Plant immunity suppression by an β-1,3-glucanase of the maize anthracnose pathogen Colletotrichum graminicola.
Callose
CgEC124
Glycosyl hydrolase
Immunity
Maize
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
26 Apr 2024
26 Apr 2024
Historique:
received:
25
01
2024
accepted:
19
04
2024
medline:
27
4
2024
pubmed:
27
4
2024
entrez:
26
4
2024
Statut:
epublish
Résumé
Many phytopathogens secrete a large number of cell wall degrading enzymes (CWDEs) to decompose host cell walls in order to penetrate the host, obtain nutrients and accelerate colonization. There is a wide variety of CWDEs produced by plant pathogens, including glycoside hydrolases (GHs), which determine the virulence, pathogenicity, and host specificity of phytopathogens. The specific molecular mechanisms by which pathogens suppress host immunity remain obscure. In this study, we found that CgEC124 encodes a glycosyl hydrolase with a signal peptide and a conserved Glyco_hydro_cc domain which belongs to glycoside hydrolase 128 family. The expression of CgEC124 was significantly induced in the early stage of Colletotrichum graminicola infection, especially at 12 hpi. Furthermore, CgEC124 positively regulated the pathogenicity, but it did not impact the vegetative growth of mycelia. Ecotopic transient expression of CgEC124 decreased the disease resistance and callose deposition in maize. Moreover, CgEC124 exhibited the β-1,3-glucanase activity and suppresses glucan-induced ROS burst in maize leaves. Our results indicate that CgEC124 is required for full virulence of C. graminicola but not for vegetative growth. CgEC124 increases maize susceptibility by inhibiting host reactive oxygen species burst as well as callose deposition. Meanwhile, our data suggests that CgEC124 explores its β-1,3-glucanase activity to prevent induction of host defenses.
Sections du résumé
BACKGROUND
BACKGROUND
Many phytopathogens secrete a large number of cell wall degrading enzymes (CWDEs) to decompose host cell walls in order to penetrate the host, obtain nutrients and accelerate colonization. There is a wide variety of CWDEs produced by plant pathogens, including glycoside hydrolases (GHs), which determine the virulence, pathogenicity, and host specificity of phytopathogens. The specific molecular mechanisms by which pathogens suppress host immunity remain obscure.
RESULT
RESULTS
In this study, we found that CgEC124 encodes a glycosyl hydrolase with a signal peptide and a conserved Glyco_hydro_cc domain which belongs to glycoside hydrolase 128 family. The expression of CgEC124 was significantly induced in the early stage of Colletotrichum graminicola infection, especially at 12 hpi. Furthermore, CgEC124 positively regulated the pathogenicity, but it did not impact the vegetative growth of mycelia. Ecotopic transient expression of CgEC124 decreased the disease resistance and callose deposition in maize. Moreover, CgEC124 exhibited the β-1,3-glucanase activity and suppresses glucan-induced ROS burst in maize leaves.
CONCLUSIONS
CONCLUSIONS
Our results indicate that CgEC124 is required for full virulence of C. graminicola but not for vegetative growth. CgEC124 increases maize susceptibility by inhibiting host reactive oxygen species burst as well as callose deposition. Meanwhile, our data suggests that CgEC124 explores its β-1,3-glucanase activity to prevent induction of host defenses.
Identifiants
pubmed: 38671375
doi: 10.1186/s12870-024-05053-0
pii: 10.1186/s12870-024-05053-0
doi:
Substances chimiques
Glucan 1,3-beta-Glucosidase
EC 3.2.1.58
Fungal Proteins
0
Glucans
0
Reactive Oxygen Species
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
339Informations de copyright
© 2024. The Author(s).
Références
Yang C, Liu R, Pang J, Ren B, Zhou H, Wang G, et al. Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat Commun. 2021;12:1–13.
Ospina-giraldo MD, Griffith JG, Laird EW, Mingora C. The CAZyome of Phytophthora spp.: A comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genomics. 2010;11:1–16.
doi: 10.1186/1471-2164-11-525
Bradley EL, Doehlemann G, Henrissat B, Bradshaw RE, Mesarich CH. Secreted glycoside hydrolase proteins as effectors and invasion patterns of plant-associated fungi and oomycetes. Front Plant Sci. 2022;13:1–16.
doi: 10.3389/fpls.2022.853106
Hane JK, Paxman J, Jones DAB, Oliver RP, De WP, Tyler BM, et al. “ CATAStrophy”, a genome-informed trophic classification of filamentous plant pathogens – how many different types of filamentous plant pathogens are there ? Front Microbiol. 2020;10:1–12.
doi: 10.3389/fmicb.2019.03088
Liu H, Lu X, Li M, Lun Z, Yan X, Yin C, et al. Plant immunity suppression by an exo-β-1,3-glucanase and an elongation factor 1α of the rice blast fungus. Nat Commun. 2023;14:1–16.
Moreno-s I, Pejenaute-O M, Navarrete B, Barrales RR, Ibeas JI. Ustilago maydis secreted endo-xylanases are involved in fungal filamentation and proliferation on and inside plants. J fun. 2021;7:1–19.
Ökmen B, Jaeger E, Schilling L, Finke N, Klemd A, Lee YJ, et al. A conserved enzyme of smut fungi facilitates cell-to-cell extension in the plant bundle sheath. Nat Commun. 2022;13:1–13.
doi: 10.1038/s41467-022-33815-7
Ma Z, Song T, Zhu L, Ye W, Wang Y, Shao Y, et al. A phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell. 2015;27:2057–72.
pubmed: 26163574
pmcid: 4531360
doi: 10.1105/tpc.15.00390
Zhang L, Yan J, Fu Z, Shi W, Ninkuu V, Li G, et al. FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum, triggers cell death and modulates plant immunity. Mol Plant Pathol. 2021;22:522–38.
pubmed: 33675158
pmcid: 8035634
doi: 10.1111/mpp.13041
Gui YJ, Chen JY, Zhang DD, Li NY, Li TG, Zhang WQ, et al. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environ Microbiol. 2017;19:1914–32.
pubmed: 28205292
doi: 10.1111/1462-2920.13695
Xu G, Zhong X, Shi Y, Liu Z, Jiang N, Liu J, et al. A fungal effector targets a heat shock-dynamin protein complex to modulate mitochondrial dynamics and reduce plant immunity. Sci Adv. 2020;6:1–11.
doi: 10.1126/sciadv.abb7719
Wang Y, Xu Y, Sun Y, Wang H, Qi J, Wan B, et al. Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection. Nat Commun. 2018;9:1–12.
Ma Z, Zhu L, Song T, Wang Y, Zhang Q, Xia Y, et al. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science. 2017;355:710–4.
pubmed: 28082413
doi: 10.1126/science.aai7919
Cao J, Yang C, Li L, Jiang L, Wu Y, Wu C, et al. Rice plasma membrane proteomics reveals Magnaporthe oryzae promotes susceptibility by sequential activation of host hormone signaling pathways. Mol Plant-Microbe Interact. 2016;29:902–13.
pubmed: 27800704
doi: 10.1094/MPMI-08-16-0165-R
Yang C, Yu Y, Huang J, Meng F, Pang J, Zhao Q, et al. Binding of the Magnaporthe oryzae chitinase MoChia1 by a rice tetratricopeptide repeat protein allows free chitin to trigger immune responses. Plant Cell. 2019;31:172–88.
pubmed: 30610168
pmcid: 6391695
doi: 10.1105/tpc.18.00382
Boutrot F, Zipfel C. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol. 2017;55:257–86.
pubmed: 28617654
doi: 10.1146/annurev-phyto-080614-120106
Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–9.
pubmed: 17108957
doi: 10.1038/nature05286
Wang B, Andargie M, Fang R. The function and biosynthesis of callose in high plants. Heliyon. 2022;8:1–5.
Han X, Huang LJ, Feng D, Jiang W, Miu W, Li N. Plasmodesmata-related structural and functional proteins: The long sought-after secrets of a cytoplasmic channel in plant cell walls. Int J Mol Sci. 2019;20:1–16.
doi: 10.3390/ijms20122946
Radja A, Horsley EM, Lavrentovich MO, Sweeney AM. Pollen cell wall patterns form from modulated phases. Cell. 2019;176:856–68.
pubmed: 30735635
doi: 10.1016/j.cell.2019.01.014
Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J. Callose deposition: A multifaceted plant defense response. Mol Plant-Microbe Interact. 2011;24:183–93.
pubmed: 20955078
doi: 10.1094/MPMI-07-10-0149
Burch-Smith TM, Zambryski PC. Plasmodesmata paradigm shift: Regulation from without versus within. Annu Rev Plant Biol. 2012;63:239–60.
pubmed: 22136566
doi: 10.1146/annurev-arplant-042811-105453
Wang Y, Li X, Fan B, Zhu C, Chen Z. Regulation and function of defense-related callose deposition in plants. Int J Mol Sci. 2021;22:1–15.
Wang Z, Li X, Wang X, Liu N, Xu B, Peng Q, et al. Arabidopsis endoplasmic reticulum-localized ubac2 proteins interact with pamp-induced coiled-coil to regulate pathogen-induced callose deposition and plant immunity. Plant Cell. 2019;31:153–71.
pubmed: 30606781
pmcid: 6391690
doi: 10.1105/tpc.18.00334
Chen XY, Kim JY. Callose synthesis in higher plants. Plant Signal Behav. 2009;4:489–92.
pubmed: 19816126
pmcid: 2688293
doi: 10.4161/psb.4.6.8359
Jashni MK, Mehrabi R, Collemare J, Mesarich CH, de Wit PJGM. The battle in the apoplast: Further insights into the roles of proteases and their inhibitors in plant–pathogen interactions. Front Plant Sci. 2015;6:1–7.
doi: 10.3389/fpls.2015.00584
Belisário R, Robertson AE, Vaillancourt LJ. Maize anthracnose stalk rot in the genomic era. Plant Dis. 2022;106:2281–98.
pubmed: 35291814
doi: 10.1094/PDIS-10-21-2147-FE
O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet. 2012;44:1060–5.
pubmed: 22885923
pmcid: 9754331
doi: 10.1038/ng.2372
Shu X, Yin D, Liang J, Xiang T, Zhang C, Li H, et al. Tilletia horrida glycoside hydrolase family 128 protein, designated ThGhd_7, modulates plant immunity by blocking reactive oxygen species production. Plant Cell Environ. 2024;47:1–16.
Beernink BM, Holan KL, Lappe RR, Whitham SA. Direct agroinoculation of maize seedlings by injection with recombinant foxtail mosaic virus and sugarcane mosaic virus infectious clones. J Vis Exp. 2021;168:1–26.
Ökmen B, Mathow D, Hof A, Lahrmann U, Aßmann D, Doehlemann G. Mining the effector repertoire of the biotrophic fungal pathogen Ustilago hordei during host and non-host infection. Mol Plant Pathol. 2018;19:2603–22.
pubmed: 30047221
pmcid: 6638180
doi: 10.1111/mpp.12732
Chandrasekar B, Wanke A, Wawra S, Saake P, Mahdi L, Charura N, et al. Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses. Plant Cell. 2022;34:2765–84.
pubmed: 35441693
pmcid: 9252488
doi: 10.1093/plcell/koac114
Bray Speth E, Lee YN, He SY. Pathogen virulence factors as molecular probes of basic plant cellular functions. Curr Opin Plant Biol. 2007;10:580–6.
doi: 10.1016/j.pbi.2007.08.003
Ning N, Xie X, Yu H, Mei J, Li Q, Zuo S, et al. Plant peroxisome-targeting effector MoPtep1 is required for the virulence of Magnaporthe oryzae. Int J Mol Sci. 2022;23:1–15.
doi: 10.3390/ijms23052515
Huang J, Gu L, Zhang Y, Yan T, Kong G, Kong L, et al. An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun. 2017;8:1–15.
doi: 10.1038/s41467-017-02233-5
Zhao Z, Liu H, Wang C, Xu JR. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics. 2013;14:1–15.
doi: 10.1186/1471-2164-14-274
Gibson DM, King BC, Hayes ML, Bergstrom GC. Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr Opin Microbiol. 2011;14:264–70.
pubmed: 21536481
doi: 10.1016/j.mib.2011.04.002
Garfoot AL, Shen Q, Wüthrich M, Klein BS, Rappleye CA. The Eng1 β-glucanase enhances Histoplasma virulence by reducing β-glucan exposure. MBio. 2016;7:1–9.
doi: 10.1128/mBio.01388-15
Guo X, Liu N, Zhang Y, Chen J. Pathogen-associated molecular pattern active sites of GH45 endoglucanohydrolase from Rhizoctonia solani. Phytopathology. 2022;112:355–63.
pubmed: 34165320
doi: 10.1094/PHYTO-04-21-0164-R
Zhu W, Ronen M, Gur Y, Minz-Dub A, Masrati G, Ben-Tal N, et al. BcXYG1, a secreted xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses. Plant Physiol. 2017;175:438–56.
pubmed: 28710128
pmcid: 5580746
doi: 10.1104/pp.17.00375
Ökmen B, Bachmann D, de Wit PJGM. A conserved GH17 glycosyl hydrolase from plant pathogenic Dothideomycetes releases a DAMP causing cell death in tomato. Mol Plant Pathol. 2019;20:1710–21.
pubmed: 31603622
pmcid: 6859711
doi: 10.1111/mpp.12872
Sørensen I, Pettolino FA, Wilson SM, Doblin MS, Johansen B, Bacic A, et al. Mixed-linkage (1 → 3), (1 → 4)-β-D-glucan is not unique to the Poales and is an abundant component of Equisetum arvense cell walls. Plant J. 2008;54:510–21.
pubmed: 18284587
doi: 10.1111/j.1365-313X.2008.03453.x
Chowdhury J, Henderson M, Schweizer P, Burton RA, Fincher GB, Little A. Differential accumulation of callose, arabinoxylan and cellulose in nonpenetrated versus penetrated papillae on leaves of barley infected with Blumeria graminis f. sp. hordei. New Phytol. 2014;204:650–60.
pubmed: 25138067
doi: 10.1111/nph.12974
Wanke A, Rovenich H, Schwanke F, Velte S, Becker S, Hehemann JH, et al. Plant species-specific recognition of long and short β-1,3-linked glucans is mediated by different receptor systems. Plant J. 2020;102:1142–56.
pubmed: 31925978
doi: 10.1111/tpj.14688
Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. DOG 1.0: Illustrator of protein domain structures. Cell Res. 2009;19:271–3.
pubmed: 19153597
doi: 10.1038/cr.2009.6
Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420–3.
pubmed: 30778233
doi: 10.1038/s41587-019-0036-z
Gietz RD, Schiestl RH, Willems AR, Woods RA. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 1995;11:355–60.
pubmed: 7785336
doi: 10.1002/yea.320110408
Yin W, Wang Y, Chen T, Lin Y, Luo C. Functional evaluation of the signal peptides of secreted proteins. Bio-Protoc. 2018;8:1–8.
doi: 10.21769/BioProtoc.2839
Mei J, Ning N, Wu H, Chen X, Li Z, Liu W. Glycosylphosphatidylinositol anchor biosynthesis pathway-related protein GPI7 is required for the vegetative growth and pathogenicity of Colletotrichum graminicola. Int J Mol Sci. 2022;23:1–15.
doi: 10.3390/ijms23062985
Yu H, Ruan H, Xia X, Chicowski AS, Whitham SA, Li Z, et al. Maize FERONIA-like receptor genes are involved in the response of multiple disease resistance in maize. Mol Plant Pathol. 2022;23:1331–45.
pubmed: 35596601
pmcid: 9366073
doi: 10.1111/mpp.13232