Plant virology in the 21st century in China: Recent advances and future directions

Abstract

Plant viruses are a group of intracellular pathogens that persistently threaten global food security. Significant advances in plant virology have been achieved by Chinese scientists over the last 20 years, including basic research and technologies for preventing and controlling plant viral diseases. Here, we review these milestones and advances, including the identification of new crop-infecting viruses, dissection of pathogenic mechanisms of multiple viruses, examination of multilayered interactions among viruses, their host plants, and virus-transmitting arthropod vectors, and in-depth interrogation of plant-encoded resistance and susceptibility determinants. Notably, various plant virus-based vectors have also been successfully developed for gene function studies and target gene expression in plants. We also recommend future plant virology studies in China.

Key words： China; emerging plant viruses; plant virology; plant resistance/susceptibility to viral infection; plant‒virus transmission vector interactions; plant virus-based vectors; viral pathogenesis

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362 Zhang, K., Zhuang, X., Dong, Z., Xu, K., Chen, X., Liu, F., and He, Z. (2021a). The dynamics of N6-methyladenine RNA modification in interactions between rice and plant viruses. Genome Biol. 22: 189.

363 Zhang, L., Liu, W., Wu, N., Wang, H., Zhang, Z., Liu, Y., and Wang, X. (2023c). Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect. PLoS Pathog. 19: e1011134.

364 Zhang, L., Wang, S., Ruan, S., Nzabanita, C., Wang, Y., and Guo, L. (2023d). A mycovirus VIGS vector confers hypovirulence to a plant pathogenic fungus to control wheat FHB. Adv. Sci. 10: e2302606.

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366 Zhang, R., Zhang, X.F., Chi, Y., Xu, Y., Chen, H., Guo, Z., and Wei, T. (2022a). Nucleoprotein of a rice rhabdovirus serves as the effector to attenuate hemolymph melanization and facilitate viral persistent propagation in its leafhopper vector. Front. Immunol. 13: 904244.

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371 Zhang, X., Peng, Y., Xiang, H., Wang, Y., Li, D., Yu, J., and Han, C. (2022c). Incidence and prevalence levels of three aphid-transmitted viruses in crucifer crops in China. J. Integr. Agric. 21: 774-780.

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373 Zhang, X., Wang, D., Zhao, P., Sun, Y., Fang, R.X., and Ye, J. (2023g). Near-infrared light and PIF4 promote plant antiviral defense by enhancing RNA interference. Plant Commun. 30: 100644.

374 Zhang, X., Wang, X., Xu, K., Jiang, Z., Dong, K., Xie, X., Zhang, H., Yue, N., Zhang, Y., Wang, X.B., et al. (2021b). The serine/threonine/tyrosine kinase STY46 defends against hordeivirus infection by phosphorylating γb protein. Plant Physiol. 186: 715-730.

375 Zhang, X.F., Zhang, S.Y., Guo, Q., Sun, R., Wei, T.Y., and Qu, F. (2018b). A new mechanistic model for viral cross protection and superinfection exclusion. Front. Plant Sci. 9: 40.

376 Zhang, X.P., Liu, D.S., Yan, T., Fang, X.D., Dong, K., Xu, J., Wang, Y., Yu, J.L., and Wang, X.B. (2017b). Cucumber mosaic virus coat protein modulates the accumulation of 2b protein and antiviral silencing that causes symptom recovery in planta. PLoS Pathog. 13: e1006522.

377 Zhang, X.Y., Xiang, H.Y., Zhou, C.J., Li, D.W., Yu, J.-L., and Han, C.G. (2014a). Complete genome sequence analysis identifies a new genotype of brassica yellows virus that infects cabbage and radish in China. Arch. Virol. 159: 2177-2180.

378 Zhang, Y., Li, B.X., Mao, Q.Z., Zhuo, J.C., Huang, H.J., Lu, J.B., Zhang, C.X., Li, J.M., Chen, J.P., and Lu, G. (2023h). The JAK-STAT pathway promotes persistent viral infection by activating apoptosis in insect vectors. PLoS Pathog. 19: e1011266.

379 Zhang, Y., Li, J., Pu, H., Jin, J., Zhang, X., Chen, M., Wang, B., Han, C., Yu, J., and Li, D. (2010b). Development of Tobacco necrosis virus A as a vector for efficient and stable expression of FMDV VP1 peptides. Plant Biotechnol. J. 8: 506-523.

380 Zhang, Y., and Zeng, L. (2020). Crosstalk between ubiquitination and other post-translational protein modifications in plant immunity. Plant Commun. 1: 100041.

381 Zhang, Y.H., Li, Z.X., Du, Y.J., Li, S.F., and Zhang, Z.X. (2023i). A universal probe for simultaneous detection of six pospiviroids and natural infection of potato spindle tuber viroid (PSTVd) in tomato in China. J. Integr. Agric. 22: 790-798.

382 Zhang, Z., Chen, H., Huang, X., Xia, R., Zhao, Q., Lai, J., Teng, K., Li, Y., Liang, L., Du, Q., et al. (2011). BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23: 273-288.

383 Zhang, Z., Wang, D., Yu, C., Wang, Z., Dong, J., Shi, K., and Yuan, X. (2016c). Identification of three new isolates of tomato spotted wilt virus from different hosts in China: Molecular diversity, phylogenetic and recombination analyses. Virol. J. 13: 8.

384 Zhang, Z.J., Gao, Q., Fang, X.D., Ding, Z.H., Gao, D.M., Xu, W.Y., Cao, Q., Qiao, J.H., Yang, Y.Z., Han, C.G., et al. (2020d). CCR4, a RNA decay factor, is hijacked by a plant cytorhabdovirus phosphoprotein to facilitate virus replication. eLife 9: e53753.

385 Zhang, Z.X., Qi, S.S., Tang, N., Zhang, X.X., Chen, S.S., Zhu, P.F., Ma, L., Cheng, J.P., Xu, Y., Lu, M.G., et al. (2014b). Discovery of replicating circular RNAs by RNA-Seq and computational algorithms. PLoS Pathog. 10: e1004553.

386 Zhao, J., Liu, Q., Zhang, H., Jia, Q., Hong, Y., and Liu, Y. (2013a). The Rubisco small subunit is involved in tobamovirus movement and Tm-2²-mediated extreme resistance. Plant Physiol. 161: 374-383.

387 Zhao, P., Yao, X., Cai, C., Li, R., Du, J., Sun, Y., Wang, M., Zou, Z., Wang, Q., Kliebenstein, D.J., et al. (2019). Viruses mobilize plant immunity to deter nonvector insect herbivores. Sci. Adv. 5: eaav9801.

388 Zhao, R.N., Wang, R., Wang, N., Fan, Z.F., Zhou, T., Shi, Y.C., and Chai, M. (2013b). First Report of Tomato chlorosis virus in China. Plant Dis. 97: 1123.

389 Zhao, S., Gong, P., Liu, J., Liu, H., Lozano-Durán, R., Zhou, X., and Li, F. (2023). Geminivirus C5 proteins mediate formation of virus complexes at plasmodesmata for viral intercellular movement. Plant Physiol. 193: 322-338.

390 Zhao, S., Gong, P., Ren, Y., Liu, H., Li, H., Li, F., and Zhou, X. (2022a). The novel C5 protein from tomato yellow leaf curl virus is a virulence factor and suppressor of gene silencing. Stress Biol. 2: 19.

391 Zhao, S., Hong, W., Wu, J., Wang, Y., Ji, S., Zhu, S., Wei, C., Zhang, J., and Li, Y. (2017). A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. eLife 6: e27529.

392 Zhao, S., and Li, Y. (2021). Current understanding of the interplays between host hormones and plant viral infections. PLoS Pathog. 17: e1009242.

393 Zhao, W., Li, Q., Sun, M., Xiao, Y., and Cui, F. (2022b). Interaction between endogenous microRNAs and virus-derived small RNAs controls viral replication in insect vectors. PLoS Pathog. 18: e1010709.

394 Zhao, W., Lu, L., Yang, P., Cui, N., Kang, L., and Cui, F. (2016). Organ-specific transcriptome response of the small brown planthopper toward rice stripe virus. Insect Biochem. Mol. Biol. 70: 60-72.

395 Zhao, W., Xu, Z., Zhang, X., Yang, M., Kang, L., Liu, R., and Cui, F. (2018). Genomic variations in the 3′-termini of Rice stripe virus in the rotation between vector insect and host plant. New Phytol. 219: 1085-1096.

396 Zhao, W., Yu, J., Jiang, F., Wang, W., Kang, L., and Cui, F. (2021). Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors. PLoS Pathog. 17: e1009424.

397 Zhao, W., Zhu, J., Lu, H., Zhu, J., Jiang, F., Wang, W., Luo, L., Kang, L., and Cui, F. (2022c). The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication. Protein Cell 13: 360-378.

398 Zhao, X., Wang, X., Dong, K., Zhang, Y., Hu, Y., Zhang, X., Chen, Y., Wang, X., Han, C., Yu, J., et al. (2015). Phosphorylation of Beet black scorch virus coat protein by PKA is required for assembly and stability of virus particles. Sci. Rep. 5: 11585.

399 Zhao, Y., Cao, X., Zhong, W., Zhou, S., Li, Z., An, H., Liu, X., Wu, R., Bohora, S., Wu, Y., et al. (2022d). A viral protein orchestrates rice ethylene signaling to coordinate viral infection and insect vector-mediated transmission. Mol. Plant 15: 689-705.

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401 Zheng, X., Wu, M., Li, X., Cao, J., Li, J., Wang, J., Huang, S., Liu, Y., and Wang, Y. (2019). Actin filaments are dispensable for bulk autophagy in plants. Autophagy 15: 2126-2141.

402 Zhong, X., Wang, Z.Q., Xiao, R., Cao, L., Wang, Y., Xie, Y., and Zhou, X. (2017). Mimic phosphorylation of a βC1 protein encoded by TYLCCNB impairs its functions as a viral suppressor of RNA silencing and a symptom determinant. J. Virol. 91: 300-317.

403 Zhou, B., and Zeng, L. (2017). Conventional and unconventional ubiquitination in plant immunity. Mol. Plant Pathol. 18: 1313-1330.

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406 Zhou, G., Zhang, S., Zou, S., Xu, Z., and Zhou, Z. (2010b). Occurrence and damage analysis of a new rice dwarf disease caused by Southern rice black-streaked dwarf virus. Plant Prot. 36: 144-146.

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408 Zhou, S., Hong, Q., Li, Y., Li, Q., and Wang, M. (2018). Autophagy contributes to regulate the ROS levels and PCD progress in TMV-infected tomatoes. Plant Sci. 269: 12-19.

409 Zhou, X. (2013). Advances in understanding begomovirus satellites. Annu. Rev. Phytopathol. 51: 357-381.

410 Zhou, X., Lin, W., Sun, K., Wang, S., Zhou, X., Jackson, A.O., and Li, Z. (2019a). Specificity of plant rhabdovirus cell-to-cell movement. J. Virol. 93: e00296-00219.

411 Zhou, X., Sun, K., Zhou, X., Jackson, A.O., and Li, Z. (2019b). The matrix protein of a plant rhabdovirus mediates superinfection exclusion by inhibiting viral transcription. J. Virol. 93: e00680-00619.

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