Transcriptional profiling reveals multiple defense responses in downy mildew-resistant transgenic grapevine expressing a TIR-NBS-LRR gene located at the MrRUN1/MrRPV1 locus

Junjie Qu , Ian Dry , Lulu Liu , Zexi Guo , Ling Yin

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 161

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :161 DOI: 10.1038/s41438-021-00597-w
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Transcriptional profiling reveals multiple defense responses in downy mildew-resistant transgenic grapevine expressing a TIR-NBS-LRR gene located at the MrRUN1/MrRPV1 locus
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Abstract

Grapevine downy mildew (DM) is a destructive oomycete disease of viticulture worldwide. MrRPV1 is a typical TIR-NBS-LRR type DM disease resistance gene cloned from the wild North American grapevine species Muscadinia rotundifolia. However, the molecular basis of resistance mediated by MrRPV1 remains poorly understood. Downy mildew-susceptible Vitis vinifera cv. Shiraz was transformed with a genomic fragment containing MrRPV1 to produce DM-resistant transgenic Shiraz lines. Comparative transcriptome analysis was used to compare the transcriptome profiles of the resistant and susceptible genotypes after DM infection. Transcriptome modulation during the response to P. viticola infection was more rapid, and more genes were induced in MrRPV1-transgenic Shiraz than in wild-type plants. In DM-infected MrRPV1-transgenic plants, activation of genes associated with Ca2+ release and ROS production was the earliest transcriptional response. Functional analysis of differentially expressed genes revealed that key genes related to multiple phytohormone signaling pathways and secondary metabolism were highly induced during infection. Coexpression network and motif enrichment analysis showed that WRKY and MYB transcription factors strongly coexpress with stilbene synthase (VvSTS) genes during defense against P. viticola in MrRPV1-transgenic plants. Taken together, these findings indicate that multiple pathways play important roles in MrRPV1-mediated resistance to downy mildew.

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Junjie Qu, Ian Dry, Lulu Liu, Zexi Guo, Ling Yin. Transcriptional profiling reveals multiple defense responses in downy mildew-resistant transgenic grapevine expressing a TIR-NBS-LRR gene located at the MrRUN1/MrRPV1 locus. Horticulture Research, 2021, 8 (1) : 161 DOI:10.1038/s41438-021-00597-w

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References

[1]

Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).

[2]

Macho, A. P. & Zipfel, C. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54, 263-272 (2014).

[3]

Elmore, J. M., Lin, Z. J. & Coaker, G. Plant NB-LRR signaling: upstreams and downstreams. Curr. Opin. Plant Biol. 14, 365-371 (2011).

[4]

McHale, L., Tan, X. P., Koehl, P . & Michelmore, R. W. Plant NBS-LRR proteins: adaptable guards. Genome Biol. 7, 212 (2006).

[5]

Weaver, R. J. Grape Growing (Wiley: Hoboken, NJ, 1976).

[6]

Kamoun, S. et al. The top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16, 413-434 (2015).

[7]

Yu, Y., Zhang, Y. L., Yin, L. & Lu, J. The mode of host resistance to Plasmopara viticola infection of grapevines. Phytopathology 102, 1094-1101 (2012).

[8]

Merdinoglu, D. et al. Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia. Acta Hort. 603, 451-456 (2003).

[9]

Wiedemann-Merdinoglu, S. et al. Genetic analysis of resistance to downy mildew from Muscadinia rotundifolia. Ninth international conference on grape genetics and breeding, Udine, Italy, July 2-6 (2006).

[10]

Welter, L. J. et al. Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol. Breed. 20, 359-374 (2007).

[11]

Bellin, D. et al. Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localised necrosis at the infection site. Theor. Appl. Genet. 120, 163-176 (2009).

[12]

Marguerit, E. et al. Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor. Appl Genet. 118, 1261-1278 (2009).

[13]

Moreira, F. M. et al. Genetic linkage maps of two interspecific grape crosses (Vitis spp.) used to localize quantitative trait loci for downy mildew resistance. Tree Genet. Genomes 7, 153-167 (2011).

[14]

Blasi, P. et al. Construction of a reference linkage map of Vitis amurensis and genetic mapping of Rpv8, a locus conferring resistance to grapevine downy mildew. Theor. Appl. Genet. 123, 43-53 (2011).

[15]

Schwander, F. et al. Rpv10: a new locus from the Asian Vitis gene pool for pyramiding downy mildew resistance loci in grapevine. Theor. Appl. Genet. 124, 163-176 (2012).

[16]

Fu, P. N. et al. Identifying Plasmopara viticola resistance Loci in grapevine (Vitis amurensis) via genotyping-by-sequencing-based QTL mapping. Plant Physiol. Bioch. 154, 75-84 (2020).

[17]

Sargolzaei, M. et al. Rpv29, Rpv30 and Rpv31: Three Novel Genomic Loci Associated With Resistance to Plasmopara viticola in Vitis vinifera. Front. Plant Sci. 11, 562432 (2020).

[18]

Feechan, A. et al. Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. Plant J. 76, 661-674 (2013).

[19]

Foria, S. et al. Gene duplication and transposition of mobile elements drive evolution of the Rpv3 resistance locus in grapevine. Plant J. 101, 529-542 (2020).

[20]

Polesani, M. et al. General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genomics 11, 117-132 (2010).

[21]

Li, X. L. et al. Comparative transcriptome analysis reveals defense-related genes and pathways against downy mildew in Vitis amurensis grapevine. Plant Physiol. Bioch. 95, 1-14 (2015).

[22]

Fröbel, S., Dudenhöffer, J., Töpfer, R. & Zyprian, E. Transcriptome analysis of early downy mildew (Plasmopara viticola) defense in grapevines carrying the Asian resistance locus Rpv10. Euphytica 215, 28 (2019).

[23]

Eisenmann, B. et al. Rpv3-1 mediated resistance to grapevine downy mildew is associated with specific host transcriptional responses and the accumulation of stilbenes. BMC Plant Biol. 19, 343 (2019).

[24]

Chitarrini, G. et al. Two-omics data revealed commonalities and differences between Rpv12- and Rpv3-mediated resistance in grapevine. Sci. Rep. 10, 12193 (2020).

[25]

Shimizu, T., Kono, A. & Suzaki, K. Transcriptional analysis of defense-related genes induced by infection with the causal agent of downy mildew, Plasmopara viticola, in grapevine cultivar Shine Muscat. J. Gen. Plant Pathol. 85, 182-188 (2019).

[26]

Liu, R. Q. et al. Transcriptomic analysis of Chinese wild Vitis pseudoreticulata in response to Plasmopara viticola. Protoplasma 256, 1409-1424 (2019).

[27]

Kortekamp, A. & Zyprian, E. Leaf hairs as a basic protective barrier against downy mildew of grape. J. Phytopathol. 147, 453-459 (1999).

[28]

Wang, C. X., Wu, J., Zhang, Y. L. & Lu, J. Muscadinia rotundifolia ‘Noble’ defense response to Plasmopara viticola inoculation by inducing phytohormone-mediated stilbene accumulation. Protoplasma 255, 95-107 (2018).

[29]

Vezzulli, S. et al. The Rpv3-3 haplotype and stilbenoid induction mediate downy mildew resistance in a grapevine interspecific population. Front. Plant Sci. 25, 2078-2079 (2019).

[30]

Cesari, S. Multiple strategies for pathogen perception by plant immune receptors. N. Phytol. 219, 17-24 (2018).

[31]

Brutus, A., Sicilia, F., Macone, A., Cervone, F. & De Lorenzo, G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl Acad. Sci. USA 107, 9452-9457 (2010).

[32]

Zhang, Y. L. & Li, X. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50, 29-36 (2019).

[33]

Yan, C. & Xie, D. X. Jasmonate in plant defence: sentinel or double agent? Plant Biotechnol. J. 13, 1233-1240 (2015).

[34]

Anver, S. & Tsuda, K. in Ethylene in Plants. (ed. Wen, C. K.) (Springer, Dordrecht, 2015).

[35]

Naseem, M., Srivastava, M., Tehseen, M. & Ahmed, N. Auxin crosstalk to plant immune networks: a plant-pathogen interaction perspective. Curr. Protein Pept. SC 16, 389-394 (2015).

[36]

Zhang, Y. X. et al. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl Acad. Sci. USA 107, 18220-18225 (2010).

[37]

Yang, D. L., Yang, Y. & He, Z. H. Roles of plant hormones and their interplay in rice immunity. Mol. Plant. 6, 675-685 (2013).

[38]

Zaynab, M. et al. Role of secondary metabolites in plant defense against pathogens. Microb. Pathogenesis 124, 198-202 (2018).

[39]

Piasecka, A., Jedrzejczak-Rey, N. & Bednarek, P. Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. N. Phytol. 206, 948-964 (2015).

[40]

Huysmans, M., Lema, A. S., Coll, N. S. & Nowack, M. K. Dying two deaths - programmed cell death regulation in development and disease. Curr. Opin. Plant Biol. 35, 37-44 (2016).

[41]

Balint-Kurti, P. The plant hypersensitive response: concepts, control and consequences. Mol. Plant Pathol. 20, 1163-1178 (2019).

[42]

Thomma, B. P., Nürnberger, T. & Joosten, M. H. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4-15 (2011).

[43]

Ngou, B. P. M., Ahn, H. K., Ding, P. & Jones, J. D. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110-115 (2021).

[44]

Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105-109 (2021).

[45]

Adachi, H. & Tsuda, K. Convergence of cell-surface and intracellular immune receptor signalling. N. Phytol. 221, 1676-1678 (2019).

[46]

Adachi, H., Kamoun, S. & Maqbool, A. A resistosome-activated ‘death switch’. Nat. Plants 5, 457-458 (2019).

[47]

Tsuda, K. & Somssich, I. E. Transcriptional networks in plant immunity. N. Phytol. 206, 932-947 (2015).

[48]

Glazebrook, J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227 (2005).

[49]

Thaler, J. S., Owen, B. & Higgins, V. J. The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol. 135, 530-538 (2004).

[50]

Lemarie, S. et al. Both the jasmonic acid and the salicylic acid pathways contribute to resistance to the biotrophic clubroot agent Plasmodiophora brassicae in Arabidopsis. Plant Cell Physiol. 56, 2158-2168 (2015).

[51]

Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J. M. & Mauch-Mani, B. β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol. Plant Microbe Interact. 18, 819-829 (2005).

[52]

Ali, K. et al. Alterations in grapevine leaf metabolism upon inoculation with Plasmopara viticola in different time-points. Plant Sci. 191, 100-107 (2012).

[53]

Marchive, C. et al. Over-Expression of VvWRKY1 in grapevines induces expression of jasmonic acid pathway-related genes and confers higher tolerance to the downy mildew. PLoS ONE 8, e54185 (2013).

[54]

Gauthier, A. et al. The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine’s induced resistance against Plasmopara viticola. PLoS ONE 9, e88145 (2014).

[55]

Figueiredo, A., Monteiro, F. & Sebastiana, M. First clues on a jasmonic acid role in grapevine resistance against the biotrophic fungus Plasmopara viticola. Eur. J. Plant Pathol. 142, 645-652 (2015).

[56]

Guerreiro, A., Figueiredo, J., Sousa, S. M. & Figueiredo, A. Linking Jasmonic Acid to Grapevine Resistance against the Biotrophic Oomycete Plasmopara viticola. Front. Plant Sci. 7, 565 (2016).

[57]

Wagner, S. et al. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Micr 14, 619-630 (2013).

[58]

van Loon, L. C., Rep, M. & Pieterse, C. M. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162 (2006).

[59]

Gantner, J., Ordon, J., Kretschmer, C., Guerois, R. & Stuttmann, J. An EDS1-SAG101 complex is essential for TNL-mediated immunity in Nicotiana benthamiana. Plant Cell 31, 2456-2474 (2019).

[60]

Makandar, R. et al. The combined action of ENHANCED DISEASE SUSCEPTIBILITY1, PHYTOALEXIN DEFICIENT4 and SENESCENCE-ASSOCIATED101 promotes salicylic acid-mediated defenses to limit Fusarium graminearum infection in Arabidopsis thaliana. Mol. Plant Microbe Interact. 28, 943-953 (2015).

[61]

Pichersky, E. & Raguso, R. A. Why do plants produce so many terpenoid compounds? N. Phytol. 220, 692-702 (2018).

[62]

Schnee, S., Viret, O. & Gindro, K. Role of stilbenes in the resistance of grapevine to powdery mildew. Physiol. Mol. Plant Pathol. 72, 128-133 (2008).

[63]

Jiao, Y. T., Xu, W. R., Duan, D., Wang, Y. J. & Nick, P. A stilbene synthase allele from a Chinese wild grapevine confers resistance to powdery mildew by recruiting salicylic acid signalling for efficient defence. J. Exp. Bot. 67, 5841-5856 (2016).

[64]

Xu, W. R. et al. VpSTS29/STS2 enhances fungal tolerance in grapevine through a positive feedback loop. Plant Cell Environ. 42, 2979-2998 (2019).

[65]

Vannozzi, A., Dry, I. B., Fasoli, M., Zenoni, S. & Lucchin, M. Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol. 12, 130 (2012).

[66]

Höll, J. et al. The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 25, 4135-4149 (2013).

[67]

Vannozzi, A. et al. Combinatorial regulation of stilbene synthase genes by WRKY and MYB transcription factors in grapevine (Vitis vinifera L.). Plant Cell Physiol. 59, 1043-1059 (2018).

[68]

Luo, Y. et al. The transcription factor MYB15 is essential for basal immunity (PTI) in Chinese wild grape. Planta 249, 1889-1902 (2019).

[69]

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Method. 57, 289-300 (1995).

[70]

Young, M. D., Wakefield, M. J., Smyth, G. K. & Oshlack, A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 11, R14 (2010).

[71]

Xie, C. et al. a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, 316-322 (2011).

[72]

Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinforma. 9, 559 (2008).

[73]

Shannon, P. & Horvath, S. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).

[74]

McLeay, R. & Bailey, T. L. Motif enrichment analysis: a unified framework and an evaluation on ChIP data. BMC Bioinforma. 11, 165 (2010).

[75]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408 (2001).

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