 101, 2123–2136.
Comménil P, Belingheri L, Dehorter B. 1998. Antilipase antibodies prevent infection of tomato leaves by Botrytis cinerea. Physiological and Molecular Plant Pathology, 52, 1–14.
Crous P W, Carstens E. 2000. Confusion surrounding white rot disease of grapevines. Winelands, 9, 89–90.
Crous P W, Phillips A J L, Baxter A P. 2000. Phytopathogenic Fungi from South Africa. Department of Plant Pathology Press, University of Stellenbosch Printers, Stellenbosch, South Africa. p. 358.
Damasio A R, Rubio M V, Gonçalves T A, Persinoti G F, Segato F, Prade R A, Contesini F J, de Souza A P, Buckeridge M S, Squina F M. 2017. Xyloglucan breakdown by endo-xyloglucanase family 74 from Aspergillus fumigatus. Applied Microbiology and Biotechnology, 101, 2893–2903.
Douaiher M N, Nowak E, Durand R, Halama P, Reignault P. 2007. Correlative analysis of Mycosphaerella graminicola pathogenicity and cell wall degrading enzymes produced in vitro: The importance of xylanases and polygalacturonases. Plant Pathology, 56, 79–86.
Feng J, Liu G, Selvaraj G, Hughes G R, Wei Y. 2005. A secreted lipase encoded by LIP1 is necessary for efficient use of saturated triglyceride lipids in Fusarium graminearum. Microbiology, 151, 3911–3921.
Grishutin S G, Gusakov A V, Markov A V, Ustinov B B, Semenova M V, Sinitsyn A P. 2004. Specific xyloglucanases as a new class of polysaccharide-degrading enzymes, Biochimica et Biophysica Acta (General Subjects), 1674, 268–281.
Gusakov A V. 2020. Additional sequence and structural characterization of an endo-processive GH74 xyloglucanase from Myceliophthora thermophila and the revision of the EC entry. Biochimica et Biophysica Acta (General Subjects), 1864, 129511.
ten Have A, Mulder W, Visser J N, van Kan A L. 1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Molecular Plant–Microbe Interaction, 11, 1009–1016.
ten Have A, Tenberge K B, Benen J A E, Tudzynski P, Visser J, van Kan J A L. 2002. The contribution of cell wall degrading enzymes to pathogenesis of fungal plant pathogens. In: Kempken F, ed., Agricultural Applications. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research). vol. 11. Springer, Berlin, Heidelberg.
He P C. 1999. Viticulture. China Agriculture Press, Beijing. (in Chinese)
He Z, Cui C Y, Jiang J X. 2017. First report of white rot of grape caused by Pilidiella castaneicola in China. Plant Disease, 101, 1673–1674.
Hématy K, Cherk C, Somerville S. 2009. Host-pathogen warfare at the plant cell wall. Current Opinion in Plant Biology, 12, 406–413.
Hugouvieux-Cotte-Pattat N, Condemine G, William Nasser A, Reverchon S. 1996. Regulation of pectinolysis in Erwinia chrysanthemi. Annual Review of Microbiology, 50, 213–257.
Kang Z, Buchenauer H. 2000. Ultraestructural and cytochemical studies on cellulose, xylan and pectin degradation in wheat spikes infected by Fusarium culmorum. Journal of Phytopatology, 148, 263–275.
Kang Z, Zingen-Sell I, Buchenauer H. 2005. Infection of wheat spikes by Fusarium avenaceum and alterations of a cell wall components in the infected tissue. European Journal of Plant Pathology, 111, 19–28.
Kikot G E, Hours R A, Alconada T M. 2009. Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: A review. Journal of Basic Microbiology, 49, 231–241.
Klechkovskaya E A, Adamovskaya V G, Wolf G A, Vovchuk S V. 1998. The role of hydrolases and trypsin inhibitor in development of winter wheat resistance to Fusarium infection. Russian Journal of Plant Physiology, 45, 728–735.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Lalaouil F, Halamal P, Dumortierl V, Paul B. 2000. Cell wall degrading enzymes produced in vitro by isolates of Phaeosphaeria nodorum differing in aggressiveness. Plant Pathology, 49, 727–733.
Laluk K, Mengiste T. 2010. Necrotroph attacks on plants: Wanton destruction or covert extortion? The Arabidopsis Book, 8, e0136.
Li D, Wan Y, Wang Y, He P. 2008. Relatedness of resistance to anthracnose and to white rot in Chinese wild grapes. Vitis, 47, 213–215.
Liu Z, Friesen T L. 2012. Polyethylene glycol (peg)-mediated transformation in filamentous fungal pathogens. Methods in Molecular Biology (Clifton, N.J.), 835, 365–375.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(–Delta C) method. Methods, 25, 402–408.
McNeill M, Darvill A G, Fry S C, Albersheim P. 1984. Structure and function of the primary cell walls of plants. Annual Review of Biochemistry, 53, 625–663.
Morales-Cruz A, Amrine K C H, Blanco-Ulate B, Lawrence D P, Travadon R, Rolshausen P E, Baumgartner K, Cantu D. 2015. Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens. BMC Genomics, 16, 469.
Musich E G. 1980. Effect of the mineral components of Czapek’s medium on the growth and cellulosolytic activity of Penicillium funiculosum Thom 28. Mikrobiologicheskii Zhurnal, 42, 586.
Nguyen Q B, Itoh K, Vu B V, Tosa Y, Nakayashiki H. 2011. Simultaneous silencing of endo-β-1,4-xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Molecular Microbiology, 81, 1008–1019.
van Niekerk J M, Groenewald J Z E, Verkley G J M, Fourie P H, Wingfield M J, Crous P W. 2004. Systematic reappraisal of Coniella and Pilidiella, with specific reference to species occurring on Eucalyptus and Vitis in South Africa. Mycology Research, 108, 283–303.
Pérez-Hernández A, González M, González C, van Kan J A, Brito N. 2017. BcSUN1, a B. cinerea SUN-family protein, is involved in virulence. Frontiers in Microbiology, 8, e65924.
Quoc N B, Bao Chau N N. 2017. The role of cell wall degrading enzymes in pathogenesis of Magnaporthe oryzae. Current Protein and Peptide Science, 18, 1019.
Raghunath R, Siddalingamurthy K R. 2017. Microbial xyloglucanases: A comprehensive review. Biocatalysis and Biotransformation, 36, 1–16.
Roeder D L, Collmer A. 1985. Marker-exchange mutagenesis of a pectate iyase isoenzyme gene in Erwinia chrysanthemi. Journal of Bacteriology, 164, 51–56.
Sato S, Ohta K, Kojima K, Kozeki T, Ohmachi T,  Yoshida T. 2016. Isolation and characterization of two types of xyloglucanases from a phytopathogenic fungus, Verticillium dahlia. Journal of Applied Glycoscience, 63, 13–18.
Siah A, Deweera C, Duyme F, Sanssené J, Durand R, Halama P, Reignault P. 2010. Correlation of in planta endo-beta-1,4-xylanase activity with the necrotrophic phase of the hemibiotrophic fungus Mycosphaerella graminicola. Plant Pathology, 59, 661–670.
Skamnioti P, Gurr S J. 2007. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. The Plant Cell, 19, 2647–2689.
Underwood W. 2012. The plant cell wall: A dynamic barrier against pathogen invasion. Frontiers in Plant Science, 3, 85.
Valette-Collet O, Cimerman A, Reignault P, Levis C, Boccara M. 2003. Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces on several host plans. Molecular Plant–Microbe Interaction, 16, 360–367.
Voigt C A, Schafer W, Salomon S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. The Plant Journal, 42, 364–375.
Voigt C A, Scheidt B, Gácser A, Kassner H, Lieberei R, Schafer W, Salomon S. 2007. Enhanced mycotoxin production of a lipase-deficient Fusarium graminearum mutant correlates to toxin-related gene expression. European Journal of Plant Pathology, 117, 1–12.
Vu B V, Itoh K, Nguyen Q B, Tosa Y, Nakayashiki H. 2012. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Molecular Plant–Microbe Interaction, 25, 1135–1141.
Walton J D. 1994. Deconstructing the cell wall. Plant Physiology, 104, 1113–1118.
Wanyoike W M, Kang Z, Buchenauer H. 2002. Importance of cell wall degrading enzymes produced by Fusarium graminearum during infection of wheat head. European Journal of Plant Pathology, 108, 803–810.
Xu C J, Sun Y C, Wu Y X, Feng H, Gao X N, Huang L L. 2017. Pathogenic function of pectate lyase gene Vmpl4 of Valsa mali in apple. Jourbal of Fruit Science, 34, 19–25.
Xu C J, Wu Y X, Dai Q Q, Li Z P, Gao X N, Huang L L. 2016. Function of polygalacturonase genes Vmpg7 and Vmpg8 of Valsa mali. Scientia Agricultura Sinica, 8, 1489–1498. (in Chinese)
Xu M, Gao X, Chen J, Yin Z, Feng H, Huang L. 2018. The feruloyl esterase genes are required for full pathogenicity of the apple tree canker pathogen Valsa mali. Molecular Plant Pathology, 19, 1353–1363.
Yaoi K, Hiyoshi A, Mitsuishi Y. 2007a. Screening, purification and characterization of a prokaryotic isoprimeverose-producing oligoxyloglucan hydrolase from Oerskovia sp. Y1. Journal of Applied Glycoscience, 54, 91–94.
Yaoi K, Kondo H, Hiyoshi A, Noro N, Sugimoto H, Tsuda S, Mitsuishi Y, Miyazaki K. 2007b. The structural basis for the exo-mode of action in GH74 oligoxyloglucan reducing end-specific cellobiohydrolase. Journal of Molecular Biology, 370, 53–62.
Yaoi K, Mitsuishi Y. 2002. Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase, Journal of Biological Chemistry, 277, 48276–48281.
Yu C, Li T, Shi X, Saleem M, Li B, Liang W, Wang C. 2018. Deletion of endo-β-1,4-Xylanase VmXyl1 impacts the virulence of Valsa mali in apple tree. Frontiers in Plant Science, 9, 663.
Zhang L, van Kan J A L. 2013. 14 pectin as a barrier and nutrient source for fungal plant pathogens. In: Kempken F, ed., Agricultural Applications. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research). vol. 11. Springer, Berlin, Heidelberg. pp. 361–375.
Zhou S, Li B. 2020. Genome sequence resource of Coniella vitis, a fungal pathogen causing grape white rot disease. Molecular Plant–Microbe Interaction, 33, 787–789.
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