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      Overexpression of MdATG18a in apple improves resistance to Diplocarpon mali infection by enhancing antioxidant activity and salicylic acid levels

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          Abstract

          Marssonina apple blotch, caused by Diplocarpon mali, is one of the most serious diseases of apple. Autophagy plays a key role in pathogen resistance. We previously showed that MdATG18a has a positive influence on drought tolerance. Herein, we describe how overexpression (OE) of MdATG18a enhances resistance to D. mali infection, probably because less H 2O 2 but more salicylic acid (SA) is accumulated in the leaves of OE apple plants. Expression of chitinase, β-1,3-glucanase, and SA-related marker genes was induced more strongly by D. mali in OE lines. Transcript levels of other important MdATG genes were also drastically increased by D. mali in OE plants, which indicated increased autophagy activities. Taken together, these results demonstrate that OE of MdATG18a enhances resistance to infection by D. mali and plays positive roles in H 2O 2-scavenging and SA accumulations. Our findings provide important information for designing strategies which could induce autophagy to minimize the impact of this disease on apple production.

          Improving resistance to apple blotch disease

          Apple plants that express high levels of a gene involved in the destruction of damaged and redundant cell components demonstrate improved resistance to a serious fungal infection. Fengwang Ma and colleagues of China’s Northwest A&F University in Shaanxi examined the effect of overexpressing the gene MdATG18a on Diplocarpon mali fungal infection in apple plants. This gene was previously found to promote drought tolerance in apple plants and is known for its involvement in autophagy, an immune response to infection that removes damaged cell organelles. The researchers found that plants overexpressing MdATG18a were more resistant to developing Marssonina apple blotch disease compared to wild apple plants, most likely due to improvements in autophagy activity. The team concludes that strategies designed to induce autophagy could improve apple resistance to fungal infection.

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          H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.

          Microbial elicitors or attempted infection with an avirulent pathogen strain causes the rapid production of reactive oxygen intermediates. We report here that H2O2 from this oxidative burst not only drives the cross-linking of cell wall structural proteins, but also functions as a local trigger of programmed death in challenged cells and as a diffusible signal for the induction in adjacent cells of genes encoding cellular protectants such as glutathione S-transferase and glutathione peroxidase. Thus, H2O2 from the oxidative burst plays a key role in the orchestration of a localized hypersensitive response during the expression of plant disease resistance.
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            Cross talk between signaling pathways in pathogen defense.

            Plant defense in response to microbial attack is regulated through a complex network of signaling pathways that involve three signaling molecules: salicylic acid (SA), jasmonic acid (JA) and ethylene. The SA and JA signaling pathways are mutually antagonistic. This regulatory cross talk may have evolved to allow plants to fine-tune the induction of their defenses in response to different plant pathogens.
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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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                Author and article information

                Contributors
                +86-29-87082648 , fwm64@sina.com , fwm64@nwsuaf.edu.cn
                Journal
                Hortic Res
                Hortic Res
                Horticulture Research
                Nature Publishing Group UK (London )
                2052-7276
                1 November 2018
                1 November 2018
                2018
                : 5
                : 57
                Affiliations
                ISNI 0000 0004 1760 4150, GRID grid.144022.1, State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, , Northwest A&F University, ; 712100 Yangling, Shaanxi China
                Article
                59
                10.1038/s41438-018-0059-5
                6210185
                30393539
                634ef96d-c39d-4fce-b703-72280677bf53
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 8 January 2018
                : 4 June 2018
                : 4 June 2018
                Funding
                Funded by: State Key Program of the National Natural Science Foundation of China (31330068) Young Scientists Fund of the National Natural Science Foundation of China (31601735) China Agriculture Research System (CARS-27)
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                © The Author(s) 2018

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