' Candidatus Liberibacter asiaticus' secretory protein SDE3 inhibits host autophagy to promote Huanglongbing disease in citrus

Jinxia Shi; Yinan Gong; Hongwei Shi; Xiaoding Ma; Yuanhong Zhu; Fan Yang; Dan Wang; Yating Fu; Yu Lin; Naiying Yang; Zhuhui Yang; Chunhua Zeng; Weimin Li; Changyong Zhou; Xuefeng Wang; Yongli Qiao

doi:10.1080/15548627.2023.2213040

' Candidatus Liberibacter asiaticus' secretory protein SDE3 inhibits host autophagy to promote Huanglongbing disease in citrus

Autophagy. 2023 Sep;19(9):2558-2574. doi: 10.1080/15548627.2023.2213040. Epub 2023 May 30.

Authors

Jinxia Shi¹, Yinan Gong¹, Hongwei Shi², Xiaoding Ma³, Yuanhong Zhu^{1

4}, Fan Yang¹, Dan Wang¹, Yating Fu¹, Yu Lin¹, Naiying Yang¹, Zhuhui Yang², Chunhua Zeng², Weimin Li⁵, Changyong Zhou², Xuefeng Wang², Yongli Qiao¹

Affiliations

¹ Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.
² National Citrus Engineering Research Center, Citrus Research Institute, Southwest University, Chongqing, China.
³ National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.
⁴ State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
⁵ Key Laboratory for Northern Urban Agriculture of Ministry of Agriculture and Rural Affairs, Beijing University of Agriculture, Beijing, China.

PMID: 37249424
PMCID: PMC10392736 (available on 2024-05-30)
DOI: 10.1080/15548627.2023.2213040

Abstract

Antimicrobial acroautophagy/autophagy plays a vital role in degrading intracellular pathogens or microbial molecules in host-microbe interactions. However, microbes evolved various mechanisms to hijack or modulate autophagy to escape elimination. Vector-transmitted phloem-limited bacteria, Candidatus Liberibacter (Ca. Liberibacter) species, cause Huanglongbing (HLB), one of the most catastrophic citrus diseases worldwide, yet contributions of autophagy to HLB disease proliferation remain poorly defined. Here, we report the identification of a virulence effector in "Ca. Liberibacter asiaticus" (Las), SDE3, which is highly conserved among the "Ca. Liberibacter". SDE3 expression not only promotes the disease development of HLB and canker in sweet orange (Citrus sinensis) plants but also facilitates Phytophthora and viral infections in Arabidopsis, and Nicotiana benthamiana (N. benthamiana). SDE3 directly associates with citrus cytosolic glyceraldehyde-3-phosphate dehydrogenases (CsGAPCs), which negatively regulates plant immunity. Overexpression of CsGAPCs and SDE3 significantly inhibits autophagy in citrus, Arabidopsis, and N. benthamiana. Intriguingly, SDE3 undermines autophagy-mediated immunity by the specific degradation of CsATG8 family proteins in a CsGAPC1-dependent manner. CsATG8 degradation is largely rescued by treatment with an inhibitor of the late autophagic pathway, E64d. Furthermore, ectopic expression of CsATG8s enhances Phytophthora resistance. Collectively, these results suggest that SDE3-CsGAPC interactions modulate CsATG8-mediated autophagy to enhance Las progression in citrus.Abbreviations: ACP: asian citrus psyllid; ACD2: ACCELERATED CELL DEATH 2; ATG: autophagy related; Ca. Liberibacter: Candidatus Liberibacter; CaMV: cauliflower mosaic virus; CMV: cucumber mosaic virus; Cs: Citrus sinensis; EV: empty vector; GAPC: cytosolic glyceraldehyde-3-phosphate dehydrogenase; HLB: huanglongbing; H₂O₂: hydrogen peroxide; Las: liberibacter asiaticus; Laf: liberibacter africanus; Lam: liberibacter americanus; Pst: Pseudomonas syringae pv. tomato; PVX: potato virus X; ROS: reactive oxygen species; SDE3: sec-delivered effector 3; TEM: transmission electron microscopy; VIVE : virus-induced virulence effector; WT: wild-type; Xcc: Xanthomonas citri subsp. citri.

Keywords: ATG8; E64D; GAPC; effector; plant immunity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Arabidopsis*
Autophagy
Citrus* / microbiology
Hemiptera* / physiology
Hydrogen Peroxide
Liberibacter
Plant Diseases / microbiology
Rhizobiaceae*

Substances

Hydrogen Peroxide

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China (32172359, 32072502, 32001883, and 31871925), the National Key Research and Development Program of China (2018YFD0201500, 2021YFD1400800), the Science and Technology Commission of Shanghai Municipality (18DZ2260500).