{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T05:53:57Z","timestamp":1791438837803,"version":"4.3.3"},"reference-count":28,"publisher":"Wiley","issue":"1","license":[{"start":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T00:00:00Z","timestamp":1791331200000},"content-version":"vor","delay-in-days":6,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["U23A20196"],"award-info":[{"award-number":["U23A20196"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["The Plant Journal"],"published-print":{"date-parts":[[2026,10]]},"abstract":"<jats:title>SUMMARY<\/jats:title>\n                  <jats:p>\n                    The ubiquitin proteasome system (UPS) and autophagy cooperatively orchestrate plant immune homeostasis, while diverse phytopathogens deploy secreted effectors to disrupt their crosstalk for successful colonization. Proteaphagy, the autophagic turnover of intact 26S proteasome holoenzymes, is a conserved stress response co\u2010opted by\n                    <jats:italic>Pseudomonas syringae<\/jats:italic>\n                    effector HopM1 to cripple host proteolysis. However, how the Huanglongbing (HLB) pathogen \u2018\n                    <jats:italic>Candidatus<\/jats:italic>\n                    Liberibacter asiaticus\u2019 (\n                    <jats:italic>C<\/jats:italic>\n                    Las) simultaneously manipulates UPS and autophagy to subvert citrus immunity remains largely uncharacterized. Here, we functionally characterize the secreted\n                    <jats:italic>C<\/jats:italic>\n                    Las effector SDE5640, which exacerbates HLB susceptibility in sweet orange (\n                    <jats:italic>Citrus sinensis<\/jats:italic>\n                    ). SDE5640 directly binds the 19S proteasome chaperone CsPSMD10, whose homodimerization via Cys163\/Cys190 disulfide bonds is required for immune suppression. CsPSMD10 overexpression enhances citrus susceptibility to\n                    <jats:italic>C<\/jats:italic>\n                    Las, whereas the dimerization\u2010deficient CsPSMD10\u2010C190S mutant confers robust HLB resistance. Mechanistically, CsPSMD10 targets CsATG8 isoforms for UPS\u2010dependent degradation to restrain autophagic flux; SDE5640 competitively occupies the Ank2\/Ank3 domains of CsPSMD10 to disrupt CsPSMD10\u2010CsATG8c complexes, thereby stabilizing CsATG8c and triggering autophagy dependent on CsPSMD10. Moreover, SDE5640\u2010induced autophagy drives selective autophagic degradation of the 20S proteasome catalytic subunit CsPBA1, which ultimately disrupts cellular proteasome activity and attenuates salicylic acid\u2010mediated citrus immunity. Collectively, our findings identify a novel SDE5640\u2010CsPSMD10\u2010CsATG8c\u2010CsPBA1 regulatory cascade, illustrating how a single\n                    <jats:italic>C<\/jats:italic>\n                    Las effector synchronously rewires the UPS\u2010autophagy crosstalk to facilitate pathogen proliferation.\n                  <\/jats:p>","DOI":"10.1111\/tpj.71147","type":"journal-article","created":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T05:24:08Z","timestamp":1791437048000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["\u2018\n                    <i>Candidatus<\/i>\n                    Liberibacter asiaticus\u2019 secretory protein\n                    <scp>SDE5640<\/scp>\n                    activates host autophagy dependent on\n                    <scp>PSMD10<\/scp>\n                    to mediate\n                    <scp>PBA1<\/scp>\n                    degradation"],"prefix":"10.1111","volume":"128","author":[{"ORCID":"https:\/\/orcid.org\/0009-0002-5352-5081","authenticated-orcid":false,"given":"Yalin","family":"Mei","sequence":"first","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5994-5832","authenticated-orcid":false,"given":"Xinyi","family":"Deng","sequence":"additional","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zaiyu","family":"Yang","sequence":"additional","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8022-6629","authenticated-orcid":false,"given":"Shimin","family":"Fu","sequence":"additional","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Changyong","family":"Zhou","sequence":"additional","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9293-3427","authenticated-orcid":false,"given":"Xuefeng","family":"Wang","sequence":"additional","affiliation":[{"name":"Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, Citrus Research Institute Southwest University  Chongqing 400712 China"},{"name":"National Citrus Engineering Research Center, Citrus Research Institute Southwest University  Chongqing 400712 China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,7]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"crossref","first-page":"6473","DOI":"10.1128\/AEM.71.11.6473-6478.2005","article-title":"Diversity of \u201cCandidatus Liberibacter asiaticus\u201d based on the omp gene sequence","volume":"71","author":"Bastianel C.","year":"2005","journal-title":"Applied and Environmental Microbiology"},{"key":"e_1_2_8_3_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1008780","article-title":"Ubiquitin\u2010like protein 5 interacts with the silencing suppressor p3 of rice stripe virus and mediates its degradation through the 26S proteasome pathway","volume":"16","author":"Chen B.","year":"2020","journal-title":"PLoS Pathogens"},{"issue":"12","key":"e_1_2_8_4_1","doi-asserted-by":"crossref","first-page":"3165","DOI":"10.1080\/15548627.2025.2569683","article-title":"A secretory protein from \u201cCandidatus Liberibacter asiaticus\u201d targets SNARE protein CsVTI13 to suppress autophagosome\u2010vacuole fusion and promote bacterial infection","volume":"21","author":"Cui X.","year":"2025","journal-title":"Autophagy"},{"key":"e_1_2_8_5_1","doi-asserted-by":"crossref","first-page":"10893","DOI":"10.1074\/jbc.M107313200","article-title":"Gankyrin is an ankyrin\u2010repeat oncoprotein that interacts with CDK4 kinase and the S6 ATPase of the 26 S proteasome","volume":"277","author":"Dawson S.","year":"2002","journal-title":"Journal of Biological Chemistry"},{"key":"e_1_2_8_6_1","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1111\/mpp.13296","article-title":"A prophage\u2010encoded effector from \u201cCandidatus Liberibacter asiaticus\u201d targets ASCORBATE PEROXIDASE6 in citrus to facilitate bacterial infection","volume":"24","author":"Du J.","year":"2023","journal-title":"Molecular Plant Pathology"},{"key":"e_1_2_8_7_1","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1105\/tpc.15.01022","article-title":"The proteasome stress regulon is controlled by a pair of NAC transcription factors in Arabidopsis","volume":"28","author":"Gladman N.P.","year":"2016","journal-title":"Plant Cell"},{"key":"e_1_2_8_8_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1005401","article-title":"Redundant roles of Rpn10 and Rpn13 in recognition of ubiquitinated proteins and cellular homeostasis","volume":"11","author":"Hamazaki J.","year":"2015","journal-title":"PLoS Genetics"},{"key":"e_1_2_8_9_1","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.gene.2019.04.021","article-title":"Functional analysis of citrus AP2 transcription factors identified CsAP2\u201009 involved in citrus canker disease response and tolerance","volume":"707","author":"He Y.","year":"2019","journal-title":"Gene"},{"key":"e_1_2_8_10_1","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1038\/nrmicro3160","article-title":"Bacteria\u2013autophagy interplay: a battle for survival","volume":"12","author":"Huang J.","year":"2014","journal-title":"Nature Reviews. Microbiology"},{"key":"e_1_2_8_11_1","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1099\/00207713-47-1-224","article-title":"Comparison of the 16S\/23S ribosomal intergenic regions of \u201cCandidatus Liberobacter asiaticum\u201d and \u201cCandidatus Liberobacter africanum,\u201d the two species associated with Citrus Huanglongbing (Greening) Disease","volume":"47","author":"Jagoueix S.","year":"1997","journal-title":"International Journal of Systematic Bacteriology"},{"key":"e_1_2_8_12_1","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1159\/000351979","article-title":"The mechanism and physiological function of macroautophagy","volume":"5","author":"Klionsky D.J.","year":"2013","journal-title":"Journal of Innate Immunity"},{"key":"e_1_2_8_13_1","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1016\/j.chom.2020.07.010","article-title":"Phytopathogen effectors use multiple mechanisms to manipulate plant autophagy","volume":"28","author":"Lal N.K.","year":"2020","journal-title":"Cell Host & Microbe"},{"key":"e_1_2_8_14_1","doi-asserted-by":"crossref","DOI":"10.15252\/embj.2021110352","article-title":"A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component","volume":"41","author":"Leong J.X.","year":"2022","journal-title":"EMBO Journal"},{"key":"e_1_2_8_15_1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.69047","article-title":"Genetically incorporated crosslinkers reveal NleE attenuates host autophagy dependent on PSMD10","volume":"10","author":"Li J.","year":"2021","journal-title":"eLife"},{"key":"e_1_2_8_16_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.xplc.2023.100626","article-title":"The E3 ubiquitin ligase OsRGLG5 targeted by the Magnaporthe oryzae effector AvrPi9 confers basal resistance against rice blast","volume":"4","author":"Liu Z.","year":"2023","journal-title":"Plant Communications"},{"issue":"8","key":"e_1_2_8_17_1","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1080\/15548627.2015.1034405","article-title":"PSMD10\/gankyrin induces autophagy to promote tumor progression through cytoplasmic interaction with ATG7 and nuclear transactivation of ATG7 expression","volume":"12","author":"Luo T.","year":"2016","journal-title":"Autophagy"},{"key":"e_1_2_8_18_1","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1016\/j.molcel.2015.04.023","article-title":"Autophagic degradation of the 26S proteasome is mediated by the dual ATG8\/ubiquitin receptor RPN10 in Arabidopsis","volume":"58","author":"Marshall R.S.","year":"2015","journal-title":"Molecular Cell"},{"key":"e_1_2_8_19_1","doi-asserted-by":"crossref","first-page":"1717","DOI":"10.1016\/j.celrep.2016.07.015","article-title":"Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 Chaperone","volume":"16","author":"Marshall R.S.","year":"2016","journal-title":"Cell Reports"},{"key":"e_1_2_8_20_1","doi-asserted-by":"crossref","first-page":"8809","DOI":"10.1021\/acs.jafc.4c12314","article-title":"Ubiquitin receptor RPN13\u2010mediated \u201cCandidatus Liberibacter asiaticus\u201d virulence effector degradation to positively regulate immunity","volume":"73","author":"Mei Y.","year":"2025","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"e_1_2_8_21_1","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1111\/pbi.12733","article-title":"Engineering canker\u2010resistant plants through CRISPR\/Cas9\u2010targeted editing of the susceptibility gene CsLOB1 promoter in citrus","volume":"15","author":"Peng A.","year":"2017","journal-title":"Plant Biotechnology Journal"},{"key":"e_1_2_8_22_1","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1126\/science.aax3769","article-title":"Cellular quality control by the ubiquitin\u2010proteasome system and autophagy","volume":"366","author":"Pohl C.","year":"2019","journal-title":"Science"},{"key":"e_1_2_8_23_1","doi-asserted-by":"crossref","first-page":"4670","DOI":"10.1093\/jxb\/erad176","article-title":"An effector of \u2018Candidatus Liberibacter asiaticus\u2019 manipulates autophagy to promote bacterial infection","volume":"74","author":"Shi H.","year":"2023","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_8_24_1","doi-asserted-by":"crossref","first-page":"2558","DOI":"10.1080\/15548627.2023.2213040","article-title":"\u201cCandidatus Liberibacter asiaticus\u201d secretory protein SDE3 inhibits host autophagy to promote Huanglongbing disease in citrus","volume":"19","author":"Shi J.","year":"2023","journal-title":"Autophagy"},{"key":"e_1_2_8_25_1","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1105\/tpc.17.00815","article-title":"Bacteria exploit autophagy for proteasome degradation and enhanced virulence in plants","volume":"30","author":"\u00dcst\u00fcn S.","year":"2018","journal-title":"The Plant Cell"},{"key":"e_1_2_8_26_1","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/nrm2688","article-title":"The ubiquitin\u201026S proteasome system at the nexus of plant biology","volume":"10","author":"Vierstra R.D.","year":"2009","journal-title":"Nature Reviews. Molecular Cell Biology"},{"key":"e_1_2_8_27_1","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.cell.2019.06.007","article-title":"A bacterial effector reveals the V\u2010ATPase\u2010ATG16L1 axis that initiates xenophagy","volume":"178","author":"Xu Y.","year":"2019","journal-title":"Cell"},{"key":"e_1_2_8_28_1","article-title":"The Arabidopsis E3 ubiquitin ligase PUB4 regulates BIK1 and is targeted by a bacterial type\u2010III effector","volume":"41","author":"Yu G.","year":"2022","journal-title":"EMBO Journal"},{"key":"e_1_2_8_29_1","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1126\/science.adq7203","article-title":"Targeted MYC2 stabilization confers citrus Huanglongbing resistance","volume":"388","author":"Zhao P.","year":"2025","journal-title":"Science"}],"container-title":["The Plant Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/tpj.71147","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/tpj.71147","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/tpj.71147","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T05:24:12Z","timestamp":1791437052000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/tpj.71147"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10]]},"references-count":28,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2026,10]]}},"alternative-id":["10.1111\/tpj.71147"],"URL":"https:\/\/doi.org\/10.1111\/tpj.71147","archive":["Portico"],"relation":{},"ISSN":["0960-7412","1365-313X"],"issn-type":[{"value":"0960-7412","type":"print"},{"value":"1365-313X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10]]},"assertion":[{"value":"2026-01-23","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-12","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-10-07","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e71147"}}