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      A histone deacetylase inhibitor enhances rice immunity by derepressing the expression of defense-related genes

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          Abstract

          Histone deacetylase (HDAC) inhibitors (HDACis) have been widely used in plants to investigate the role of histone acetylation, particularly the function of HDACs, in the regulation of development and stress response. However, how histone acetylation is involved in rice ( Oryza sativa L.) disease resistance has hardly been studied. In this paper, four HDACis including Sodium butyrate (NaBT), Suberoylanilide Hydroxamic Acid (SAHA), LBH-589 and Trichostatin A (TSA) were used to treat rice seedlings at different concentrations before inoculation of Magnaporthe oryzae. We found that only 10mM NaBT treatment can significantly enhanced rice blast resistance. However, treatment of the four HDACis all increased global histone acetylation but at different sites, suggesting that the inhibition selectivity of these HDACis is different. Notably, the global H3K9ac level was dramatically elevated after both NaBT and LBH589 treatment although LBH589 could not enhance rice blast resistance. This indicates that the HDACs they inhibit target different genes. In accordance with the phenotype, transcriptomic analysis showed that many defense-related genes were up-regulated by NaBT treatment. Up-regulation of the four genes bsr-d1, PR10B, OsNAC4, OsKS4 were confirmed by RT-qPCR. ChIP-qPCR results revealed that H3K9ac level on these genes was increased after NaBT treatment, suggesting that these defense-related genes were repressed by HDACs. In addition, by promoter motif analysis of the genes that induced by both NaBT treatment and rice blast infection, we found that the motifs bound by ERF and AHL transcription factors (TFs) were the most abundant, which demonstrates that ERF and AHL proteins may act as the candidate TFs that recruit HDACs to defense-related genes to repress their expression when plants are not infected by rice blast.

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          Most cited references44

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          Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes.

          Sequence similarity and profile searching tools were used to analyze the genome sequences of Arabidopsis thaliana, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Caenorhabditis elegans and Drosophila melanogaster for genes encoding three families of histone deacetylase (HDAC) proteins and three families of histone acetyltransferase (HAT) proteins. Plants, animals and fungi were found to have a single member of each of three subfamilies of the GNAT family of HATs, suggesting conservation of these functions. However, major differences were found with respect to sizes of gene families and multi-domain protein structures within other families of HATs and HDACs, indicating substantial evolutionary diversification. Phylogenetic analysis identified a new class of HDACs within the RPD3/HDA1 family that is represented only in plants and animals. A similar analysis of the plant-specific HD2 family of HDACs suggests a duplication event early in dicot evolution, followed by further diversification in the lineage leading to Arabidopsis. Of three major classes of SIR2-type HDACs that are found in animals, fungi have representatives only in one class, whereas plants have representatives only in the other two. Plants possess five CREB-binding protein (CBP)-type HATs compared with one to two in animals and none in fungi. Domain and phylogenetic analyses of the CBP family proteins showed that this family has evolved three distinct types of CBPs in plants. The domain architecture of CBP and TAF(II)250 families of HATs show significant differences between plants and animals, most notably with respect to bromodomain occurrence and their number. Bromodomain-containing proteins in Arabidopsis differ strikingly from animal bromodomain proteins with respect to the numbers of bromodomains and the other types of domains that are present. The substantial diversification of HATs and HDACs that has occurred since the divergence of plants, animals and fungi suggests a surprising degree of evolutionary plasticity and functional diversification in these core chromatin components.
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            A Natural Allele of a Transcription Factor in Rice Confers Broad-Spectrum Blast Resistance.

            Rice feeds half the world's population, and rice blast is often a destructive disease that results in significant crop loss. Non-race-specific resistance has been more effective in controlling crop diseases than race-specific resistance because of its broad spectrum and durability. Through a genome-wide association study, we report the identification of a natural allele of a C2H2-type transcription factor in rice that confers non-race-specific resistance to blast. A survey of 3,000 sequenced rice genomes reveals that this allele exists in 10% of rice, suggesting that this favorable trait has been selected through breeding. This allele causes a single nucleotide change in the promoter of the bsr-d1 gene, which results in reduced expression of the gene through the binding of the repressive MYB transcription factor and, consequently, an inhibition of H2O2 degradation and enhanced disease resistance. Our discovery highlights this novel allele as a strategy for breeding durable resistance in rice.
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              Against the grain: safeguarding rice from rice blast disease.

              Rice is the staple diet of more than three billion people. Yields must double over the next 40 years if we are to sustain the nutritional needs of the ever-expanding global population. Between 10% and 30% of the annual rice harvest is lost due to infection by the rice blast fungus Magnaporthe oryzae. Evaluation of genetic and virulence diversity of blast populations with diagnostic markers will aid disease management. We review the M. oryzae species-specific and cultivar-specific avirulence determinants and evaluate efforts towards generating durable and broad-spectrum resistance in single resistant cultivars or mixtures. We consider modern usage of fungicides and plant defence activators, assess the usefulness of biological control and categorize current approaches towards blast-tolerant genetically modified rice.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                02 November 2022
                2022
                : 13
                : 1041095
                Affiliations
                [1] 1 Hubei Engineering Research Center for Specialty Flowers Biological Breeding/College of Bioengineering, Jingchu University of Technology , Jingmen, China
                [2] 2 Center for Science Popularization Jingmen, Science and Technology Museum , Jingmen, China
                [3] 3 State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan/Ministry of Education Key Laboratory of Agricultural Biodiversity for Plant Disease Management, Yunnan Agricultural University , Kunming, China
                [4] 4 Department of Biochemistry and Molecular Biology, College of Life Sciences, Nanjing Agricultural University , Nanjing, China
                [5] 5 Key Laboratory of Three Gorges Regional Plant Genetics and Germplasm Enhancement, Biotechnology Research Center, China Three Gorges University , Yichang, China
                Author notes

                Edited by: Yi Han, Anhui Agricultural University, China

                Reviewed by: Fujun Qin, Zhengzhou University, China; Xiaoyun Liu, Jianghan University, China

                †These authors have contributed equally to this work

                This article was submitted to Plant Bioinformatics, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2022.1041095
                9667192
                28f0dd54-80e6-4103-909e-50b41d2ce113
                Copyright © 2022 Xu, Miao, Cai, Yi, Tian, Wang, Ma, Luo, Tan and Hu

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 10 September 2022
                : 13 October 2022
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 44, Pages: 12, Words: 5939
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                hdac inhibitors,rice blast,histone acetylation,defense-related genes,rice
                Plant science & Botany
                hdac inhibitors, rice blast, histone acetylation, defense-related genes, rice

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