C4, the Pathogenic Determinant of Tomato Leaf Curl Guangdong Virus, May Suppress Post-transcriptional Gene Silencing by Interacting With BAM1 Protein.

Xiaomei Wang,Xiaoman She,Yanhua Zhu,Zifu He,Zhenggang Li,Zhenguo Du,Lin Yu,Guobing Lan,Yafei Tang

doi:10.3389/fmicb.2020.00851

Xiaomei Wang, Xiaoman She + Show 7 more

Open Access

https://doi.org/10.3389/fmicb.2020.00851

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Abstract

Tomato leaf curl Guangdong virus (ToLCGdV) is a begomovirus associated with a Tomato yellow leaf curl disease (TYLCD) epidemic in Guangdong province, China. Being the least conserved protein among geminivirus proteins, the function of C4 during ToLCGdV infection has not been elucidated. In this study, the infectious clones of ToLCGdV and a ToLCGdV mutant (ToLCGdVmC4) with disrupted C4 ORF were constructed. Although ToLCGdV and ToLCGdVmC4 could infect Nicotiana benthamiana and tomato plants, ToLCGdVmC4 elicited much milder symptoms compared with ToLCGdV. To further verify the role of C4 in viral pathogenesis, C4 was expressed in N. benthamiana from Potato virus X (PVX) vector. The results showed that ToLCGdV C4 enhanced the pathogenicity of PVX and induced more severe developmental abnormalities in plants compared with PVX alone or PVX-mC4. In addition, ToLCGdV C4 suppresses systemic gene silencing in the transgenic N. benthamiana line 16c, but not local gene silencing induced by sense GFP in wild-type N. benthamiana plants. Moreover, C4 suppresses transcriptional gene silencing (TGS) by reducing the DNA methylation level of 35S promoter in 16c-TGS N. benthamiana plants. Furthermore, C4 could also interact with the receptor-like kinase (RLK) BARELY ANY MERISTEM 1 (BAM1), suggesting that C4 may suppress gene silencing by interfering with the function of BAM1 in the cell-to-cell spread of RNAi. All these results suggest that C4 is a pathogenic determinant of ToLCGdV, and C4 may suppress post-transcriptional gene silencing (PTGS) by interacting with BAM1.

Highlights

Geminiviridae constitutes a large family of plant viruses with small, single-stranded and circular DNA genomes encompassed within characteristic twinned icosahedral particles (HanleyBowdoin et al, 1999; Fauquet et al, 2008)
Phylogenetic analysis shows that Tomato leaf curl Guangdong virus (ToLCGdV) C4 shares the highest amino acids similarity (92.94%) with AC4 of Euphorbia leaf curl virus (EuLCuV) (Figure 1B), an Euphorbia pulcherrima-infecting monopartite begomovirus firstly identified in China (Ma et al, 2004)
ToLCGdV C4 is close to AC4 proteins encoded by other weed-infecting begomoviruses like Asystasia begomovirus 2 (ABgV2), Allamanda leaf curl virus (AllLCV), and Pouzolzia mosaic Guangdong virus (PouMGDV) (Figure 1B)

Summary

Introduction

Geminiviridae constitutes a large family of plant viruses with small, single-stranded and circular DNA (sscDNA) genomes encompassed within characteristic twinned icosahedral particles (HanleyBowdoin et al, 1999; Fauquet et al, 2008). The DNA B component of bipartite begomovirus encodes two proteins, the nuclear shuttle protein (NSP, ORF BV1) on the virion-sense strand and the movement protein (MP, ORF BC1) on the complementary-sense strand (Hanley-Bowdoin et al, 1999). For both DNA A and DNA B, the bidirectionally arranged ORFs are separated by a long intergenic region (IR) which carries key elements for initiating viral replication and transcription (Hanley-Bowdoin et al, 1999). An increasing number of monopartite begomoviruses have been found to require betasatellites for successful infection and symptom induction in some host plants (Zhou, 2013; Yang et al, 2019)

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