Dataset Information

The wheat LLM-domain-containing transcription factor TaGATA1 positively modulates host immune response to Rhizoctonia cerealis.

ABSTRACT: Wheat (Triticum aestivum) is essential for global food security. Rhizoctonia cerealis is the causal pathogen of sharp eyespot, an important disease of wheat. GATA proteins in model plants have been implicated in growth and development; however, little is known about their roles in immunity. Here, we report a defence role for a wheat LLM-domain-containing B-GATA transcription factor, TaGATA1, against R. cerealis infection and explore the underlying mechanism. Through transcriptomic analysis, TaGATA1 was identified to be more highly expressed in resistant wheat genotypes than in susceptible wheat genotypes. TaGATA1 was located on chromosome 3B and had two homoeologous genes on chromosomes 3A and 3D. TaGATA1 was found to be localized in the nucleus, possessed transcriptional activation activity, and bound to GATA-core cis-elements. TaGATA1 overexpression significantly enhanced resistance of transgenic wheat to R. cerealis, whereas silencing of TaGATA1 suppressed the resistance. Quantitative reverse transcription-PCR and ChIP-qPCR results indicated that TaGATA1 directly bound to and activated certain defence genes in host immune response to R. cerealis. Collectively, TaGATA1 positively regulates immune responses to R. cerealis through activating expression of defence genes in wheat. This study reveals a new function of plant GATAs in immunity and provides a candidate gene for improving crop resistance to R. cerealis.

SUBMITTER: Liu X

PROVIDER: S-EPMC6913698 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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The wheat LLM-domain-containing transcription factor TaGATA1 positively modulates host immune response to Rhizoctonia cerealis.

Liu Xin X Zhu Xiuliang X Wei Xuening X Lu Chungui C Shen Fangdi F Zhang Xuewen X Zhang Zengyan Z

Journal of experimental botany 20200101 1

Wheat (Triticum aestivum) is essential for global food security. Rhizoctonia cerealis is the causal pathogen of sharp eyespot, an important disease of wheat. GATA proteins in model plants have been implicated in growth and development; however, little is known about their roles in immunity. Here, we report a defence role for a wheat LLM-domain-containing B-GATA transcription factor, TaGATA1, against R. cerealis infection and explore the underlying mechanism. Through transcriptomic analysis, TaGA ...[more]

PMID: 31536614

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Project description:Eukaryotic type 2A protein phosphatases (protein phosphatase 2A, PP2A) consist of a scaffold subunit A, a regulatory subunit B, and a catalytic subunit C. Little is known about the roles of PP2Ac proteins that are involved in plant responses to necrotrophic fungal pathogens. Sharp eyespot, caused by the necrotrophic fungus Rhizoctonia cerealis, is a destructive disease of wheat (Triticum aestivum), an important staple food crop. Here, we isolated TaPP2Ac-4D from wheat, which encodes a catalytic subunit of the heterotrimeric PP2A, and characterized its properties and role in plant defense response to R. cerealis. Based on the sequence alignment of TaPP2Ac-4D with the draft sequences of wheat chromosomes from the International Wheat Genome Sequencing Consortium (IWGSC), it was found that TaPP2Ac-4D gene is located on the long arm of the wheat chromosome 4D and has two homologs assigned on wheat chromosomes 4A and 4B. Sequence and phylogenetic tree analyses revealed that the TaPP2Ac protein is a typical member of the PP2Ac family and belongs to the subfamily II. TaPP2Ac-4B and TaPP2Ac-4D displayed higher transcriptional levels in the R. cerealis-susceptible wheat cultivar Wenmai 6 than those seen in the resistant wheat line CI12633. The transcriptional levels of TaPP2Ac-4B and TaPP2Ac-4D were significantly elevated in wheat R. cerealis after infection and upon H2O2 treatment. Virus-induced gene silencing results revealed that the transcriptional knockdown of TaPP2Ac-4D and TaPP2Ac-4B significantly increased wheat resistance to R. cerealis infection. Meanwhile, the transcriptional levels of certain pathogenesis-related (PR) and reactive oxygen species (ROS)-scavenging enzyme encoding genes were increased in TaPP2Ac-silenced wheat plants. These results suggest that TaPP2Ac-4B and TaPP2Ac-4D negatively regulate defense response to R. cerealis infection possibly through modulation of the expression of certain PR and ROS-scavenging enzyme genes in wheat. This study reveals a novel function of the plant PP2Ac genes in plant immune responses.

Project description:Wheat sharp eyespot caused by Rhizoctonia cerealis is primarily a severe threat to worldwide wheat production. Currently, there are no resistant wheat cultivars, and the use of fungicides is the primary method for controlling this disease. Elucidating the mechanisms of R. cerealis pathogenicity can accelerate the pace of the control of this disease. Long intergenic noncoding RNAs (lincRNAs) that function in plant-pathogen interactions might provide a new perspective. We systematically analyzed lincRNAs and identified a total of 1,319 lincRNAs in R. cerealis. We found that lincRNAs are involved in various biological processes, as shown by differential expression analysis and weighted correlation network analysis (WGCNA). Next, one of nine hub lincRNAs in the blue module that was related to infection and growth processes, MSTRG.4380.1, was verified to reduce R. cerealis virulence on wheat by a host-induced gene silencing (HIGS) assay. Following that, RNA sequencing (RNA-Seq) analysis revealed that the significantly downregulated genes in the MSTRG.4380.1 knockdown lines were associated mainly with infection-related processes, including hydrolase, transmembrane transporter, and energy metabolism activities. Additionally, 23 novel microRNAs (miRNAs) were discovered during small RNA (sRNA) sequencing (sRNA-Seq) analysis of MSTRG.4380.1 knockdown, and target prediction of miRNAs suggested that MSTRG.4380.1 does not act as a competitive endogenous RNA (ceRNA). This study performed the first genome-wide identification of R. cerealis lincRNAs and miRNAs. It confirmed the involvement of a lincRNA in the infection process, providing new insights into the mechanism of R. cerealis infection and offering a new approach for protecting wheat from R. cerealis. IMPORTANCE Rhizoctonia cerealis, the primary causal agent of wheat sharp eyespot, has caused significant losses in worldwide wheat production. Since no resistant wheat cultivars exist, chemical control is the primary method. However, this approach is environmentally unfriendly and costly. RNA interference (RNAi)-mediated pathogenicity gene silencing has been proven to reduce the growth of Rhizoctonia and provides a new perspective for disease control. Recent studies have shown that lincRNAs are involved in various biological processes across species, such as biotic and abiotic stresses. Therefore, verifying the function of lincRNAs in R. cerealis is beneficial for understanding the infection mechanism. In this study, we reveal that lincRNAs could contribute to the virulence of R. cerealis, which provides new insights into controlling this pathogen.

Project description:Rhizoctonia cerealis is the pathogen of wheat sharp eyespot, which occurs throughout temperate wheat-growing regions of the world. In this project, the genomes of viruses from four strains of R. cerealis were analyzed based on Illumina high-throughput transcriptome sequencing (RNA-Seq) data. After filtering out reads that mapped to the fungal genome, viral genomes were assembled. In total, 131 virus-like sequences containing complete open reading frames (ORFs), belonging to 117 viruses, were obtained. Based on phylogenetic analysis, some of them were identified as novel members of the families Curvulaviridae, Endornaviridae, Hypoviridae, Mitoviridae, Mymonaviridae, and Phenuiviridae, while others were unclassified viruses. Most of these viruses from R. cerealis were significantly different from the viruses already reported. We propose the establishment of a new family, Rhizoctobunyaviridae, and two new genera, Rhizoctobunyavirus and Iotahypovirus. We further clarified the distribution and coinfection of these viruses in the four strains. Surprisingly, 39 viral genomes of up to 12 genera were found in strain R1084. Strain R0942, containing the fewest viruses, also contained 21 viral genomes belonging to 10 genera. Based on the RNA-Seq data, we estimated the accumulation level of some viruses in host cells and found that the mitoviruses in R. cerealis generally have very high accumulation. In conclusion, in the culturable phytopathogenic fungus R. cerealis, we discovered a considerable diversity of mycoviruses and a series of novel viruses. This study expands our understanding of the mycoviral diversity in R. cerealis and provides a rich resource for the further use of mycoviruses to control wheat sharp eyespot. IMPORTANCE Rhizoctonia cerealis is a binucleate fungus that is widely distributed worldwide and can cause sharp eyespot disease in cereal crops. In this study, 131 virus-like sequences belonging to 117 viruses were obtained based on analysis of high-throughput RNA-Seq data from four strains of R. cerealis. Many of these viruses were novel members of various virus families, while others were unclassified viruses. As a result, a new family named Rhizoctobunyaviridae and two new genera, Rhizoctobunyavirus and Iotahypovirus, were proposed. Moreover, the discovery of multiple viruses coinfecting a single host and the high accumulation levels of mitoviruses have shed light on the complex interactions between different viruses in a single host. In conclusion, a significant diversity of mycoviruses was discovered in the culturable phytopathogenic fungus R. cerealis. This study expands our understanding of mycoviral diversity, and provides a valuable resource for the further utilization of mycoviruses to control wheat diseases.

Dataset Information

The wheat LLM-domain-containing transcription factor TaGATA1 positively modulates host immune response to Rhizoctonia cerealis.

Publications

The wheat LLM-domain-containing transcription factor TaGATA1 positively modulates host immune response to Rhizoctonia cerealis.

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