The tomato yellow leaf curl virus C4 protein alters the expression of plant developmental genes correlating to leaf upward cupping phenotype in tomato

Authors: Padmanabhan, Chellappan; ZHENG, YI - Boyce Thompson Institute; Shamimuzzaman, Md - Shamim; Wilson, Jennifer - Jenny; Gilliard, Andrea; FEI, ZHANGJUN - Boyce Thompson Institute; Ling, Kai-Shu

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/13/2022
Publication Date: 5/12/2022
Citation: Padmanabhan, C., Zheng, Y., Shamimuzzaman, M., Fei, Z., Ling, K. 2022. The tomato yellow leaf curl virus C4 protein alters the expression of plant developmental genes correlating to leaf upward cupping phenotype in tomato. PLOS ONE. 17(5):e0257936. https://doi.org/10.1371/journal.pone.0257936.
DOI: https://doi.org/10.1371/journal.pone.0257936

Interpretive Summary: Tomato (Solanum lycopersicum L.) is one of the most economically important vegetable crops widely grown in the world. Viral diseases are a major factor limiting tomato production. Tomato yellow leaf curl virus (TYLCV), a whitefly (Bemisia tabaci)-transmitted begomovirus, has caused serious economic losses to tomato production worldwide. The C4 is a relatively conserved protein, which may display diverse biological functions in monopartite and bipartite geminiviruses. However, it is still unclear as to the function of C4 as a pathogenicity determinant of TYLCV or how it may regulate gene expression in tomato plants. In this study, Scientists at the USDA-ARS in Charleston, SC in collaboration with Boyce Thompson Institute investigated the functional role of TYLCV-encoded C4 protein by generating transgenic tomato plants over-expressing the TYLCV C4 gene, which showed plant stunting and dramatic leaf upward cupping, resembling the symptoms in field tomato plants naturally infected by TYLCV. We further investigated the differential gene expression and their associated gene networks in transgenic tomato plants using RNA sequencing. Comparative transcriptome analysis revealed 241 differentially expressed genes. Our analysis revealed that the C4 protein of TYLCV interferes in expression of transcription factors that are crucial for leaf development, resulting in leaf upward cupping phenotype in the TYLCV-infected tomato plants. A basic understanding of the virus-encoded virulent factor and host response is important as it may lead to the development of an effective strategy to control this and other devastating diseases.

Technical Abstract: Tomato yellow leaf curl virus (TYLCV), a monopartite begomovirus in the family Geminiviridae, is efficiently transmitted by the whitefly (Bemisia tabaci) and causes serious economic losses to tomato crops around the world. The TYLCV-infected tomato plants develop distinctive symptoms of yellowing and leaf upper cupping phenotype. However, the molecular mechanism leading to those disease symptoms has not been well characterized. In the present study, we characterized the TYLCV C4 protein function by generating stably transformed C4 transgenic tomato plants. Interestingly, the C4 transgenic tomato plants displayed an upward leaf curling and plant stunting phenotype that is similar to the disease symptom as observed on tomato plants naturally infected by TYLCV. We further compared transcriptome profiles between the transgenic C4 plants and the transgenic GFP control plants, and identified a total of 241 differentially expressed genes (DEGs). Interestingly, expression of several leaf developmental transcription factors (TFs), including NAC/NAM, MADS box, LOB, MYB and BZIP, was altered. This TF alteration might have led to the development of leaf curl phenotype observed on the transgenic C4 plants. These results provide direct evidence that the unique virus-encoded protein C4 causes leaf yellowing and upward cupping phenotype upon TYLCV infection.