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A transcriptional regulatory network of Rsv3-mediated extreme resistance against Soybean mosaic virus.

ABSTRACT: 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.

SUBMITTER: DeMers LC

PROVIDER: S-EPMC7173922 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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A transcriptional regulatory network of Rsv3-mediated extreme resistance against Soybean mosaic virus.

DeMers Lindsay C LC Redekar Neelam R NR Kachroo Aardra A Tolin Sue A SA Li Song S Saghai Maroof M A MA

PloS one 20200421 4

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 unex ...[more]

PMID: 32315334

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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:BackgroundSoybean mosaic virus (SMV) is the most prevalent viral disease in many soybean production areas. Due to a large number of SMV resistant loci and alleles, SMV strains and the rapid evolution in avirulence/effector genes, traditional breeding for SMV resistance is complex. Genetic engineering is an effective alternative method for improving SMV resistance in soybean. Potassium (K+) is the most abundant inorganic solute in plant cells, and is involved in plant responses to abiotic and biotic stresses. Studies have shown that altering the level of K+ status can reduce the spread of the viral diseases. Thus K+ transporters are putative candidates to target for soybean virus resistance.ResultsThe addition of K+ fertilizer significantly reduced SMV incidence. Analysis of K+ channel gene expression indicated that GmAKT2, the ortholog of Arabidopsis K+ weak channel encoding gene AKT2, was significantly induced by SMV inoculation in the SMV highly-resistant genotype Rsmv1, but not in the susceptible genotype Ssmv1. Transgenic soybean plants overexpressing GmAKT2 were produced and verified by Southern blot and RT-PCR analysis. Analysis of K+ concentrations on different leaves of both the transgenic and the wildtype (Williams 82) plants revealed that overexpression of GmAKT2 significantly increased K+ concentrations in young leaves of plants. In contrast, K+ concentrations in the old leaves of the GmAKT2-Oe plants were significantly lower than those in WT plants. These results indicated that GmAKT2 acted as a K+ transporter and affected the distribution of K+ in soybean plants. Starting from 14 days after inoculation (DAI) of SMV G7, severe mosaic symptoms were observed on the WT leaves. In contrast, the GmAKT2-Oe plants showed no symptom of SMV infection. At 14 and 28 DAI, the amount of SMV RNA in WT plants increased 200- and 260- fold relative to GmAKT2-Oe plants at each time point. Thus, SMV development was significantly retarded in GmAKT2-overexpressing transgenic soybean plants.ConclusionsOverexpression of GmAKT2 significantly enhanced SMV resistance in transgenic soybean. Thus, alteration of K+ transporter expression is a novel molecular approach for enhancing SMV resistance in soybean.

Dataset Information

A transcriptional regulatory network of Rsv3-mediated extreme resistance against Soybean mosaic virus.

Publications

A transcriptional regulatory network of Rsv3-mediated extreme resistance against Soybean mosaic virus.

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