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 β-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.

Soybean Resistance to Soybean Mosaic Virus

“…The molecular signaling involved in the Rsv3-mediated ER was elucidated using the Rsv3-harbouring L29 plants. Infection with G5H allows Rsv3 to recognize the CI protein, which induces several genes in the ABA pathway, including the negative regulator PP2C3a [18,100]. Expression of PP2C3a induces callous accumulation and thus restricts G5H movement at the infected points [100].…”

“…In addition, reduction in the expression of many genes in the jasmonic acid pathway and WRKY transcription factors were also observed following G5H infection on L29 plants. Interestingly, ABA can also induce resistance L29 plants against the G7H virulent strain by enhancing callous accumulation and increasing the expression of several genes involved in the antiviral RNA silencing pathway [18,19]. Future research addressing the localization of Rsv3, factors associated with Rsv3, and downstream defense signaling pathways would help us better understand the molecular mechanisms underlying Rsv3-mediated resistance.…”

“…Apart from individual genes involved in SMV-soybean interaction, the antiviral RNA silencing pathway has been also reported to be involved in soybean resistance to SMV [18,19,125]. The viral replication intermediate, i.e., double-stranded (ds) RNA, is sensed by RNase type III-like enzymes called Dicer-like (DCL) proteins, which cleave the dsRNA into primary short interfering (si) RNAs of 21-24 nucleotides (nt) in length [126].…”

“…Viral-derived siRNAs (vsiRNAs) are loaded into the RNA-induced silencing complex (RISC), where they guide argonaute proteins (AGO) to cleave the viral RNA genes upon perfect complementation between vsiRNA and viral genes [126,127]. In the Rsv3-cultivar L29, several genes in the antiviral RNA silencing pathway were induced in response to infection by the avirulent strain G5H but showed no change or even downregulation in response to infection by the virulent strain G7H [18]. This indicates that the antiviral RNA silencing pathway contributes to the ER against G5H.…”

“…Levels of other hormones such as cytokinins and brassinosteroids and expression levels of their related genes were mildly elevated in response to infection by SMV-G5H or SMV-G7H. Cytokinins and brassinosteroids have various functions in plant growth and development and also increase plant tolerance to infection by some viruses [16,18,132].…”