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      Proteomic analysis of the defense response to Magnaporthe oryzae in rice harboring the blast resistance gene Piz-t

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          Abstract

          Background

          Rice blast (caused by Magnaporthe oryzae) is one of the most destructive diseases of rice. While many blast resistance ( R) genes have been identified and deployed in rice cultivars, little is known about the R gene-mediated defense mechanism. We used a rice transgenic line harboring the resistance gene Piz-t to investigate the R gene-mediated resistance response to infection.

          Results

          We conducted comparative proteome profiling of the Piz-t transgenic Nipponbare line (NPB-Piz-t) and wild-type Nipponbare (NPB) inoculated with M. oryzae at 24, 48, 72 h post-inoculation (hpi) using isobaric tags for relative and absolute quantification (iTRAQ) analysis. Comparative analysis of the response of NPB-Piz-t to the avirulent isolate KJ201 and the virulent isolate RB22 identified 114 differentially expressed proteins (DEPs) between KJ201-inoculated NPB-Piz-t (KJ201-Piz-t) and mock-treated NPB-Piz-t (Mock-Piz-t), and 118 DEPs between RB22-inoculated NPB-Piz-t (RB22-Piz-t) and Mock-Piz-t. Among the DEPs, 56 occurred commonly in comparisons KJ201-Piz-t/Mock-Piz-t and RB22-Piz-t/Mock-Piz-t. In a comparison of the responses of NPB and NPB-Piz-t to isolate KJ201, 93 DEPs between KJ201-Piz-t and KJ201-NPB were identified. DEPs in comparisons KJ201-Piz-t/Mock-Piz-t, RB22-Piz-t/Mock-Piz-t and KJ201-Piz-t/KJ201-NPB contained a number of proteins that may be involved in rice response to pathogens, including pathogenesis-related (PR) proteins, hormonal regulation-related proteins, defense and stress response-related proteins, receptor-like kinase, and cytochrome P450. Comparative analysis further identified 7 common DEPs between the comparisons KJ201-Piz-t/KJ201-NPB and KJ201-Piz-t/RB22-Piz-t, including alcohol dehydrogenase I, receptor-like protein kinase, endochitinase, similar to rubisco large subunit, NADP-dependent malic enzyme, and two hypothetical proteins.

          Conclusions

          Our results provide a valuable resource for discovery of complex protein networks involved in the resistance response of rice to blast fungus.

          Electronic supplementary material

          The online version of this article (10.1186/s12284-018-0240-3) contains supplementary material, which is available to authorized users.

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          Most cited references24

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          Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.

          Receptor-like kinases (RLKs) belong to the large RLK/Pelle gene family, and it is known that the Arabidopsis thaliana genome contains >600 such members, which play important roles in plant growth, development, and defense responses. Surprisingly, we found that rice (Oryza sativa) has nearly twice as many RLK/Pelle members as Arabidopsis does, and it is not simply a consequence of a larger predicted gene number in rice. From the inferred phylogeny of all Arabidopsis and rice RLK/Pelle members, we estimated that the common ancestor of Arabidopsis and rice had >440 RLK/Pelles and that large-scale expansions of certain RLK/Pelle members and fusions of novel domains have occurred in both the Arabidopsis and rice lineages since their divergence. In addition, the extracellular domains have higher nonsynonymous substitution rates than the intracellular domains, consistent with the role of extracellular domains in sensing diverse signals. The lineage-specific expansions in Arabidopsis can be attributed to both tandem and large-scale duplications, whereas tandem duplication seems to be the major mechanism for recent expansions in rice. Interestingly, although the RLKs that are involved in development seem to have rarely been duplicated after the Arabidopsis-rice split, those that are involved in defense/disease resistance apparently have undergone many duplication events. These findings led us to hypothesize that most of the recent expansions of the RLK/Pelle family have involved defense/resistance-related genes.
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            The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice.

            Although the functions of a few effector proteins produced by bacterial and oomycete plant pathogens have been elucidated in recent years, information for the vast majority of pathogen effectors is still lacking, particularly for those of plant-pathogenic fungi. Here, we show that the avirulence effector AvrPiz-t from the rice blast fungus Magnaporthe oryzae preferentially accumulates in the specialized structure called the biotrophic interfacial complex and is then translocated into rice (Oryza sativa) cells. Ectopic expression of AvrPiz-t in transgenic rice suppresses the flg22- and chitin-induced generation of reactive oxygen species (ROS) and enhances susceptibility to M. oryzae, indicating that AvrPiz-t functions to suppress pathogen-associated molecular pattern (PAMP)-triggered immunity in rice. Interaction assays show that AvrPiz-t suppresses the ubiquitin ligase activity of the rice RING E3 ubiquitin ligase APIP6 and that, in return, APIP6 ubiquitinates AvrPiz-t in vitro. Interestingly, agroinfection assays reveal that AvrPiz-t and AvrPiz-t Interacting Protein 6 (APIP6) are both degraded when coexpressed in Nicotiana benthamiana. Silencing of APIP6 in transgenic rice leads to a significant reduction of flg22-induced ROS generation, suppression of defense-related gene expression, and enhanced susceptibility of rice plants to M. oryzae. Taken together, our results reveal a mechanism in which a fungal effector targets the host ubiquitin proteasome system for the suppression of PAMP-triggered immunity in plants.
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              Magnaporthe as a model for understanding host-pathogen interactions.

              The rice blast pathosystem has been the subject of intense interest in part because of the importance of the disease to world agriculture, but also because both Magnaporthe oryzae and its host are amenable to advanced experimental approaches. The goal of this review is to provide an overview of the system and to point out recent significant studies that update our understanding of the biology of M. oryzae. The genome sequence of M. oryzae has provided insight into how genome structure and pathogen population genetic variability has been shaped by transposable elements. The sequence allows systematic approaches to long-standing areas of investigation, including pathogen development and the molecular basis of compatible and incompatible interactions with its host. Rice blast provides an integrated system to illustrate most of the important concepts governing fungal/plant interactions and serves as an excellent starting point for gaining a broad perspective of issues in plant pathology.
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                Author and article information

                Contributors
                yangliming@njfu.edu.cn
                songbiao_chen@hotmail.com , sbchen@fjage.org
                Journal
                Rice (N Y)
                Rice (N Y)
                Rice
                Springer US (New York )
                1939-8425
                1939-8433
                15 August 2018
                15 August 2018
                2018
                : 11
                : 47
                Affiliations
                [1 ]ISNI 0000 0001 2229 4212, GRID grid.418033.d, Biotechnology Research Institute, Fujian Key Laboratory of Genetic Engineering for Agriculture, , Fujian Academy of Agricultural Sciences, ; Fuzhou, 350003 China
                [2 ]GRID grid.410625.4, College of Biology and the Environment, , Nanjing Forestry University, ; Nanjing, 210037 China
                [3 ]GRID grid.449133.8, Institute of Oceanography, Marine Biotechnology Center, , Minjiang University, ; Fuzhou, 350108 China
                [4 ]ISNI 0000 0004 1760 2876, GRID grid.256111.0, College of Crop Science, , Fujian Agricultural and Forestry University, ; Fuzhou, 350002 China
                [5 ]ISNI 0000 0004 1804 2567, GRID grid.410738.9, College of Life Sciences, , Huaiyin Normal University, ; Huaian, 223300 China
                Author information
                http://orcid.org/0000-0003-1500-2298
                Article
                240
                10.1186/s12284-018-0240-3
                6093832
                30112588
                3c35ae62-13f6-46a7-b45a-d2a8d6ef85d7
                © The Author(s). 2018

                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
                : 9 April 2018
                : 2 August 2018
                Funding
                Funded by: National Natural Science Foundation of China (CN)
                Award ID: U1405212
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31640006
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003392, Natural Science Foundation of Fujian Province;
                Award ID: 2014J07004
                Award Recipient :
                Categories
                Original Article
                Custom metadata
                © The Author(s) 2018

                Agriculture
                proteomic analysis,rice blast disease,resistance gene,piz-t,itraq
                Agriculture
                proteomic analysis, rice blast disease, resistance gene, piz-t, itraq

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