The Botrytis cinerea transglycosylase BcCrh4 is a cell death-inducing protein with cell death-promoting and -suppressing domains.
apoplast
fungal development
pathogenicity
pattern-triggered immunity
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
04
09
2023
received:
01
07
2023
accepted:
12
09
2023
medline:
5
12
2023
pubmed:
17
10
2023
entrez:
17
10
2023
Statut:
ppublish
Résumé
Botrytis cinerea is a necrotrophic fungal plant pathogen that causes grey mould and rot diseases in many crops. Here, we show that the B. cinerea BcCrh4 transglycosylase is secreted during plant infection and induces plant cell death and pattern-triggered immunity (PTI), fulfilling the characteristics of a cell death-inducing protein (CDIP). The CDIP activity of BcCrh4 is independent of the transglycosylase enzymatic activity, it takes place in the apoplast and does not involve the receptor-like kinases BAK1 and SOBIR1. During saprophytic growth, BcCrh4 is localized in the endoplasmic reticulum and in vacuoles, but during plant infection, it accumulates in infection cushions (ICs) and is then secreted to the apoplast. Two domains within the BcCrh4 protein determine the CDIP activities: a 20aa domain at the N' end activates intense cell death and PTI, while a stretch of 52aa in the middle of the protein induces a weaker response and suppresses the activity of the 20aa N' domain. Deletion of bccrh4 affected fungal development and IC formation in particular, resulting in reduced virulence. Collectively, our findings demonstrate that BcCrh4 is required for fungal development and pathogenicity, and hint at a dual mechanism that balances the virulence activity of this, and potentially other CDIPs.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
354-371Subventions
Organisme : China Scholarship Council
ID : 202108280009
Organisme : BARD
ID : #5261-20C
Organisme : Key Laboratory of Integrated Pests Management on Crops in Central China/Hubei Key Laboratory of Crop Diseases, Insect Pests and Weeds Control
ID : #2022ZTSJJ6
Informations de copyright
© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Bailey, B.A. (1995) Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology, 85, 1250-1255.
Bi, K., Liang, Y., Mengiste, T. & Sharon, A. (2023) Killing softly: a roadmap of Botrytis cinerea pathogenicity. Trends in Plant Science, 28, 211-222. Available from: https://doi.org/10.1016/j.tplants.2022.08.024
Bi, K., Scalschi, L., Jaiswal, N., Mengiste, T., Fried, R., Sanz, A.B. et al. (2021) The Botrytis cinerea Crh1 transglycosylase is a cytoplasmic effector triggering plant cell death and defense response. Nature Communications, 12, 2166.
Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V. & Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research, 37, D233-D238.
Choquer, M., Fournier, E., Kunz, C., Levis, C., Pradier, J.-M., Simon, A. et al. (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters, 277, 1-10.
Crumiere, M., De Vallee, A., Rascle, C., Nahar, S., van Kan, J.A. & Bruel, C.et al. (2022) A multifunctional LysM effector of Botrytis cinerea contributes to plant infection. bioRxiv, 2022.11.05.515289.
Cuesta Arenas, Y., Kalkman, E.R.I.C., Schouten, A., Dieho, M., Vredenbregt, P., Uwumukiza, B. et al. (2010) Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea. Physiological and Molecular Plant Pathology, 74, 376-386.
Dean, R., Van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D. et al. (2012) The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13, 414-430.
Eizner, E., Ronen, M., Gur, Y., Gavish, A., Zhu, W. & Sharon, A. (2017) Characterization of Botrytis-plant interactions using PathTrack©-an automated system for dynamic analysis of disease development. Molecular Plant Pathology, 18, 503-512.
Fang, W., Sanz, A.B., Bartual, S.G., Wang, B., Ferenbach, A.T. & Farkaš, V.et al. (2019) Mechanisms of redundancy and specificity of the Aspergillus fumigatus Crh transglycosylases. Nature Communications, 10, 1669.
Finkelshtein, A., Shlezinger, N., Bunis, O. & Sharon, A. (2011) Botrytis cinerea BcNma is involved in apoptotic cell death but not in stress adaptation. Fungal Genetics and Biology, 48, 621-630.
Frías, M., González, C. & Brito, N. (2011) BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytologist, 192, 483-495.
Frías, M., González, M., González, C. & Brito, N. (2016) BcIEB1, a Botrytis cinerea secreted protein, elicits a defense response in plants. Plant Science, 250, 115-124.
Gietz, R.D. & Woods, R.A. (2006) Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods in Molecular Biology, 313, 107-120.
Gu, B., Gao, W., Liu, Z., Shao, G., Peng, Q., Mu, Y. et al. (2023) A single region of the Phytophthora infestans avirulence effector Avr3b functions in both cell death induction and plant immunity suppression. Molecular Plant Pathology, 24, 317-330.
Gui, Y.-J., Chen, J.-Y., Zhang, D.-D., Li, N.-Y., Li, T.-G., Zhang, W.-Q. et al. (2017) Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environmental Microbiology, 19, 1914-1932. Available from: https://doi.org/10.1111/1462-2920.13695
Have, A., Mulder, W., Visser, J. & van Kan, J.A.L. (1998) The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Molecular Plant-Microbe Interactions®, 11, 1009-1016.
Jeblick, T., Leisen, T., Steidele, C.E., Albert, I., Müller, J., Kaiser, S. et al. (2022) Botrytis hypersensitive response inducing protein 1 triggers noncanonical PTI to induce plant cell death. Plant Physiology, 191, 125-141. Available from: https://doi.org/10.1093/plphys/kiac476.
De Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R. et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science, 329, 953-955.
Kars, I., Krooshof, G.H., Wagemakers, L., Joosten, R., Benen, J.A.E. & Van Kan, J.A.L. (2005) Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. The Plant Journal, 43, 213-225.
Kostylev, M., Otwell, A.E., Richardson, R.E. & Suzuki, Y. (2015) Cloning should be simple: Escherichia coli DH5α-mediated assembly of multiple DNA fragments with short end homologies. PLoS One, 10, e0137466.
Landeo Villanueva, S., Malvestiti, M.C., van Ieperen, W., Joosten, M.H.A.J. & van Kan, J.A.L. (2021) Red light imaging for programmed cell death visualization and quantification in plant-pathogen interactions. Molecular Plant Pathology, 22, 361-372. Available from: https://doi.org/10.1111/mpp.13027
Leisen, T., Bietz, F., Werner, J., Wegner, A., Schaffrath, U., Scheuring, D. et al. (2020) CRISPR/Cas with ribonucleoprotein complexes and transiently selected telomere vectors allows highly efficient marker-free and multiple genome editing in Botrytis cinerea. PLoS Pathogens, 16, e1008326.
Leisen, T., Werner, J., Pattar, P., Safari, N., Ymeri, E., Sommer, F. et al. (2022) Multiple knockout mutants reveal a high redundancy of phytotoxic compounds contributing to necrotrophic pathogenesis of Botrytis cinerea. PLoS Pathogens, 18, e1010367. Available from: https://doi.org/10.1371/journal.ppat.1010367
Lenarčič, T., Albert, I., Böhm, H., Hodnik, V., Pirc, K., Zavec, A.B. et al. (2017) Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science, 358, 1431-1434.
Li, Y., Han, Y., Qu, M., Chen, J., Chen, X., Geng, X. et al. (2020) Apoplastic cell death-inducing proteins of filamentous plant pathogens: roles in plant-pathogen interactions. Frontiers in Genetics, 11, 661.
Ma, L., Liu, T., Zhang, K., Shi, H., Zhang, L. & Zou, G. et al. (2022) Botrytis cinerea transcription factor BcXyr1 regulates (Hemi-) cellulase production and fungal virulence. mSystems, 7, e0104222.
Ma, L., Salas, O., Bowler, K., Bar-Peled, M. & Sharon, A. (2017) UDP-4-keto-6-deoxyglucose, a transient antifungal metabolite, weakens the fungal cell wall partly by inhibition of UDP-galactopyranose mutase. mBio, 8, e01559-17.
Ma, L., Salas, O., Bowler, K., Oren-Young, L., Bar-Peled, M. & Sharon, A. (2017) Genetic alteration of UDP-rhamnose metabolism in Botrytis cinerea leads to the accumulation of UDP-KDG that adversely affects development and pathogenicity. Molecular Plant Pathology, 18, 263-275. Available from: https://doi.org/10.1111/mpp.12398
Minz-Dub, A. & Sharon, A. (2017) The Botrytis cinerea PAK kinase BcCla4 mediates morphogenesis, growth and cell cycle regulating processes downstream of BcRac. Molecular Microbiology, 104, 487-498.
Mohammadi, N., Mehrabi, R., Mirzadi Gohari, A., Mohammadi Goltapeh, E., Safaie, N. & Kema, G.H.J. (2017) The ZtVf1 transcription factor regulates development and virulence in the foliar wheat pathogen Zymoseptoria tritici. Fungal Genetics and Biology, 109, 26-35.
Nesher, I., Minz, A., Kokkelink, L., Tudzynski, P. & Sharon, A. (2011) Regulation of pathogenic spore germination by CgRac1 in the fungal plant pathogen Colletotrichum gloeosporioides. Eukaryotic Cell, 10, 1122-1130.
Nie, J., Yin, Z., Li, Z., Wu, Y. & Huang, L. (2019) A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern. New Phytologist, 222, 995-1011.
Noda, J., Brito, N. & González, C. (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biology, 10, 38.
Oren-Young, L., Llorens, E., Bi, K., Zhang, M. & Sharon, A. (2021) Botrytis cinerea methyl isocitrate lyase mediates oxidative stress tolerance and programmed cell death by modulating cellular succinate levels. Fungal Genetics and Biology, 146, 103484.
Pardini, G., De Groot, P.W.J., Coste, A.T., Karababa, M., Klis, F.M., de Koster, C.G. et al. (2006) The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. Journal of Biological Chemistry, 281, 40399-40411.
Pemberton, C.L. & Salmond, G.P.C. (2004) The Nep1-like proteins-a growing family of microbial elicitors of plant necrosis. Molecular Plant Pathology, 5, 353-359.
Rafiei, V., Vélëz, H. & Tzelepis, G. (2021) The role of glycoside hydrolases in phytopathogenic fungi and oomycetes virulence. International Journal of Molecular Sciences, 22, 9359.
Schenk, S. & Schikora, A. (2015) Staining of callose depositions in root and leaf tissues. Bio-protocol, 5, e1429.
Schouten, A., Van Baarlen, P. & Van Kan, J.A.L. (2008) Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytologist, 177, 493-505.
Schumacher, J. (2012) Tools for Botrytis cinerea: new expression vectors make the gray mold fungus more accessible to cell biology approaches. Fungal Genetics and Biology, 49, 483-497.
Seidl, M.F. & Van den Ackerveken, G. (2019) Activity and phylogenetics of the broadly occurring family of microbial Nep1-like proteins. Annual Review of Phytopathology, 57, 367-386. Available from: https://doi.org/10.1146/annurev-phyto-082718-100054
Song, T., Zhang, Y., Zhang, Q., Zhang, X., Shen, D. & Yu, J. et al. (2021) The N-terminus of an Ustilaginoidea virens Ser-Thr-rich glycosylphosphatidylinositol-anchored protein elicits plant immunity as a MAMP. Nature Communications, 12, 2451.
Steentjes, M.B.F., Herrera Valderrama, A.L., Fouillen, L., Bahammou, D., Leisen, T., Albert, I. et al. (2022) Cytotoxic activity of Nep1-like proteins on monocots. New Phytologist, 235, 690-700. Available from: https://doi.org/10.1111/nph.18146
Wang, D., Zhang, D.-D., Song, J., Li, J.-J., Wang, J. & Li, R. et al. (2022) Verticillium dahliae CFEM proteins manipulate host immunity and differentially contribute to virulence. BMC Biology, 20, 55.
Wang, S., Xing, R., Wang, Y., Shu, H., Fu, S., Huang, J. et al. (2021) Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity. New Phytologist, 229, 3424-3439. Available from: https://doi.org/10.1111/nph.17120
Yang, Y., Yang, X., Dong, Y. & Qiu, D. (2018) The Botrytis cinerea xylanase BcXyl1 modulates plant immunity. Frontiers in Microbiology, 9, 2535.
Yin, Z., Wang, N., Pi, L., Li, L., Duan, W., Wang, X. et al. (2021) Nicotiana benthamiana LRR-RLP NbEIX2 mediates the perception of an EIX-like protein from Verticillium dahliae. Journal of Integrative Plant Biology, 63, 949-960.
Zhang, M., Trushina, N., Lang, T., Hahn, M., Pasmanik-Chor, M. & Sharon, A. et al. (2023) Serine peptidases and increased amounts of soluble proteins contribute to heat priming of the plant pathogenic fungus Botrytis cinerea. Mbio, 14, e01077-23.
Zhang, Y., Zhang, Y., Qiu, D., Zeng, H., Guo, L. & Yang, X. (2015) BcGs1, a glycoprotein from Botrytis cinerea, elicits defence response and improves disease resistance in host plants. Biochemical and Biophysical Research Communications, 457, 627-634.
Zhu, W., Ronen, M., Gur, Y., Minz-Dub, A., Masrati, G., Ben-Tal, N. et al. (2017) BcXYG1, a secreted xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses. Plant Physiology, 175, 438-456.
Zhu, W., Yu, M., Xu, R., Bi, K., Yu, S., Xiong, C. et al. (2022) Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector. Environmental Microbiology, 24, 3420-3435.