J Integr Plant Biol. ›› 2023, Vol. 65 ›› Issue (5): 1328-1343.DOI: 10.1111/jipb.13452

• Plant Biotic Interactions • Previous Articles     Next Articles

Geminiviral C2 proteins inhibit active autophagy to facilitate virus infection by impairing the interaction of ATG7 and ATG8

Buwei Cao1†, Linhao Ge1†, Mingzhen Zhang1, Fangfang Li1* and Xueping Zhou1,2*   

  1. 1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China;
    2. State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou 310058, China
    Buwei Cao and Linhao Ge contributed equally to this article.
    *Correspondences: Fangfang Li (lifangfang@caas.cn, Dr. Li is fully responsible for the distributions of the materials associated with this article); Xueping Zhou (zzhou@zju.edu.cn)
  • Received:2022-07-08 Accepted:2023-01-13 Online:2023-03-10 Published:2023-05-01

Abstract: Autophagy is a conserved intracellular degradation process that plays an active role in plant response to virus infections. Here we report that geminiviruses counteract activated autophagy-mediated antiviral defense in plant cells through the C2 proteins they encode. We found that, in Nicotiana benthamiana plants, tomato leaf curl Yunnan virus (TLCYnV) infection upregulated the transcription levels of autophagy-related genes (ATGs). Overexpression of NbATG5, NbATG7, or NbATG8a in N. benthamiana plants decreased TLCYnV accumulation and attenuated viral symptoms. Interestingly, transgenic overexpression of NbATG7 promoted the growth of N. benthamiana plants and enhanced plant resistance to TLCYnV. We further revealed that the C2 protein encoded by TLCYnV directly interacted with the ubiquitin-activating domain of ATG7. This interaction competitively disrupted the ATG7–ATG8 binding in N. benthamiana and Solanum lycopersicum plants, thereby inhibiting autophagy activity. Furthermore, we uncovered that the C2-mediated autophagy inhibition mechanism was conserved in three other geminiviruses. In summary, we discovered a novel counter-defensive strategy employed by geminiviruses that enlists their C2 proteins as disrupters of ATG7–ATG8 interactions to defeat antiviral autophagy.

Key words: autophagy, C2, counterdefense, geminivirus, plant defense, the ATG7–ATG8 interaction

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