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      Osa‐miR398b boosts H 2O 2 production and rice blast disease‐resistance via multiple superoxide dismutases

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          Summary

          • mi RNAs contribute to plant resistance against pathogens. Previously, we found that the function of miR398b in immunity in rice differs from that in Arabidopsis. However, the underlying mechanisms are unclear.

          • In this study, we characterized the mutants of miR398b target genes and demonstrated that multiple superoxide dismutase genes contribute to miR398b‐regulated rice immunity against the blast fungus Magnaporthe oryzae.

          • Out of the four target genes of miR398b, mutations in Cu/Zn‐Superoxidase Dismutase1 ( CSD1 ), CSD2 and Os11g09780 ( Superoxide DismutaseX, SODX ) led to enhanced resistance to M. oryzae and increased hydrogen peroxide (H 2O 2) accumulation. By contrast, mutations in Copper Chaperone for Superoxide Dismutase ( CCSD ) resulted in enhanced susceptibility. Biochemical studies revealed that csd1, csd2 and sodx displayed altered expression of CSDs and other superoxide dismutase ( SOD) family members, leading to increased total SOD enzyme activity that positively contributed to higher H 2O 2 production. By contrast, the ccsd mutant showed CSD protein deletion, resulting in decreased CSD and total SOD enzyme activity.

          • Our results demonstrate the roles of different SODs in miR398b‐regulated resistance to rice blast disease, and uncover an integrative regulatory network in which miR398b boosts total SOD activity to upregulate H 2O 2 concentration and thereby improve disease resistance.

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          Most cited references 53

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          Superoxide radical and superoxide dismutases.

           I Fridovich (1995)
          O2- oxidizes the [4Fe-4S] clusters of dehydratases, such as aconitase, causing-inactivation and release of Fe(II), which may then reduce H2O2 to OH- +OH.. SODs inhibit such HO. production by scavengingO2-, but Cu, ZnSODs, by virtue of a nonspecific peroxidase activity, may peroxidize spin trapping agents and thus give the appearance of catalyzing OH. production from H2O2. There is a glycosylated, tetrameric Cu, ZnSOD in the extracellular space that binds to acidic glycosamino-glycans. It minimizes the reaction of O2- with NO. E. coli, and other gram negative microorganisms, contain a periplasmic Cu, ZnSOD that may serve to protect against extracellular O2-. Mn(III) complexes of multidentate macrocyclic nitrogenous ligands catalyze the dismutation of O2- and are being explored as potential pharmaceutical agents. SOD-null mutants have been prepared to reveal the biological effects of O2-. SodA, sodB E. coli exhibit dioxygen-dependent auxotrophies and enhanced mutagenesis, reflecting O2(-)-sensitive biosynthetic pathways and DNA damage. Yeast, lacking either Cu, ZnSOD or MnSOD, are oxygen intolerant, and the double mutant was hypermutable and defective in sporulation and exhibited requirements for methionine and lysine. A Cu, ZnSOD-null Drosophila exhibited a shortened lifespan.
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            Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance.

            MicroRNAs (miRNAs) are a class of regulatory RNAs of approximately 21 nucleotides that posttranscriptionally regulate gene expression by directing mRNA cleavage or translational inhibition. Increasing evidence points to a potential role of miRNAs in diverse physiological processes. miR398 targets two closely related Cu/Zn superoxide dismutases (cytosolic CSD1 and chloroplastic CSD2) that can detoxify superoxide radicals. CSD1 and CSD2 transcripts are induced in response to oxidative stress, but the regulatory mechanism of the induction is unknown. Here, we show that miR398 expression is downregulated transcriptionally by oxidative stresses, and this downregulation is important for posttranscriptional CSD1 and CSD2 mRNA accumulation and oxidative stress tolerance. We also provide evidence for an important role of miR398 in specifying the spatial and temporal expression patterns of CSD1 and CSD2 mRNAs. Our results suggest that CSD1 and CSD2 expression is fine-tuned by miR398-directed mRNA cleavage. Additionally, we show that transgenic Arabidopsis thaliana plants overexpressing a miR398-resistant form of CSD2 accumulate more CSD2 mRNA than plants overexpressing a regular CSD2 and are consequently much more tolerant to high light, heavy metals, and other oxidative stresses. Thus, relieving miR398-guided suppression of CSD2 in transgenic plants is an effective new approach to improving plant productivity under oxidative stress conditions.
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              Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.

              Reactive oxygen intermediates (ROI) are strongly associated with plant defense responses. The origin of these ROI has been controversial. Arabidopsis respiratory burst oxidase homologues (rboh genes) have been proposed to play a role in ROI generation. We analyzed lines carrying dSpm insertions in the highly expressed AtrbohD and AtrbohF genes. Both are required for full ROI production observed during incompatible interactions with the bacterial pathogen Pseudomonas syringae pv. tomato DC3000(avrRpm1) and the oomycete parasite Peronospora parasitica. We also observed reduced cell death, visualized by trypan blue stain and reduced electrolyte leakage, in the Atrboh mutants after DC3000(avrRpm1) inoculation. However, enhanced cell death is observed after infection of mutant lines with P. parasitica. Paradoxically, although atrbohD mutation eliminated the majority of total ROI production, atrbohF mutation exhibited the strongest effect on cell death.
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                Author and article information

                Contributors
                jiazaihy@163.com
                j316wenmingwang@sicau.edu.cn
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                06 February 2019
                May 2019
                : 222
                : 3 ( doiID: 10.1111/nph.2019.222.issue-3 )
                : 1507-1522
                Affiliations
                [ 1 ] Rice Research Institute and Key Lab for Major Crop Diseases Sichuan Agricultural University Chengdu 611131 China
                [ 2 ] Collaborative Innovation Center for Hybrid Rice in Yangtze River Basin Sichuan Agricultural University Chengdu 611131 China
                [ 3 ] Department of Plant Pathology University of California Davis Davis CA 95616 USA
                Author notes
                [* ] Authors for correspondence:

                Yan Li

                Tel: +86 028 86290947

                Email: jiazaihy@ 123456163.com

                Wen‐Ming Wang

                Tel: +86 028 86290947

                Email: j316wenmingwang@ 123456sicau.edu.cn

                [†]

                These authors contributed equally to this work.

                Article
                NPH15678 2018-27971
                10.1111/nph.15678
                6593823
                30632163
                © 2019 The Authors. New Phytologist © 2019 New Phytologist Trust

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 8, Tables: 0, Pages: 16, Words: 10660
                Product
                Funding
                Funded by: National Natural Science Foundation of China
                Award ID: 31471761
                Award ID: 31430072
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph15678
                May 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.5 mode:remove_FC converted:26.06.2019

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