Xuejin Cui, Meixia Du, Xiyin Zheng, Li Ren, Yingzhe Yuan, Shimian Ma, Caifu Liu, Xiuping Zou, Shimin Fu, Changyong Zhou, Xuefeng Wang
{"title":"亚洲Liberibacter asiaticus分泌蛋白靶向SNARE蛋白CsVTI13抑制自噬体-液泡融合，促进细菌感染。","authors":"Xuejin Cui, Meixia Du, Xiyin Zheng, Li Ren, Yingzhe Yuan, Shimian Ma, Caifu Liu, Xiuping Zou, Shimin Fu, Changyong Zhou, Xuefeng Wang","doi":"10.1080/15548627.2025.2569683","DOIUrl":null,"url":null,"abstract":"<p><p>Macroautophagy/autophagy functions in plant host immunity responses to pathogen infection. The molecular mechanisms and functions used by the citrus Huanglongbing (HLB)-associated intracellular bacterium \"<i>Candidatus</i> Liberibacter asiaticus\" (<i>C</i>Las) to manipulate autophagy are largely unknown. Here, we identified a <i>C</i>Las effector, SDE4580 (CLIBASIA_04580), which contributes to HLB progression. Transgenic SDE4405 in Wanjincheng orange (<i>Citrus sinensi</i>s) promotes <i>C</i>Las proliferation and symptom expression, while inhibiting autophagosome-vacuole fusion. Further investigations revealed that SDE4580 interacts with the citrus SNARE protein CsVTI13, which positively regulates autophagosome-vacuole fusion and limits pathogen proliferation. CsVTI13 interacts with CsSYP22, which acts as a bridge connecting CsVTI13 to CsATG8g, a process that is critical for the CsVTI13-mediated promotion of autophagic flux. Additional analyses demonstrated that SDE4580 competitively disrupts the interaction between CsVTI13 and CsSYP22, thereby inhibiting CsVTI13-mediated autophagy. Our findings demonstrate the role of SDE4580 in manipulating SNARE proteins for disrupting autophagosome-vacuole fusion and impairing autophagy-mediated antimicrobial defenses, unraveling a novel pathogen strategy to counteract defense-related autophagy during plant-bacteria interaction.<b>Abbreviations</b>: ATG: autophagy related; BSMV: barley stripe mosaic virus; BiFC: bimolecular fluorescence complementation; BTH: benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester; <i>C</i>Las: <i>Candidatus</i> Liberibacter asiaticus; co-IP: co-immunoprecipitation; CsACD2: ACCELERATED CELL DEATH 2; HLB: Huanglongbing; <i>N. benthamiana: Nicotiana benthamiana</i>; PhoA: alkaline phosphatase; PtdIns3K: phosphatidylinositol 3-kinase; SNARE: soluble N-ethylmaleimide-sensitive factor attachment protein receptor; VPS34: vacuolar protein sorting 34; WT: wild-type; Y2H: yeast two-hybrid.</p>","PeriodicalId":93893,"journal":{"name":"Autophagy","volume":" ","pages":"1-17"},"PeriodicalIF":14.3000,"publicationDate":"2025-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"A secretory protein from \\\"<i>candidatus</i> Liberibacter asiaticus\\\" targets SNARE protein CsVTI13 to suppress autophagosome-vacuole fusion and promote bacterial infection.\",\"authors\":\"Xuejin Cui, Meixia Du, Xiyin Zheng, Li Ren, Yingzhe Yuan, Shimian Ma, Caifu Liu, Xiuping Zou, Shimin Fu, Changyong Zhou, Xuefeng Wang\",\"doi\":\"10.1080/15548627.2025.2569683\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Macroautophagy/autophagy functions in plant host immunity responses to pathogen infection. The molecular mechanisms and functions used by the citrus Huanglongbing (HLB)-associated intracellular bacterium \\\"<i>Candidatus</i> Liberibacter asiaticus\\\" (<i>C</i>Las) to manipulate autophagy are largely unknown. Here, we identified a <i>C</i>Las effector, SDE4580 (CLIBASIA_04580), which contributes to HLB progression. Transgenic SDE4405 in Wanjincheng orange (<i>Citrus sinensi</i>s) promotes <i>C</i>Las proliferation and symptom expression, while inhibiting autophagosome-vacuole fusion. Further investigations revealed that SDE4580 interacts with the citrus SNARE protein CsVTI13, which positively regulates autophagosome-vacuole fusion and limits pathogen proliferation. CsVTI13 interacts with CsSYP22, which acts as a bridge connecting CsVTI13 to CsATG8g, a process that is critical for the CsVTI13-mediated promotion of autophagic flux. Additional analyses demonstrated that SDE4580 competitively disrupts the interaction between CsVTI13 and CsSYP22, thereby inhibiting CsVTI13-mediated autophagy. Our findings demonstrate the role of SDE4580 in manipulating SNARE proteins for disrupting autophagosome-vacuole fusion and impairing autophagy-mediated antimicrobial defenses, unraveling a novel pathogen strategy to counteract defense-related autophagy during plant-bacteria interaction.<b>Abbreviations</b>: ATG: autophagy related; BSMV: barley stripe mosaic virus; BiFC: bimolecular fluorescence complementation; BTH: benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester; <i>C</i>Las: <i>Candidatus</i> Liberibacter asiaticus; co-IP: co-immunoprecipitation; CsACD2: ACCELERATED CELL DEATH 2; HLB: Huanglongbing; <i>N. benthamiana: Nicotiana benthamiana</i>; PhoA: alkaline phosphatase; PtdIns3K: phosphatidylinositol 3-kinase; SNARE: soluble N-ethylmaleimide-sensitive factor attachment protein receptor; VPS34: vacuolar protein sorting 34; WT: wild-type; Y2H: yeast two-hybrid.</p>\",\"PeriodicalId\":93893,\"journal\":{\"name\":\"Autophagy\",\"volume\":\" \",\"pages\":\"1-17\"},\"PeriodicalIF\":14.3000,\"publicationDate\":\"2025-10-08\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Autophagy\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1080/15548627.2025.2569683\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"\",\"JCRName\":\"\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Autophagy","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1080/15548627.2025.2569683","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
A secretory protein from "candidatus Liberibacter asiaticus" targets SNARE protein CsVTI13 to suppress autophagosome-vacuole fusion and promote bacterial infection.
Macroautophagy/autophagy functions in plant host immunity responses to pathogen infection. The molecular mechanisms and functions used by the citrus Huanglongbing (HLB)-associated intracellular bacterium "Candidatus Liberibacter asiaticus" (CLas) to manipulate autophagy are largely unknown. Here, we identified a CLas effector, SDE4580 (CLIBASIA_04580), which contributes to HLB progression. Transgenic SDE4405 in Wanjincheng orange (Citrus sinensis) promotes CLas proliferation and symptom expression, while inhibiting autophagosome-vacuole fusion. Further investigations revealed that SDE4580 interacts with the citrus SNARE protein CsVTI13, which positively regulates autophagosome-vacuole fusion and limits pathogen proliferation. CsVTI13 interacts with CsSYP22, which acts as a bridge connecting CsVTI13 to CsATG8g, a process that is critical for the CsVTI13-mediated promotion of autophagic flux. Additional analyses demonstrated that SDE4580 competitively disrupts the interaction between CsVTI13 and CsSYP22, thereby inhibiting CsVTI13-mediated autophagy. Our findings demonstrate the role of SDE4580 in manipulating SNARE proteins for disrupting autophagosome-vacuole fusion and impairing autophagy-mediated antimicrobial defenses, unraveling a novel pathogen strategy to counteract defense-related autophagy during plant-bacteria interaction.Abbreviations: ATG: autophagy related; BSMV: barley stripe mosaic virus; BiFC: bimolecular fluorescence complementation; BTH: benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester; CLas: Candidatus Liberibacter asiaticus; co-IP: co-immunoprecipitation; CsACD2: ACCELERATED CELL DEATH 2; HLB: Huanglongbing; N. benthamiana: Nicotiana benthamiana; PhoA: alkaline phosphatase; PtdIns3K: phosphatidylinositol 3-kinase; SNARE: soluble N-ethylmaleimide-sensitive factor attachment protein receptor; VPS34: vacuolar protein sorting 34; WT: wild-type; Y2H: yeast two-hybrid.
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