Necrotrophic lifestyle of Rhizoctonia solani AG3-PT during interaction with its host plant potato as revealed by transcriptome analysis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 07 2020
28 07 2020
Historique:
received:
23
10
2019
accepted:
24
06
2020
entrez:
30
7
2020
pubmed:
30
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
The soil-borne pathogen Rhizoctonia solani infects a broad range of plants worldwide and is responsible for significant crop losses. Rhizoctonia solani AG3-PT attacks germinating potato sprouts underground while molecular responses during interaction are unknown. To gain insights into processes induced in the fungus especially at early stage of interaction, transcriptional activity was compared between growth of mycelium in liquid culture and the growing fungus in interaction with potato sprouts using RNA-sequencing. Genes coding for enzymes with diverse hydrolase activities were strongly differentially expressed, however with remarkably dissimilar time response. While at 3 dpi, expression of genes coding for peptidases was predominantly induced, strongest induction was found for genes encoding hydrolases acting on cell wall components at 8 dpi. Several genes with unknown function were also differentially expressed, thus assuming putative roles as effectors to support host colonization. In summary, the presented analysis characterizes the necrotrophic lifestyle of R. solani AG3-PT during early interaction with its host.
Identifiants
pubmed: 32724205
doi: 10.1038/s41598-020-68728-2
pii: 10.1038/s41598-020-68728-2
pmc: PMC7387450
doi:
Substances chimiques
Fungal Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
12574Références
Yang, G. & Li. C. General description of Rhizoctonia species complex. In Plant Pathology, ed C.J. Cumagun (2012).
Ogoshi, A. Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kuhn. Annu. Rev. Phytopathol. 25, 125–143 (1987).
doi: 10.1146/annurev.py.25.090187.001013
Garcia, V. G., Onco, M. A. P. & Susan, V. R. Review. Biology and systematics of the form genus Rhizoctonia. Span. J. Agric. Res. 4, 55–79 (2006).
doi: 10.5424/sjar/2006041-178
Ajayi-Oyetunde, O. O. & Bradley, C. A. Rhizoctonia solani: taxonomy, population biology and management of rhizoctonia seedling disease of soybean. Plant Pathol. 67, 3–17 (2018).
doi: 10.1111/ppa.12733
Carling, D. E., Kuninaga, S. & Brainard, K. A. Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology 92, 43–50. https://doi.org/10.1094/PHYTO.2002.92.1.43 (2002).
doi: 10.1094/PHYTO.2002.92.1.43
pubmed: 18944138
Sharon, M., Kuninaga, S., Hyakumachi, M., Naito, S. & Sneh, B. Classification of Rhizoctonia spp. using rDNA-ITS sequence analysis supports the genetic basis of the classical anastomosis grouping. Mycoscience 49, 93–114. https://doi.org/10.1007/s10267-007-0394-0 (2008).
doi: 10.1007/s10267-007-0394-0
Wibberg, D. et al. Development of a Rhizoctonia solani AG1-IB specific gene model enables comparative genome analyses between phytopathogenic R. solani AG1-IA, AG1-IB, AG3 and AG8 isolates. PLoS ONE 10, e0144769. https://doi.org/10.1371/journal.pone.0144769 (2015).
doi: 10.1371/journal.pone.0144769
pubmed: 26690577
pmcid: 4686921
Banville, G. J. Yield losses and damage to potato plants caused by Rhizoctonia solani Kuhn. Am. Potato J. 66, 821–834 (1989).
doi: 10.1007/BF02853963
Campion, C., Chatot, C., Perraton, B. & Andrivon, D. Anastomosis groups, pathogenicity and sensitivity to fungicides of Rhizoctonia solani isolates collected on potato crops in France. Eur. J. Plant Pathol. 109, 983–992. https://doi.org/10.1023/B:EJPP.0000003829.83671.8f (2003).
doi: 10.1023/B:EJPP.0000003829.83671.8f
Woodhall, J. W., Lees, A. K., Edwards, S. G. & Jenkinson, P. Characterization of Rhizoctonia solani from potato in Great Britain. Plant Pathol. 56, 286–295. https://doi.org/10.1111/j.1365-3059.2006.01545.x (2007).
doi: 10.1111/j.1365-3059.2006.01545.x
Lehtonen, M. J., Somervuo, P. & Valkonen, J. P. Infection with Rhizoctonia solani induces defense genes and systemic resistance in potato sprouts grown without light. Phytopathology 98, 1190–1198. https://doi.org/10.1094/PHYTO-98-11-1190 (2008).
doi: 10.1094/PHYTO-98-11-1190
pubmed: 18943407
Tsror, L. Biology, epidemiology and management of Rhizoctonia solani on potato. J. Phytopathol. 158, 649–658. https://doi.org/10.1111/j.1439-0434.2010.01671.x (2010).
doi: 10.1111/j.1439-0434.2010.01671.x
Fiers, M. et al. Genetic diversity of Rhizoctonia solani associated with potato tubers in France. Mycologia 103, 1230–1244. https://doi.org/10.3852/10-231 (2011).
doi: 10.3852/10-231
pubmed: 21642342
Kuninaga, S., Carling, D. E., Takeuchi, T. & Yokosawa, R. Comparison of rDNA-ITS sequences between potato and tobacco strains in Rhizoctonia solani AG-3. J. Gen. Plant Pathol. 66, 2–11. https://doi.org/10.1007/PL00012917 (2000).
doi: 10.1007/PL00012917
Wilson, P. S., Ketola, E. O., Ahvenniemi, P. M., Lehtonen, M. J. & Valkonen, J. P. T. Dynamics of soilborne Rhizoctonia solani in the presence of Trichoderma harzianum: effects on stem canker, black scurf and progeny tubers of potato. Plant Pathol. 57, 152–161. https://doi.org/10.1111/j.1365-3059.2007.01706.x (2008).
doi: 10.1111/j.1365-3059.2007.01706.x
Hide, G. A. & Horrocks, J. K. Influence of stem canker (Rhizoctonia solani Kuhn) on tuber yield, tuber size, reducing sugars and crisp color in cv Record. Potato Res. 37, 43–49 (1994).
doi: 10.1007/BF02360431
Stevenson, W. R., Loria, R., Franc, G. D. & Weingartner, D. P. Compendium of potato diseases 2nd edn. (American Phytopathological Society Press, New York, 2001).
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
Horbach, R., Navarro-Quesada, A. R., Knogge, W. & Deising, H. B. When and how to kill a plant cell: infection strategies of plant pathogenic fungi. J. Plant Physiol. 168, 51–62. https://doi.org/10.1016/j.jplph.2010.06.014 (2011).
doi: 10.1016/j.jplph.2010.06.014
pubmed: 20674079
Laluk, K. & Mengiste, T. Necrotroph attacks on plants: wanton destruction or covert extortion?. Arabidopsis Book 8, e0136. https://doi.org/10.1199/tab.0136 (2010).
doi: 10.1199/tab.0136
pubmed: 22303261
pmcid: 3244965
Mengiste, T. Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 50, 267–294. https://doi.org/10.1146/annurev-phyto-081211-172955 (2012).
doi: 10.1146/annurev-phyto-081211-172955
pubmed: 22726121
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
Zhang, X. Y. et al. Histological observation of potato in response to Rhizoctonia solani infection. Eur. J. Plant Pathol. 145, 289–303. https://doi.org/10.1007/s10658-015-0842-1 (2016).
doi: 10.1007/s10658-015-0842-1
Kankam, F. et al. Isolation, purification and characterization of phytotoxins produced by Rhizoctonia solani AG-3, the cause agent of potato stem canker. Am. J. Potato Res. 93, 321–330 (2016).
doi: 10.1007/s12230-016-9506-8
Genzel, F., Franken, P., Witzel, K. & Grosch, R. Systemic induction of salicylic acid-related plant defences in potato in response to Rhizoctonia solani AG3PT. Plant Pathol. 67, 337–348 (2018).
doi: 10.1111/ppa.12746
Rioux, R. et al. Comparative analysis of putative pathogenesis-related gene expression in two Rhizoctonia solani pathosystems. Curr. Genet. 57, 391–408. https://doi.org/10.1007/s00294-011-0353-3 (2011).
doi: 10.1007/s00294-011-0353-3
pubmed: 21909999
Samsatly, J., Copley, T. R. & Jabaji, S. H. Antioxidant genes of plants and fungal pathogens are distinctly regulated during disease development in different Rhizoctonia solani pathosystems. PLoS ONE 13, e0192682. https://doi.org/10.1371/journal.pone.0192682 (2018).
doi: 10.1371/journal.pone.0192682
pubmed: 29466404
pmcid: 5821333
Yang, F., Li, W. S. & Jorgensen, H. J. L. Transcriptional reprogramming of wheat and the hemibiotrophic pathogen Septoria tritici during two phases of the compatible interaction. PLoS ONE 8, e81606. https://doi.org/10.1371/journal.pone.0081606 (2013).
doi: 10.1371/journal.pone.0081606
pubmed: 24303057
pmcid: 3841193
Wibberg, D. et al. Transcriptome analysis of the phytopathogenic fungus Rhizoctonia solani AG1-IB 7/3/14 applying high-throughput sequencing of expressed sequence tags (ESTs). Fungal Biol. Uk 118, 800–813. https://doi.org/10.1016/j.funbio.2014.06.007 (2014).
doi: 10.1016/j.funbio.2014.06.007
Verwaaijen, B. et al. The Rhizoctonia solani AG1-IB (isolate 7/3/14) transcriptome during interaction with the host plant lettuce (Lactuca sativa L.). PLoS ONE 12, e0177278. https://doi.org/10.1371/journal.pone.0177278 (2017).
doi: 10.1371/journal.pone.0177278
pubmed: 28486484
pmcid: 5423683
Verwaaijen, B. et al. A comprehensive analysis of the Lactuca sativa, L. transcriptome during different stages of the compatible interaction with Rhizoctonia solani. Sci. Rep. 9, 7221. https://doi.org/10.1038/s41598-019-43706-5 (2019).
doi: 10.1038/s41598-019-43706-5
pubmed: 31076623
pmcid: 6510776
Copley, T. R., Duggavathi, R. & Jabaji, S. The transcriptional landscape of Rhizoctonia solani AG1-IA during infection of soybean as defined by RNA-seq. PLoS ONE 12, e0184095. https://doi.org/10.1371/journal.pone.0184095 (2017).
doi: 10.1371/journal.pone.0184095
pubmed: 28877263
pmcid: 5587340
Gkarmiri, K. et al. Transcriptomic changes in the plant pathogenic fungus Rhizoctonia solani AG-3 in response to the antagonistic bacteria Serratia proteamaculans and Serratia plymuthica. BMC Genom. 16, 630. https://doi.org/10.1186/s12864-015-1758-z (2015).
doi: 10.1186/s12864-015-1758-z
Wibberg, D. et al. Draft genome sequence of the potato pathogen Rhizoctonia solani AG3-PT isolate Ben3. Arch Microbiol 199, 1065–1068. https://doi.org/10.1007/s00203-017-1394-x (2017).
doi: 10.1007/s00203-017-1394-x
pubmed: 28597196
Cubeta, M. A. et al. Draft genome sequence of the plant-pathogenic soil fungus Rhizoctonia solani anastomosis group 3 strain Rhs1AP. Genome Announc. https://doi.org/10.1128/genomeA.01072-14 (2014).
doi: 10.1128/genomeA.01072-14
pubmed: 25359908
pmcid: 4214984
Patil, V. U., Girimalla, V., Sagar, V., Bhardwaj, V. & Chakrabarti, S. K. Draft genome sequencing of Rhizoctonia solani anastomosis group 3 (AG3-PT) causing stem canker and black scurf of potato. Am. J. Potato Res. 95, 87–91. https://doi.org/10.1007/s12230-017-9606-0 (2018).
doi: 10.1007/s12230-017-9606-0
Kellens, J. T. C. & Peumans, W. J. Developmental accumulation of lectin in Rhizoctonia solani - a potential role as a storage protein. J. Gen. Microbiol. 136, 2489–2495. https://doi.org/10.1099/00221287-136-12-2489 (1990).
doi: 10.1099/00221287-136-12-2489
Palma, L., Munoz, D., Berry, C., Murillo, J. & Caballero, P. Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6, 3296–3325. https://doi.org/10.3390/toxins6123296 (2014).
doi: 10.3390/toxins6123296
pubmed: 25514092
pmcid: 4280536
Ohba, M., Mizuki, E. & Uemori, A. Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res. 29, 427–433 (2009).
pubmed: 19331182
van Driel, K. G. A. et al. Septal pore cap protein SPC18, isolated from the basidiomycetous fungus Rhizoctonia solani, also resides in pore plugs. Eukaryot. Cell 7, 1865–1873. https://doi.org/10.1128/Ec.00125-08 (2008).
doi: 10.1128/Ec.00125-08
pubmed: 18757567
pmcid: 2568075
Nagase, H. & Woessner, J. F. Jr. Matrix metalloproteinases. J. Biol. Chem. 274, 21491–21494. https://doi.org/10.1074/jbc.274.31.21491 (1999).
doi: 10.1074/jbc.274.31.21491
pubmed: 10419448
Dufour, A., Sampson, N. S., Zucker, S. & Cao, J. Role of the hemopexin domain of matrix metalloproteinases in cell migration. J. Cell Physiol. 217, 643–651. https://doi.org/10.1002/jcp.21535 (2008).
doi: 10.1002/jcp.21535
pubmed: 18636552
pmcid: 2574584
Hilker, R. et al. ReadXplorer–visualization and analysis of mapped sequences. Bioinformatics 30, 2247–2254. https://doi.org/10.1093/bioinformatics/btu205 (2014).
doi: 10.1093/bioinformatics/btu205
pubmed: 24790157
pmcid: 4217279
Xu, X. H., He, Q., Chen, C. & Zhang, C. L. Differential communications between fungi and host plants revealed by secretome analysis of phylogenetically related endophytic and pathogenic fungi. PLoS ONE 11, e0163368. https://doi.org/10.1371/journal.pone.0163368 (2016).
doi: 10.1371/journal.pone.0163368
pubmed: 27658302
pmcid: 5033329
Krishnan, P., Ma, X., McDonald, B. A. & Brunner, P. C. Widespread signatures of selection for secreted peptidases in a fungal plant pathogen. BMC Evol. Biol. 18, 7. https://doi.org/10.1186/s12862-018-1123-3 (2018).
doi: 10.1186/s12862-018-1123-3
pubmed: 29368587
pmcid: 5784588
Lowe, R. G. T. et al. Extracellular peptidases of the cereal pathogen Fusarium graminearum. Front. Plant Sci. 6, 962. https://doi.org/10.3389/fpls.2015.00962 (2015).
doi: 10.3389/fpls.2015.00962
pubmed: 26635820
pmcid: 4645717
Wibberg, D. et al. Genome analysis of the sugar beet pathogen Rhizoctonia solani AG2-2IIIB revealed high numbers in secreted proteins and cell wall degrading enzymes. BMC Genom. 17, 245. https://doi.org/10.1186/s12864-016-2561-1 (2016).
doi: 10.1186/s12864-016-2561-1
Xia, Y. J. Proteases in pathogenesis and plant defence. Cell. Microbiol. 6, 905–913. https://doi.org/10.1111/j.1462-5822.2004.00438.x (2004).
doi: 10.1111/j.1462-5822.2004.00438.x
pubmed: 15339266
Franceschetti, M. et al. Effectors of filamentous plant pathogens: commonalities amid diversity. Microbiol. Mol. Biol. Rev. https://doi.org/10.1128/MMBR.0006616 (2017).
doi: 10.1128/MMBR.0006616
pubmed: 28356329
pmcid: 5485802
Boller, T. & He, S. Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324, 742–744. https://doi.org/10.1126/science.1171647 (2009).
doi: 10.1126/science.1171647
pubmed: 19423812
pmcid: 2729760
Cui, H., Xiang, T. & Zhou, J. M. Plant immunity: a lesson from pathogenic bacterial effector proteins. Cell Microbiol. 11, 1453–1461. https://doi.org/10.1111/j.1462-5822.2009.01359.x (2009).
doi: 10.1111/j.1462-5822.2009.01359.x
pubmed: 19622098
Dou, D. & Zhou, J. M. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484–495. https://doi.org/10.1016/j.chom.2012.09.003 (2012).
doi: 10.1016/j.chom.2012.09.003
pubmed: 23084917
Liu, T. et al. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5, 4686. https://doi.org/10.1038/ncomms5686 (2014).
doi: 10.1038/ncomms5686
pubmed: 25156390
pmcid: 4348438
Qin, J. et al. The plant-specific transcription factors CBP6Og and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. Elife 7, e34902. https://doi.org/10.7554/eLife.34902 (2018).
doi: 10.7554/eLife.34902
pubmed: 29757140
pmcid: 5993538
Soustre, I., Letourneux, Y. & Karst, F. Characterization of the Saccharomyces cerevisiae RTA1 gene involved in 7-aminocholesterol resistance. Curr Genet 30, 121–125. https://doi.org/10.1007/s002940050110 (1996).
doi: 10.1007/s002940050110
pubmed: 8660468
Manente, M. & Ghislain, M. The lipid-translocating exporter family and membrane phospholipid homeostasis in yeast. FEMS Yeast Res. 9, 673–687. https://doi.org/10.1111/j.1567-1364.2009.00513.x (2009).
doi: 10.1111/j.1567-1364.2009.00513.x
pubmed: 19416366
Kawahara, Y. et al. Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7, e49423. https://doi.org/10.1371/journal.pone.0049423 (2012).
doi: 10.1371/journal.pone.0049423
pubmed: 23139845
pmcid: 3490861
Bolton, M. D. & Thomma, B. P. H. J. The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiol. Mol. Plant Pathol. 72, 104–110. https://doi.org/10.1016/j.pmpp.2008.07.001 (2008).
doi: 10.1016/j.pmpp.2008.07.001
Fernandez, J., Marroquin-Guzman, M. & Wilson, R. A. Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annu. Rev. Phytopathol. 52, 155–174. https://doi.org/10.1146/annurev-phyto-102313-050135 (2014).
doi: 10.1146/annurev-phyto-102313-050135
pubmed: 24848414
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: 23618408
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628. https://doi.org/10.1038/nmeth.1226 (2008).
doi: 10.1038/nmeth.1226
pubmed: 18516045
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).
doi: 10.1186/s13059-014-0550-8
pubmed: 4302049
pmcid: 4302049
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).
Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676. https://doi.org/10.1093/bioinformatics/bti610 (2005).
doi: 10.1093/bioinformatics/bti610
Andersen, C. L., Jensen, J. L. & Ørntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250. https://doi.org/10.1158/0008-5472.CAN-04-0496 (2004).
doi: 10.1158/0008-5472.CAN-04-0496
pubmed: 15289330