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Geminivirus satellite-encoded βC1 activates UPR, induces bZIP60 nuclear export, and manipulates the expression of bZIP60 downstream genes to benefit virus infection

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Abstract

UPR is a conserved response in eukaryotes and can alleviate endoplasmic reticulum (ER) stresses induced by abiotic and biotic stresses. The interactions between UPR and plant RNA viruses have been documented, while the interplays between UPR and plant DNA viruses remain unknown. Using tomato yellow leaf curl China virus (TYLCCNV) and its associated betasatellite (TYLCCNB) as a model, we indicate that TYLCCNB βC1 is a major inducer of UPR and can upregulate the expression of bZIP60, a transcription factor in Nicotiana benthamiana plants. Treatment using ER stress inducers or overexpression of NbbZIP60 increases βC1 accumulation and benefits TYLCCNV/TYLCCNB infection in N. benthamiana plants, and vice versa. In the TYLCCNV/TYLCCNB-infected or the βC1-expressing cells, NbbZIP60 is exported from the nucleus to the nuclear periphery via the XPO1 pathway, and blocking the XPO1 pathway inhibited TYLCCNV/TYLCCNB infection. We have found that the NbbZIP60-regulated pro-survival genes could promote virus infection, and the pro-death gene plays a contrasting role in virus infection. This study reveals that geminivirus infection activates UPR and utilizes the up-regulated molecular chaperons to promote viral infection, and then induces the nuclear export of NbbZIP60 to evade plant defense response, which is a distinct virulence strategy exploited by plant pathogens.

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2021YFD1400400) and the National Natural Science Foundation of China (32172385, 31930089). We thank Dr. Xinshun Ding for his valuable suggestions and the English editing of the manuscript. We thank Dr. Yule Liu (Tsinghua University, China) for providing the TRV VIGS vector and Dr. Jianxiang Wu (Zhejiang University, China) for providing the anti-βC1 antibody. We thank Dr. Michael M. Goodin (University of Kentucky, United States) for seeds of the RFP-H2B transgenic line (Dutch and Whitfield, 2021; Verchot et al., 2021).

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Authors and Affiliations

  1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Mingzhen Zhang, Buwei Cao, Xueping Zhou & Fangfang Li

  2. State Key Laboratory of Agro-Biotechnology and Key Laboratory of Pest Monitoring and Green Management-MARA, China Agricultural University, Beijing, 100193, China

    Mingzhen Zhang & Zaifeng Fan

  3. Horticultural Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, 201403, China

    Hui Zhang

  4. State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Xueping Zhou

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  1. Mingzhen Zhang
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Correspondence to Xueping Zhou or Fangfang Li.

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Zhang, M., Cao, B., Zhang, H. et al. Geminivirus satellite-encoded βC1 activates UPR, induces bZIP60 nuclear export, and manipulates the expression of bZIP60 downstream genes to benefit virus infection. Sci. China Life Sci. 66, 1408–1425 (2023). https://doi.org/10.1007/s11427-022-2196-y

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