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      Identification and characterization of a spotted-leaf mutant spl40 with enhanced bacterial blight resistance in rice

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          Abstract

          Background

          Spotted leaf mutants show typical necrotic lesions that appear spontaneously in the absence of any pathogen attack. These mutants are often characterized to exhibit programmed cell death (PCD) and activation of plant defense responses resulting in enhanced disease resistance to multiple pathogens. Here, we reported a novel spotted-leaf mutant, spl40 that showed enhanced disease resistance response.

          Results

          Initially lesions appeared at leaf tips during seedling stage and gradually covered the whole leaf at the tillering stage. The lesion development was light-dependent. spl40 showed obvious cell death at and around the lesion, and burst of reactive oxygen species (ROS) was accompanied by disturbed ROS scavenging system. Photosynthetic capacity was compromised as evidenced by significant reductions in chlorophyll content, important photosynthesis parameters and downregulated expression of photosynthesis-related genes which ultimately led to poor performance of major agronomic traits. spl40 exhibited enhanced resistance to 14 out of 16 races of bacterial blight pathogen of rice, caused by Xanthomonas oryzae pv. oryzae, most probably though activation of SA and JA signaling pathways, owing to upregulated expression of SA and JA signaling genes, though the exact mechanism remain to be elucidated. The spotted-leaf phenotype was controlled by a novel single recessive nuclear gene. Genetic mapping combined with high throughput sequencing analysis identified Os05G0312000 as the most probable candidate gene. Sequencing of ORF revealed a single SNP change from C to T that resulted in non-synonymous change in amino acid residue from leucine to phenylalanine. Interestingly, the complementation plants did not display lesions before heading but showed lesions at the heading stage and the transgenic T 1 progenies could be classified into 3 categories based on their lesion intensity, indicating the complex genetic nature of the spl40 mutation.

          Conclusion

          The results obtained here clearly show that genes related to defense and PCD were upregulated in accordance with enhanced disease resistance and occurrence of PCD, whereas the photosynthetic capacity and overall ROS homeostasis was compromised in spl40. Our data suggest that a novel spotted-leaf mutant, spl40, would help to elucidate the mechanism behind lesion development involving programmed cell death and associated defense responses.

          Electronic supplementary material

          The online version of this article (10.1186/s12284-019-0326-6) contains supplementary material, which is available to authorized users.

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          Most cited references49

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          Plant pathogens and integrated defence responses to infection.

          Plants cannot move to escape environmental challenges. Biotic stresses result from a battery of potential pathogens: fungi, bacteria, nematodes and insects intercept the photosynthate produced by plants, and viruses use replication machinery at the host's expense. Plants, in turn, have evolved sophisticated mechanisms to perceive such attacks, and to translate that perception into an adaptive response. Here, we review the current knowledge of recognition-dependent disease resistance in plants. We include a few crucial concepts to compare and contrast plant innate immunity with that more commonly associated with animals. There are appreciable differences, but also surprising parallels.
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            Autophagy regulates programmed cell death during the plant innate immune response.

            The plant innate immune response includes the hypersensitive response (HR), a form of programmed cell death (PCD). PCD must be restricted to infection sites to prevent the HR from playing a pathologic rather than protective role. Here we show that plant BECLIN 1, an ortholog of the yeast and mammalian autophagy gene ATG6/VPS30/beclin 1, functions to restrict HR PCD to infection sites. Initiation of HR PCD is normal in BECLIN 1-deficient plants, but remarkably, healthy uninfected tissue adjacent to HR lesions and leaves distal to the inoculated leaf undergo unrestricted PCD. In the HR PCD response, autophagy is induced in both pathogen-infected cells and distal uninfected cells; this is reduced in BECLIN 1-deficient plants. The restriction of HR PCD also requires orthologs of other autophagy-related genes including PI3K/VPS34, ATG3, and ATG7. Thus, the evolutionarily conserved autophagy pathway plays an essential role in plant innate immunity and negatively regulates PCD.
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              Programmed cell death, mitochondria and the plant hypersensitive response.

              The plant response to attempted infection by microbial pathogens is often accompanied by rapid cell death in and around the initial infection site, a reaction known as the hypersensitive response. This response is associated with restricted pathogen growth and represents a form of programmed cell death (PCD). Recent pharmacological and molecular studies have provided functional evidence for the conservation of some of the basic regulatory mechanisms underlying the response to pathogens and the activation of PCD in animal and plant systems. In animals, the mitochondrion integrates diverse cellular stress signals and initiates the death execution pathway, and studies indicate a similar involvement for mitochondria in regulating PCD in plants. But many of the cell-death regulators that have been characterized in humans, worms and flies are absent from the Arabidopsis genome, indicating that plants probably use other regulators to control this process.
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                Author and article information

                Contributors
                atulsathe@163.com
                suxiaona1990@163.com
                chenzheng7@126.com
                chenting218@163.com
                weixiangjing@caas.cn
                sqtang@126.com
                86-571-63370295 , hello.xiaobo@163.com
                86-571-63370326 , beishangd@163.com
                Journal
                Rice (N Y)
                Rice (N Y)
                Rice
                Springer US (New York )
                1939-8425
                1939-8433
                24 August 2019
                24 August 2019
                2019
                : 12
                : 68
                Affiliations
                [1 ]ISNI 0000 0000 9824 1056, GRID grid.418527.d, State Key Laboratory of Rice Biology, , China National Rice Research Institute, ; Hangzhou, 310006 China
                [2 ]ISNI 0000 0004 1808 3238, GRID grid.411859.0, Nanchang Business College of Jiangxi Agricultural University, ; Nanchang, 330044 China
                Author information
                http://orcid.org/0000-0003-3480-1503
                Article
                326
                10.1186/s12284-019-0326-6
                6708518
                31446514
                b8b8a955-035a-4c52-b9d1-826b49dd6b0d
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 11 January 2019
                : 15 August 2019
                Funding
                Funded by: Ministry of Agriculture of China
                Award ID: 2016ZX08001-002
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004751, Department of Science and Technology for Social Development;
                Award ID: 2016YFD0101104
                Award Recipient :
                Categories
                Original Article
                Custom metadata
                © The Author(s) 2019

                Agriculture
                rice,spotted-leaf,programmed cell death,bacterial blight,defense response
                Agriculture
                rice, spotted-leaf, programmed cell death, bacterial blight, defense response

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