Identification of effector candidate genes of Rhizoctonia solani AG-1 IA expressed during infection in Brachypodium distachyon.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
10 09 2020
10 09 2020
Historique:
received:
30
04
2020
accepted:
24
08
2020
entrez:
11
9
2020
pubmed:
12
9
2020
medline:
16
3
2021
Statut:
epublish
Résumé
Rhizoctonia solani is a necrotrophic phytopathogen belonging to basidiomycetes. It causes rice sheath blight which inflicts serious damage in rice production. The infection strategy of this pathogen remains unclear. We previously demonstrated that salicylic acid-induced immunity could block R. solani AG-1 IA infection in both rice and Brachypodium distachyon. R. solani may undergo biotrophic process using effector proteins to suppress host immunity before necrotrophic stage. To identify pathogen genes expressed at the early infection process, here we developed an inoculation method using B. distachyon which enables to sample an increased amount of semi-synchronous infection hyphae. Sixty-one R. solani secretory effector-like protein genes (RsSEPGs) were identified using in silico approach with the publicly available gene annotation of R. solani AG-1 IA genome and our RNA-sequencing results obtained from hyphae grown on agar medium. Expression of RsSEPGs was analyzed at 6, 10, 16, 24, and 32 h after inoculation by a quantitative reverse transcription-polymerase chain reaction and 52 genes could be detected at least on a single time point tested. Their expressions showed phase-specific patterns which were classified into 6 clusters. The 23 RsSEPGs in the cluster 1-3 and 29 RsSEPGs in the cluster 4-6 are expected to be involved in biotrophic and necrotrophic interactions, respectively.
Identifiants
pubmed: 32913311
doi: 10.1038/s41598-020-71968-x
pii: 10.1038/s41598-020-71968-x
pmc: PMC7483729
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14889Références
Anderson, N. A. The genetics and pathology of Rhizoctonia solani. Annu. Rev. Phytopathol. 20, 329–347 (1982).
doi: 10.1146/annurev.py.20.090182.001553
Ogoshi, A. Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kühn. Annu. Rev. Phytopathol. 25, 125–143 (1987).
doi: 10.1146/annurev.py.25.090187.001013
Lee, F. & Rush, M. Rice sheath blight: a major rice disease. Plant Dis. 67, 829–832 (1983).
doi: 10.1094/PD-67-829
Hashiba, T. Estimation method of severity and yield loss by rice sheath blight disease. Bull. Hokuriku Natl. Agric. Exp. Station 26, 115–164 (1984).
Uppala, S. S. & Zhou, X.-G. Rice sheath blight. The Plant Health Instructor. https://doi.org/10.1094/PHI-I-2018-0403-01 (2018).
Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923 (2005).
doi: 10.1146/annurev.phyto.43.040204.135923
pubmed: 16078883
Selin, C., de Kievit, T. R., Belmonte, M. F. & Fernando, W. G. Elucidating the role of effectors in plant-fungal interactions: progress and challenges. Front. Microbiol. 7, 600. https://doi.org/10.3389/fmicb.2016.00600 (2016).
doi: 10.3389/fmicb.2016.00600
pubmed: 27199930
pmcid: 4846801
de Jonge, R., Bolton, M. D. & Thomma, B. P. How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr. Opin. Plant Biol. 14, 400–406. https://doi.org/10.1016/j.pbi.2011.03.005 (2011).
doi: 10.1016/j.pbi.2011.03.005
pubmed: 21454120
Tan, K.-C., Oliver, R. P., Solomon, P. S. & Moffat, C. S. Proteinaceous necrotrophic effectors in fungal virulence. Funct. Plant Biol. 37, 907–912 (2010).
doi: 10.1071/FP10067
Wang, X., Jiang, N., Liu, J., Liu, W. & Wang, G. L. The role of effectors and host immunity in plant-necrotrophic fungal interactions. Virulence 5, 722–732. https://doi.org/10.4161/viru.29798 (2014).
doi: 10.4161/viru.29798
pubmed: 25513773
pmcid: 4189878
Balance, G., Lamari, L. & Bernier, C. Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 35, 203–213 (1989).
doi: 10.1016/0885-5765(89)90051-9
Tuori, R. P., Wolpert, T. J. & Ciuffetti, L. M. Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 8, 41–48 (1995).
doi: 10.1094/MPMI-8-0041
Tomas, A., Feng, G., Reeck, G., Bockus, W. & Leach, J. Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol. Plant Microbe Interact. 3, 221–224 (1990).
doi: 10.1094/MPMI-3-221
Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. U. S. A. 107, 13544–13549. https://doi.org/10.1073/pnas.1004090107 (2010).
doi: 10.1073/pnas.1004090107
pubmed: 20624958
pmcid: 2922177
Lorang, J. M., Sweat, T. A. & Wolpert, T. J. Plant disease susceptibility conferred by a “resistance” gene. Proc. Natl. Acad. Sci. U. S. A. 104, 14861–14866. https://doi.org/10.1073/pnas.0702572104 (2007).
doi: 10.1073/pnas.0702572104
pubmed: 17804803
pmcid: 1976202
Lorang, J. et al. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338, 659–662. https://doi.org/10.1126/science.1226743 (2012).
doi: 10.1126/science.1226743
pubmed: 23087001
pmcid: 4125361
de Jonge, R. et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 109, 5110–5115. https://doi.org/10.1073/pnas.1119623109 (2012).
doi: 10.1073/pnas.1119623109
pubmed: 22416119
pmcid: 3323992
Kawchuk, L. M. et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. U. S. A. 98, 6511–6515. https://doi.org/10.1073/pnas.091114198 (2001).
doi: 10.1073/pnas.091114198
pubmed: 11331751
pmcid: 33499
Kombrink, A. et al. Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts. Mol. Plant Pathol. 18, 596–608. https://doi.org/10.1111/mpp.12520 (2017).
doi: 10.1111/mpp.12520
pubmed: 27911046
pmcid: 6638240
Qin, J. et al. The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. eLife https://doi.org/10.7554/eLife.34902 (2018).
doi: 10.7554/eLife.34902
pubmed: 29927384
pmcid: 6029845
Aoki, H., Sassa, T. & Tamura, T. Phytotoxic metabolites of Rhizoctonia solani. Nature 200, 575 (1963).
doi: 10.1038/200575a0
Vidhyasekaran, P. et al. Host-specific toxin production by Rhizoctonia solani, the rice sheath blight pathogen. Phytopathology 87, 1258–1263. https://doi.org/10.1094/PHYTO.1997.87.12.1258 (1997).
doi: 10.1094/PHYTO.1997.87.12.1258
pubmed: 18945027
Zheng, A. et al. The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat. Commun. 4, 1424. https://doi.org/10.1038/ncomms2427 (2013).
doi: 10.1038/ncomms2427
pubmed: 23361014
pmcid: 3562461
Anderson, J. P. et al. Proteomic Analysis of Rhizoctonia solani identifies infection-specific, redox associated proteins and insight into adaptation to different plant hosts. Mol. Cell Proteomics 15, 1188–1203. https://doi.org/10.1074/mcp.M115.054502 (2016).
doi: 10.1074/mcp.M115.054502
pubmed: 26811357
pmcid: 4824849
Kouzai, Y. et al. Salicylic acid-dependent immunity contributes to resistance against Rhizoctonia solani, a necrotrophic fungal agent of sheath blight, in rice and Brachypodium distachyon. New Phytol. 217, 771–783. https://doi.org/10.1111/nph.14849 (2018).
doi: 10.1111/nph.14849
pubmed: 29048113
Kouzai, Y. et al. Benzothiadiazole, a plant defense inducer, negatively regulates sheath blight resistance in Brachypodium distachyon. Sci. Rep. 8, 17358. https://doi.org/10.1038/s41598-018-35790-w (2018).
doi: 10.1038/s41598-018-35790-w
pubmed: 30478396
pmcid: 6255916
Kouzai, Y. et al. Expression profiling of marker genes responsive to the defence-associated phytohormones salicylic acid, jasmonic acid and ethylene in Brachypodium distachyon. BMC Plant Biol. 16, 59. https://doi.org/10.1186/s12870-016-0749-9 (2016).
doi: 10.1186/s12870-016-0749-9
pubmed: 26935959
pmcid: 4776424
Nováková, M., Sašek, V., Dobrev, P. I., Valentová, O. & Burketová, L. Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum—reassessing the role of salicylic acid in the interaction with a necrotroph. Plant Physiol. Biochem. 80, 308–317. https://doi.org/10.1016/j.plaphy.2014.04.019 (2014).
doi: 10.1016/j.plaphy.2014.04.019
pubmed: 24837830
Xia, Y. et al. Transcriptome analysis reveals the host selection fitness mechanisms of the Rhizoctonia solani AG1IA pathogen. Sci. Rep. 7, 10120. https://doi.org/10.1038/s41598-017-10804-1 (2017).
doi: 10.1038/s41598-017-10804-1
pubmed: 28860554
pmcid: 5579035
Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786. https://doi.org/10.1038/nmeth.1701 (2011).
doi: 10.1038/nmeth.1701
pubmed: 21959131
Emanuelsson, O., Nielsen, H., Brunak, S. & von Heijne, G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005–1016. https://doi.org/10.1006/jmbi.2000.3903 (2000).
doi: 10.1006/jmbi.2000.3903
pubmed: 10891285
Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580. https://doi.org/10.1006/jmbi.2000.4315 (2001).
doi: 10.1006/jmbi.2000.4315
pubmed: 11152613
Pierleoni, A., Martelli, P. L. & Casadio, R. PredGPI: a GPI-anchor predictor. BMC Bioinformatics 9, 392. https://doi.org/10.1186/1471-2105-9-392 (2008).
doi: 10.1186/1471-2105-9-392
pubmed: 18811934
pmcid: 2571997
Sperschneider, J. et al. EffectorP: predicting fungal effector proteins from secretomes using machine learning. New Phytol. 210, 743–761. https://doi.org/10.1111/nph.13794 (2016).
doi: 10.1111/nph.13794
pubmed: 26680733
Cheadle, C., Vawter, M. P., Freed, W. J. & Becker, K. G. Analysis of microarray data using Z score transformation. J. Mol. Diagn. 5, 73–81. https://doi.org/10.1016/S1525-1578(10)60455-2 (2003).
doi: 10.1016/S1525-1578(10)60455-2
pubmed: 12707371
pmcid: 1907322
D’haeseleer, P. How does gene expression clustering work?. Nat. Biotechnol. 23, 1499–1501. https://doi.org/10.1038/nbt1205-1499 (2005).
doi: 10.1038/nbt1205-1499
pubmed: 16333293
Asai, S. et al. Expression profiling during arabidopsis/downy mildew interaction reveals a highly-expressed effector that attenuates responses to salicylic acid. PLoS Pathog. 10, e1004443. https://doi.org/10.1371/journal.ppat.1004443 (2014).
doi: 10.1371/journal.ppat.1004443
pubmed: 25329884
pmcid: 4199768
Nobori, T. et al. Transcriptome landscape of a bacterial pathogen under plant immunity. Proc. Natl. Acad. U. S. A. 115, E3055–E3064. https://doi.org/10.1073/pnas.1800529115 (2018).
doi: 10.1073/pnas.1800529115
Yamamoto, N. et al. Integrative transcriptome analysis discloses the molecular basis of a heterogeneous fungal phytopathogen complex, Rhizoctonia solani AG-1 subgroups. Sci. Rep. 9, 19626. https://doi.org/10.1038/s41598-019-55734-2 (2019).
doi: 10.1038/s41598-019-55734-2
pubmed: 31873088
pmcid: 6928066
Singh, K., Winter, M., Zouhar, M. & Ryšánek, P. Cyclophilins: Less studied proteins with critical roles in pathogenesis. Phytopathology 108, 6–14. https://doi.org/10.1094/PHYTO-05-17-0167-RVW (2018).
doi: 10.1094/PHYTO-05-17-0167-RVW
pubmed: 28643580
Viaud, M. C., Balhadère, P. V. & Talbot, N. J. A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14, 917–930. https://doi.org/10.1105/tpc.010389 (2002).
doi: 10.1105/tpc.010389
pubmed: 11971145
pmcid: 150692
Viaud, M., Brunet-Simon, A., Brygoo, Y., Pradier, J. M. & Levis, C. Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea. Mol. Microbiol. 50, 1451–1465 (2003).
doi: 10.1046/j.1365-2958.2003.03798.x
Chen, M. M. et al. CYP1, a hypovirus-regulated cyclophilin, is required for virulence in the chestnut blight fungus. Mol. Plant Pathol. 12, 239–246. https://doi.org/10.1111/j.1364-3703.2010.00665.x (2011).
doi: 10.1111/j.1364-3703.2010.00665.x
pubmed: 21355996
Panwar, V., McCallum, B. & Bakkeren, G. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol. Biol. 81, 595–608. https://doi.org/10.1007/s11103-013-0022-7 (2013).
doi: 10.1007/s11103-013-0022-7
pubmed: 23417582
Williams, H. L. et al. Gene expression profiling of candidate virulence factors in the laminated root rot pathogen Phellinus sulphurascens. BMC Genomics 15, 603. https://doi.org/10.1186/1471-2164-15-603 (2014).
doi: 10.1186/1471-2164-15-603
pubmed: 25030912
pmcid: 4117978
Pennington, H. G. et al. The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathog. 15, e1007620. https://doi.org/10.1371/journal.ppat.1007620 (2019).
doi: 10.1371/journal.ppat.1007620
pubmed: 30856238
pmcid: 6464244
Zhang, S. & Xu, J. R. Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathog. 10, e1003826. https://doi.org/10.1371/journal.ppat.1003826 (2014).
doi: 10.1371/journal.ppat.1003826
pubmed: 24391496
pmcid: 3879361
Jia, Y., McAdams, S. A., Bryan, G. T., Hershey, H. P. & Valent, B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004–4014. https://doi.org/10.1093/emboj/19.15.4004 (2000).
doi: 10.1093/emboj/19.15.4004
pubmed: 10921881
pmcid: 306585
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, 490–495. https://doi.org/10.1093/nar/gkt1178 (2014).
doi: 10.1093/nar/gkt1178
Bolton, M. D. et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69, 119–136. https://doi.org/10.1111/j.1365-2958.2008.06270.x (2008).
doi: 10.1111/j.1365-2958.2008.06270.x
pubmed: 18452583
Dölfors, F., Holmquist, L., Dixelius, C. & Tzelepis, G. A LysM effector protein from the basidiomycete Rhizoctonia solani contributes to virulence through suppression of chitin-triggered immunity. Mol. Genet. Genomics https://doi.org/10.1007/s00438-019-01573-9 (2019).
doi: 10.1007/s00438-019-01573-9
pubmed: 31076860
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. https://doi.org/10.1038/nmeth.1923 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 22388286
Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36. https://doi.org/10.1186/gb-2013-14-4-r36 (2013).
doi: 10.1186/gb-2013-14-4-r36
pubmed: 23618408
pmcid: 4053844
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578. https://doi.org/10.1038/nprot.2012.016 (2012).
doi: 10.1038/nprot.2012.016
pubmed: 3334321
pmcid: 3334321
Untergasser, A. et al. Primer3–new capabilities and interfaces. Nucleic Acids Res. 40, e115. https://doi.org/10.1093/nar/gks596 (2012).
doi: 10.1093/nar/gks596
pubmed: 3424584
pmcid: 3424584
Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80. https://doi.org/10.1186/gb-2004-5-10-r80 (2004).
doi: 10.1186/gb-2004-5-10-r80
pubmed: 15461798
pmcid: 545600
Saeed, A. I. et al. TM4 microarray software suite. Methods Enzymol. 411, 134–193. https://doi.org/10.1016/S0076-6879(06)11009-5 (2006).
doi: 10.1016/S0076-6879(06)11009-5
pubmed: 16939790