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Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus.

ABSTRACT: Extreme resistance (ER) is a type of R-gene-mediated resistance that rapidly induces a symptomless resistance phenotype, which is different from the phenotypical R-resistance manifested by the programmed cell death, accumulation of reactive oxygen species, and hypersensitive response. The Rsv3 gene in soybean cultivar L29 is responsible for ER against the avirulent strain G5H of soybean mosaic virus (SMV), but is ineffective against the virulent strain G7H. Rsv3-mediated ER is achieved through the rapid accumulation of callose, which arrests SMV-G5H at the point of infection. Callose accumulation, however, may not be the lone mechanism of this ER. Analyses of RNA-seq data obtained from infected soybean plants revealed a rapid induction of the abscisic acid pathway at 8 h post infection (hpi) in response to G5H but not to G7H, which resulted in the down-regulation of transcripts encoding ?-1,3 glucanases that degrade callose in G5H-infected but not G7H-infected plants. In addition, parts of the autophagy and the small interfering (si) RNA pathways were temporally up-regulated at 24 hpi in response to G5H but not in response to G7H. The jasmonic acid (JA) pathway and many WRKY factors were clearly up-regulated only in G7H-infected plants. These results suggest that ER against SMV-G5H is achieved through the quick and temporary induction of ABA, autophagy, and the siRNA pathways, which rapidly eliminate G5H. The results also suggest that suppression of the JA pathway in the case of G5H is important for the Rsv3-mediated ER.

SUBMITTER: Alazem M

PROVIDER: S-EPMC6267276 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus.

Alazem Mazen M Tseng Kuan-Chieh KC Chang Wen-Chi WC Seo Jang-Kyun JK Kim Kook-Hyung KH

Viruses 20181024 11

Extreme resistance (ER) is a type of R-gene-mediated resistance that rapidly induces a symptomless resistance phenotype, which is different from the phenotypical R-resistance manifested by the programmed cell death, accumulation of reactive oxygen species, and hypersensitive response. The Rsv3 gene in soybean cultivar L29 is responsible for ER against the avirulent strain G5H of soybean mosaic virus (SMV), but is ineffective against the virulent strain G7H. Rsv3-mediated ER ...[more]

PMID: 30355968

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Project description:Resistance (R) genes are very effective for disease control in plants. Current research shows that R genes predominantly function by inducing a hypersensitive reaction (HR), which results in localized cell death thought to restrict pathogen spread. Some R genes elicit a more atypical response where resistance is not associated with HR or the associated gene expression changes, termed extreme resistance (ER). The molecular regulatory mechanism underlying ER is largely unexplored. One of the few known, naturally occurring, instances of ER is resistance derived from the soybean Rsv3 gene, which confers resistance against the most virulent strains of soybean mosaic virus (SMV). To discern the regulatory mechanism underlying the Rsv3-mediated ER reaction, we generated a gene regulatory network using transcriptomic data from a time course comparison of SMV-G7-infected resistant (L29, Rsv3-genotype) and susceptible (Williams82, rsv3-genotype) soybean cultivars. We identified putative interactions between transcription factors (TFs) regulating gene expression in hormone regulatory pathways, such as abscisic acid (ABA) and jasmonic acid (JA). This is consistent with the demonstrated involvement of these pathways in Rsv3-mediated resistance. We found significant enrichment for the G-box motif (“CACGTG”) among genes implicated in ABA- and JA-related activities. This motif is specifically recognized by MYC2, which is a master regulator of ABA and JA signaling. Our network identified a MYC2 TF encoded by Glyma.07G051500 as a putative transcriptional regulator whose expression was significantly down-regulated in L29. This correlated with the down-regulation of expression of genes involved in ABA and JA processes. Our results suggest an important function for Glyma.07G051500 in ABA and JA derived defense signaling. Additionally, our regulatory network found other putative TFs with differential expression, such as MYBs and ERFs, which may also be involved in regulating ABA and JA signaling for defense. The regulatory network presented here offers new insights into the regulation of the molecular defense mechanism underlying Rsv3-mediated ER against SMV.

Project description:Resistance genes are an effective means for disease control in plants. They predominantly function by inducing a hypersensitive reaction, which results in localized cell death restricting pathogen spread. Some resistance genes elicit an atypical response, termed extreme resistance, where resistance is not associated with a hypersensitive reaction and its standard defense responses. Unlike hypersensitive reaction, the molecular regulatory mechanism(s) underlying extreme resistance is largely unexplored. One of the few known, naturally occurring, instances of extreme resistance is resistance derived from the soybean Rsv3 gene, which confers resistance against the most virulent Soybean mosaic virus strains. To discern the regulatory mechanism underlying Rsv3-mediated extreme resistance, we generated a gene regulatory network using transcriptomic data from time course comparisons of Soybean mosaic virus-G7-inoculated resistant (L29, Rsv3-genotype) and susceptible (Williams82, rsv3-genotype) soybean cultivars. Our results show Rsv3 begins mounting a defense by 6 hpi via a complex phytohormone network, where abscisic acid, cytokinin, jasmonic acid, and salicylic acid pathways are suppressed. We identified putative regulatory interactions between transcription factors and genes in phytohormone regulatory pathways, which is consistent with the demonstrated involvement of these pathways in Rsv3-mediated resistance. One such transcription factor identified as a putative transcriptional regulator was MYC2 encoded by Glyma.07G051500. Known as a master regulator of abscisic acid and jasmonic acid signaling, MYC2 specifically recognizes the G-box motif ("CACGTG"), which was significantly enriched in our data among differentially expressed genes implicated in abscisic acid- and jasmonic acid-related activities. This suggests an important role for Glyma.07G051500 in abscisic acid- and jasmonic acid-derived defense signaling in Rsv3. Resultantly, the findings from our network offer insights into genes and biological pathways underlying the molecular defense mechanism of Rsv3-mediated extreme resistance against Soybean mosaic virus. The computational pipeline used to reconstruct the gene regulatory network in this study is freely available at https://github.com/LiLabAtVT/rsv3-network.

Dataset Information

Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus.

Publications

Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus.

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