Pospiviroid infection of tomato regulates the expression of genes involved in flower and fruit development

Authors: AVINA-PADILLA, KATIA - Guanajuato Campus Of Cinvestav; RIVERA-BUSTAMANTE, RAFAEL - Guanajuato Campus Of Cinvestav; Kovalskaya, Natalia; Hammond, Rosemarie

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2018
Publication Date: 9/21/2018
Citation: Avina-Padilla, K., Rivera-Bustamante, R., Kovalskaya, N.Y., Hammond, R. 2018. Pospiviroid infection of tomato regulates the expression of genes involved in flower and fruit development. Viruses. 10(10):516.

Interpretive Summary: Yield losses caused by viroids (small noncoding infectious RNAs) can reach 17-64% depending on the viroid strain and plant crop species. Viroid systemic infection in tomato is commonly associated with the expression of severe symptoms, including stunting, leaf epinasty and distortion, veinal chlorosis, reduction of flower size, flower abortion, and reduced size and numbers of fruits. Despite significant achievements in the understanding of tomato fruit development and viroid RNA biology, the mechanisms by which viroid RNAs regulate gene expression of the complex regulatory pathways involved in plant development are not fully understood. In this study, we report the differential expression of selected genes in the leaves and flowers of viroid-infected plants. Our data reveal a positive correlation between gene expression and phenotypic symptoms and further elucidates the mechanism(s) underlying the effect of viroid infection on plant development and reproductive gene expression.

Technical Abstract: Viroids are unencapsidated, single-stranded, covalently-closed circular, highly structured, noncoding RNAs of 239 – 401 nucleotides that cause disease in several economically important crop plants. In tomato, symptoms of pospiviroid infection include stunting, reduced vigor, flower abortion, and reduced size and number of fruits, resulting in significant crop losses. The dramatic alterations in plant development that are triggered by viroid infection are the result of differential gene expression patterns where many genes are up-regulated and others are down-regulated; evidence is accumulating that short RNA fragments derived from the viroid molecule (vd-sRNAs) target host gene transcripts for cleavage and result in down-regulation. In this study, we examined the effect of tomato planta macho viroid (TPMVd) and Mexican papita viroid (MPVd) infection on tomato (Solanum lycopersicum cv. Rutgers) with a focus on flower and fruit development. We analyzed changes in gene expression of SolBIGPETAL1 (bHLH transcription factor) and SolOVULEABORTION6 (proline-like tRNA synthetase), two tomato genes predicted as targets of vd-sRNAs, that are conserved in Arabidopsis and are involved in petal morphology and fertility, respectively. Expression of SolOVULEABORTION6 was down-regulated in flowers of TPMVd- and MPVd-infected plants, while expression of SolBIGPETAL1was upregulated in flowers. Up regulation of SolBIGPETAL1 and down regulation of SolOVULEABORTION6 are positively correlated with viroid-derived phenotypic symptoms such as reduced petal size and flower abortion suggesting a functional interaction between viroid RNAs and plant RNAs. In addition, expression analysis of additional genes and transcription factors further elucidates the mechanism(s) underlying the effect of viroid infection on plant development and reproductive gene expression.