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      Chilli veinal mottle virus HCPro interacts with catalase to facilitate virus infection in Nicotiana tabacum

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          Abstract

          This study uncovered a novel role for HCPro in ChiVMV pathogenicity by interacting with catalases and inhibiting their activities to counter plant immunity.

          Abstract

          Plant symptoms are derived from specific interactions between virus and host components. However, little is known about viral or host factors that participate in the establishment of systemic necrosis. Here, we showed that helper component proteinase (HCPro), encoded by Chilli veinal mottle virus (ChiVMV), could directly interact with catalase 1 (CAT1) and catalase 3 (CAT3) in the cytoplasm of tobacco ( Nicotiana tabacum) plants to facilitate viral infection. In vitro, the activities of CAT1 and CAT3 were inhibited by the interaction between HCPro and CATs. The C-terminus of HCPro was essential for their interaction and was also required for the decrease of enzyme activities. Interestingly, the mRNA and protein level of CATs were up-regulated in tobacco plants in response to ChiVMV infection. Nicotiana tabacum plants with HCPro overexpression or CAT1 knockout were more susceptible to ChiVMV infection, which was similar to the case of H 2O 2-pre-treated plants, and the overexpression of CAT1 inhibited ChiVMV accumulation. Also, neither CAT1 nor CAT3 could affect the RNA silencing suppression (RSS) activity of HCPro. Our results showed that the interaction between HCPro and CATs promoted the development of plant systemic necrosis, revealing a novel role for HCPro in virus infection and pathogenicity.

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          Most cited references39

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          RNA silencing in plants.

          There are at least three RNA silencing pathways for silencing specific genes in plants. In these pathways, silencing signals can be amplified and transmitted between cells, and may even be self-regulated by feedback mechanisms. Diverse biological roles of these pathways have been established, including defence against viruses, regulation of gene expression and the condensation of chromatin into heterochromatin. We are now in a good position to investigate the full extent of this functional diversity in genetic and epigenetic mechanisms of genome control.
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            Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.

            Cell expansion is a central process in plant morphogenesis, and the elongation of roots and root hairs is essential for uptake of minerals and water from the soil. Ca2+ influx from the extracellular store is required for (and sets the rates of) cell elongation in roots. Arabidopsis thaliana rhd2 mutants are defective in Ca2+ uptake and consequently cell expansion is compromised--rhd2 mutants have short root hairs and stunted roots. To determine the regulation of Ca2+ acquisition in growing root cells we show here that RHD2 is an NADPH oxidase, a protein that transfers electrons from NADPH to an electron acceptor leading to the formation of reactive oxygen species (ROS). We show that ROS accumulate in growing wild-type (WT) root hairs but their levels are markedly decreased in rhd2 mutants. Blocking the activity of the NADPH oxidase with diphenylene iodonium (DPI) inhibits ROS formation and phenocopies Rhd2-. Treatment of rhd2 roots with ROS partly suppresses the mutant phenotype and stimulates the activity of plasma membrane hyperpolarization-activated Ca2+ channels, the predominant root Ca2+ acquisition system. This indicates that NADPH oxidases control development by making ROS that regulate plant cell expansion through the activation of Ca2+ channels.
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              Diversity of structures and properties among catalases.

              More than 300 catalase sequences are now available, divided among monofunctional catalases (> 225), bifunctional catalase-peroxidases (> 50) and manganese-containing catalases (> 25). When combined with the recent appearance of crystal structures from at least two representatives from each of these groups (nine from the monofunctional catalases), valuable insights into the catalatic reaction mechanism in its various forms and into catalase evolution have been gained. The structures have revealed an unusually large number of modifications unique to catalases, a result of interacting with reactive oxygen species. Biochemical and physiological characterization of catalases from many different organisms has revealed a surprisingly wide range of catalatic efficiencies, despite similar sequences. Catalase gene expression in micro-organisms generally is controlled either by sensors of reactive oxygen species or by growth phase regulons, although the detailed mechanisms vary considerably.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                J Exp Bot
                J. Exp. Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                19 September 2020
                28 June 2020
                28 June 2020
                : 71
                : 18
                : 5656-5668
                Affiliations
                [1 ] Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University , Chengdu, Sichuan, PR China
                [2 ] Cardiff University , UK
                Author notes
                Correspondence: xidh@ 123456scu.edu.cn
                Author information
                http://orcid.org/0000-0002-1314-1262
                Article
                eraa304
                10.1093/jxb/eraa304
                7501817
                32594157
                4580d72f-7fac-41e0-bbe4-ff8cd6ad67a6
                © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 December 2019
                : 22 May 2020
                : 19 June 2020
                : 09 August 2020
                Page count
                Pages: 13
                Funding
                Funded by: National Natural Science Foundation of China, DOI 10.13039/501100001809;
                Award ID: 31772131
                Award ID: 31270290
                Award ID: 31171835
                Funded by: Applied Basic Research Fund of Sichuan Province;
                Award ID: 2019YJ0135
                Funded by: Fundamental Research Funds for the Central Universities, DOI 10.13039/501100012226;
                Award ID: SCU2019D013
                Categories
                Research Papers
                Plant—Environment Interactions
                AcademicSubjects/SCI01210

                Plant science & Botany
                catalase,chilli veinal mottle virus,hcpro,nicotiana tabacum,suppressor of rna silencing,systemic necrosis

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