Genome-Wide Identification and Expression Analysis of Cutinase Gene Family in Rhizoctonia cerealis and Functional Study of an Active Cutinase RcCUT1 in the Fungal–Wheat Interaction
Massart, Sébastien ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs
Zhang, Zengyan
Language :
English
Title :
Genome-Wide Identification and Expression Analysis of Cutinase Gene Family in Rhizoctonia cerealis and Functional Study of an Active Cutinase RcCUT1 in the Fungal–Wheat Interaction
Ausubel, F. M. (2005). Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6, 973-979. doi: 10.1038/ni1253
Balbi-Pena, M. I., Schwan-Estrada, K. R. F., and Stangarlin, J. R. (2012). Differential occurrence of the oxidative burst and the activity of defence related enzymes in compatible and incompatible tomato-Oidium neolycopersici interactions. Aust. Plant Pathol. 41, 573-586. doi: 10.1007/s13313-012-0150-6
Burpee, L. L., Sanders, P. L., Cole, H. Jr., and Sherwood, R. T. (1980). Anastomosis groups among isolates of anastomosis groups among isolates of Ceratobasidium cornigerum and related fungi. Mycologia 72, 689-701. doi: 10.2307/3759762
Chassot, C., and Metraux, J. P. (2005). The cuticle as source of signals for plant defense. Plant Biosys. 139, 28-31. doi: 10.1080/11263500500056344
Chen, J., Li, G. H., Du, Z. Y., Quan, W., Zhang, H. Y., Che, M. Z., et al. (2013). Mapping of QTL conferring resistance to sharp eyespot (Rhizoctonia cerealis) in bread wheat at the adult plant growth stage. Theor. Appl. Genet. 126, 2865-2878. doi: 10.1007/s00122-013-2178-6
Chen, L., Zhang, Z. Y., Liang, H. X., Liu, H., Du, L. P., Xu, H. J., et al. (2008). Overexpression of TiERF1 enhances resistance to sharp eyespot in transgenic wheat. J. Exp. Bot. 59, 4195-4204. doi: 10.1093/jxb/ern259
Chen, S., Su, L., Chen, J., and Wu, J. (2013). Cutinase: characteristics, preparation, and application. Biotechnol. Adv. 31, 1754-1767. doi: 10.1016/j.biotechadv.2013.09.005
Chen, S., Tong, X., Woodard, R. W., Du, G., Wu, J., and Chen, J. (2008). Identification and characterization of bacterial cutinase. J. Biol. Chem. 283, 25854-25862. doi: 10.1074/jbc. M800848200
Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814. doi: 10.1016/j.cell.2006.02.008
Deising, H., Nicholson, R. L., Haug, M., Howard, R. J., and Mendgen, K. (1992). Adhesion pad formation and the involvement of cutinase and esterases in the attachment of uredo spores to the host cuticle. Plant Cell 4, 1101-1111. doi: 10.1105/tpc.4.9.1101
Dixon, R. A., Harrison, M. J., and Lamb, C. J. (1994). Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32, 479-501. doi: 10.1146/annurev.phyto.32.1.479
Dong, N., Liu, X., Liu, Y., Du, L. P., Xu, H. J., Xin, Z. Y., et al. (2010). Overexpression of TaPIEP1, a pathogen-induced ERF gene of wheat, confers host-enhanced resistance to fungal pathogen Bipolaris sorokiniana. Funct. Integr. Genomics 10, 215-226. doi: 10.1007/s10142-009-0157-4
Ebel, J., and Mithofer, A. (1998). Early events in the elicitation of plant defence. Planta 206, 335-348. doi: 10.1007/s004250050409
Francis, S. A., Dewey, F. M., and Gurr, S. J. (1996). The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei. Physiol. Mol. Plant Pathol. 49, 201-211. doi: 10.1006/pmpp.1996.0049
Garcia-Brugger, A., Lamotte, O., Vandelle, E., Bourque, S., Lecourieux, D., Poinssot, B., et al. (2006). Early signaling events induced by elicitors of plant defenses. Mol. Plant Microbe Interact. 19, 711-724. doi: 10.1094/mpmi-19-0711
Gilbert, R. D., Johnson, A. M., and Dean, R. A. (1996). Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol. Mol. Plant Pathol. 38, 335-346. doi: 10.1006/pmpp.1996.0027
Gui, Y. J., Zhang, W. Q., Zhang, D. D., Zhou, L., Short, D. P. G., Wang, J., et al. (2018). A Verticillium dahliae extracellular cutinase modulates plant immune responses. Mol. Plant Microbe Interact. 31, 260-273. doi: 10.1094/MPMI-06-17-0136-R
Hamada, M. S., Yin, Y., Chen, H., and Ma, Z. (2011). The escalating threat of Rhizoctonia cerealis, the causal agent of sharp eyespot in wheat. Pest Manag. Sci. 67, 1411-1419. doi: 10.1002/ps.2236
Hogenhout, S. A., Van der Hoorn, R. A., Terauchi, R., and Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22, 115-122. doi: 10.1094/MPMI-22-2-0115
James, K. H., Jonathan, P. A., Angela, H. W., Jana, S., and Karam, B. S. (2014). Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet. 10:e1004281. doi: 10.1371/journal.pgen.1004281
Ji, L., Liu, C., Zhang, L., Liu, A., and Yu, J. (2017). Variation of rDNA internal transcribed spacer sequences in Rhizoctonia cerealis. Curr. Microbiol. 74, 877-884. doi: 10.1007/s00284-017-1258-2
Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
Kiran, K., Rawal, H. C., Dubey, H., Jaswal, R., Devanna, B. N., Gupta, D. K., et al. (2016). Draft genome of the wheat rust pathogen (puccinia triticina) unravels genome-wide structural variations during evolution. Genome Biol. Evol. 8, 2702-2721. doi: 10.1093/gbe/evw197
Kolattukudy, P. E., Li, D. X., Hwang, C. S., and Flaishman, M. A. (1995). Host signals in fungal gene-expression involved in penetration into the host. Can. J. Bot. 73, 1160-1168. doi: 10.1139/b95-373
Koller, W., Parker, D. M., and Becker, C. M. (1991). Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopathology 81, 1375-1379. doi: 10.1094/Phyto-81-1375
Koschorreck, K., Liu, D., Kazenwadel, C., Schmid, R. D., and Hauer, B. (2010). Heterologous expression, characterization and site-directed mutagenesis of cutinase CUTAB1 from Alternaria brassicicola. Appl. Microbiol. Biotechnol. 87, 991-997. doi: 10.1007/s00253-010-2533-3
Lee, B. H., Lee, H., Xiong, L., and Zhu, J. K. (2002). A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14, 1235-1251. doi: 10.1105/tpc.010433
Lemanczyk, G., and Kwasna, H. (2013). Effects of sharp eyespot (Rhizoctonia cerealis) on yield and grain quality of winter wheat. Eur. J. Plant Pathol. 135, 187-200. doi: 10.1007/s10658-012-0077-3
Li, D., Ashby, A. M., and Johnstone, K. (2003). Molecular evidence that the extracellular cutinase Pbc1 is required for pathogenicity of Pyrenopeziza brassicae on oilseed rape. Mol. Plant Microbe Interact. 16, 545-552. doi: 10.1094/MPMI.2003.16.6.545
Li, W., Guo, Y., Zhang, A., and Chen, H. (2017). Genetic structure of populations of the wheat sharp eyespot pathogen Rhizoctonia cerealis AG-DI in China. Phytopathology 107, 224-230. doi: 10.1094/PHYTO-05-16-0213-R
Li, W., Sun, H., Deng, Y., Zhang, A., and Chen, H. (2014). The heterogeneity of the rDNA-ITS sequence and its phylogeny in Rhizoctonia cerealis, the cause of sharp eyespot in wheat. Curr. Genet. 60, 1-9. doi: 10.1007/s00294-013-0397-7
Liu, T., Hou, J., Wang, Y., Jin, Y., Borth, W., Zhao, F., et al. (2016). Genome-wide identification, classification and expression analysis in fungal-plant interactions of cutinase gene family and functional analysis of a putative ClCUT7 in Curvularia lunata. Mol. Genet. Genomics 291, 1105-1115. doi: 10.1007/s00438-016-1168-1
Liu, X., Yang, L. H., Zhou, X., Zhou, M., Lu, Y., and Liang, J. (2013). Transgenic wheat expressing Thinopyrum intermedium MYB transcription factor TiMYB2R-1 shows enhanced resistance to the take-all disease. J. Exp. Bot. 64, 2243-2253. doi: 10.1093/jxb/ert084
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
Ma, Y., Han, C., Chen, J., Li, H., He, K., Liu, A., et al. (2015). Fungal cellulase is an elicitor but its enzymatic activity is not required for its elicitor activity. Mol. Plant Pathol. 16, 14-26. doi: 10.1111/mpp.12156
Maddock, S. E. (1979). Studies of the Biology of Light Leaf Spot Disease of Oilseed Rape and Other Brassicas. Ph. D. thesis, University of Cambridge, Cambridge
Moore, J. W., Herrerafoessel, S., Lan, C., Schnippenkotter, W., Ayliffe, M., Huerta-Espino, J., et al. (2015). A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 47, 1494-1498. doi: 10.1038/ng.3439
Morid, B., Zare, R., Rezaee, S., Zamani-Zadeh, H., and Hajmansour, S. (2009). The relationship between cutinases and the pathogenicity/virulence of Fusarium solani in potato tubers. Phytopathol. Mediterr. 48, 403-410
Nicholson, P., and Parry, D. W. (1996). Development and use of a PCR assay to detect Rhizoctonia cerealis, the cause of sharp eyespot in wheat. Plant Pathol. 45, 872-883. doi: 10.1111/j.1365-3059.1996.tb02898.x
Park, J. H., Suh, M. C., Kim, T. H., Kim, M. C., and Cho, S. H. (2008). Expression of glycine-rich protein genes, AtGRP5 and AtGRP23, induced by the cutin monomer 16-hydroxypalmitic acid in Arabidopsis thaliana. Plant Physiol. Biochem. 46, 1015-1018. doi: 10.1016/j.plaphy.2008.06.008
Parker, D. M., and Köller, W. (1998). Cutinase and other lipolytic esterases protect bean leaves from infection by Rhizoctonia solani. Mol. Plant Microbe Interact. 11, 514-522. doi :10.1094/MPMI.1998.11.6.514
Pitt, D. (1966). Studies on sharp eyespot disease of cereals. III. Effects of the disease on the wheat host and the incidence of disease in the field. Ann. Appl. Biol. 58, 299-308. doi: 10.1111/j.1744-7348.1966.tb04389.x
Rogers, L. M., Flaishman, M. A., and Kolattukudy, P. E. (1994). Cutinase gene disruption in Fusarium solani f. sp. pisi decreases its virulence on pea. Plant Cell 6, 935-945. doi: 10.1105/tpc.6.7.935
Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425. doi: 10.1093/oxfordjournals.molbev.a040454
Saunders, D., Win, J., Cano, L. M., Szabo, L. J., and Kamoun, S. (2012). Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS One 7:e29847. doi: 10.1371/journal.pone.0029847
Schweizer, P., Felix, G., Buchala, A., Müller, C., and Métraux, J. (1996b). Perception of free cutin monomers by plant cells. Plant J. 10, 331-341. doi: 10.1046/j.1365-313X.1996.10020331.x
Schweizer, P., Jeanguenat, A., Whitacre, D., Metraux, J. P., and Mosinger, E. (1996a). Induction of resistance in barley against Erysiphe graminis f.sp. hordei by free cutin monomers. Physiol. Mol. Plant Pathol. 49, 103-120. doi: 10.1006/pmpp.1996.0043
Sharon, M., Sneh, B., Kuninaga, S., and Hyakumachi, M. (2006). The advancing identification and classification of Rhizoctonia, spp. using molecular and biotechnological methods compared with the classical anastomosis grouping. Mycoscience 47, 299-316. doi: 10.1007/S10267-006-0320-X
Skamnioti, P., and Gurr, S. J. (2007). Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19, 2674-2689. doi: 10.1105/tpc.107.051219
Skamnioti, P., Furlong, R. F., and Gurr, S. J. (2008). Evolutionary history of the ancient cutinase family in five filamentous Ascomycetes reveals differential gene duplications and losses and in Magnaporthe grisea shows evidence of sub-and neo-functionalization. New Phytol. 180, 711-721. doi: 10.1111/j.1469-8137.2008.02598.x
Stahl, D. J., and Schafer, W. (1992). Cutinase is not required for fungal pathogenicity on pea. Plant Cell 4, 621-629. doi: 10.1105/tpc.4.6.621
Sweigard, J. A., Chumley, F. G., and Valent, B. (1992). Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 232, 183-190. doi: 10.1105/tpc.4.6.621
Temme, N., and Tudzynski, P. (2009). Does Botrytis cinerea ignore H2O2-induced oxidative stress during infection? Characterization of Botrytis activator protein 1. Mol. Plant Microbe Interact. 22, 987-998. doi: 10.1094/mpmi-22-8-0987
Thordal-Christensen, H., Zhang, Z., Wei, Y., and Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194. doi: 10.1046/j.1365-313X.1997.11061187.x
Tomaso-Peterson, M., and Trevathan, L. E. (2007). Characterization of Rhizoctonia-like fungi isolated from agronomic crops and turfgrasses in Mississippi. Plant Dis. 91, 260-265. doi: 10.1094/PDIS-91-3-0260
Van Der Hoeven, E. P., and Bollen, G. J. (1980). Effect of benomyl on soil fungi associated with rye. 1. Effect on the incidence of sharp eyespot caused by Rhizoctonia cerealis. Neth. J. Plant Pathol. 86, 163-180. doi: 10.1007/BF01989709
Wang, X. L., Jiang, N., Liu J. L., Liu, W. D., and Wang G. L. (2014). The role of effectors and host immunity in plant-necrotrophic fungal interactions. Virulence 5, 722-732. doi: 10.4161/viru.29798
Wang, Y., Chen, J., Li, D. W., Zheng, L., and Huang, J. (2017). CglCUT1 gene required for cutinase activity and pathogenicity of Colletotrichum gloeosporioides causing anthracnose of Camellia oleifera. Eur. J. Plant Pathol. 147, 103-114. doi: 10.1007/s10658-016-0983-x
Zhang, H., Wu, Q., Cao, S., Zhao, T., Chen, L., Zhuang, P., et al. (2014). A novel protein elicitor (SsCut) from Sclerotinia sclerotiorum induces multiple defense responses in plants. Plant Mol. Biol. 86, 495-511. doi: 10.1007/s11103-014-0244-3
Zhang, Z. Y., Liu, X., Wang, X., Zhou, M., Zhou, X., Ye, X. G., et al. (2012). An R2R3 MYB transcription factor in wheat, TaPIMP1, mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense-and stress-related genes. New Phytol. 196, 1155-1170. doi: 10.1111/j.1469-8137.2012.04353.x
Zhang, Z., Yao, W., Dong, N., Laing, H., Liu, H., and Huang, R. (2007). A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. J. Exp. Bot. 58, 2993-3003. doi: 10.1093/jxb/erm151
Zheng, A., Lin, R., Zhang, D., Qin, P., Xu, L., Ai, P., et al. (2013). The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat. Commun. 4:1424. doi: 10.1038/ncomms2427
Zhu, X. L., Qi, L., Liu, X., Cai, S. B., Xu, H. J., Huang, R. F., et al. (2014). The wheat ethylene response factor transcription factor pathogen-induced ERF1 mediated host responses to both the necrotrophic pathogen Rhizoctonia cerealis and freezing stresses. Plant Physiol. 164, 1499-1514. doi: 10.1104/pp.113.229575
Zhu, X. L., Yang, K., Wei, X. N., Zhang, Q., Rong, W., Du, L. P., et al. (2015). The wheat AGC kinase TaAGC1 is a positive contributor to host resistance to the necrotrophic pathogen Rhizoctonia cerealis. J. Exp. Bot. 66, 6591-6603. doi: 10.1093/jxb/erv367
