Insights into the transcriptional reprogramming in tomato response to PSTVd variants using network approaches

Authors: AVINA-PADILLA, KATIA - Guanajuato Campus Of Cinvestav; ZAMBADA-MORENO, OCTAVIO - Guanajuato Campus Of Cinvestav; HERRERA-OROPEZA, GABRIEL EMILIO - King'S College; JIMENEZ-LIMAS, MARCO ANTONIO - Universidad Autonoma De Ciudad Juarez; Abrahamian, Peter; Hammond, Rosemarie; HERNANDEZ-ROSALES, MARIBEL - Guanajuato Campus Of Cinvestav

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/21/2022
Publication Date: 5/26/2022
Citation: Avina-Padilla, K., Zambada-Moreno, O., Herrera-Oropeza, G., Jimenez-Limas, M., Abrahamian, P., Hammond, R., Hernandez-Rosales, M. 2022. Insights into the transcriptional reprogramming in tomato response to PSTVd variants using network approaches. International Journal of Molecular Sciences. 23:5983. https://doi.org/10.3390/ijms23115983.
DOI: https://doi.org/10.3390/ijms23115983

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, using an omics approach, we identified specific master transcription regulators that regulate genes involved in critical signaling pathways affecting biological processes linked to metabolism and plant defense in viroid-infected plants. Our results provide a foundation for further research on viroid/host genome interactions to elucidate the mechanism(s) underlying the effect of viroid infection on plant development and reproductive gene expression and for the development of novel disease control measures.

Technical Abstract: Viroids are the smallest pathogens of angiosperms, consisting of non-coding RNAs that cause severe diseases in agronomic crops. Symptoms associated with viroid infection are linked to developmental alterations due to genetic regulation. To understand the global mechanisms of host viroid response, we implemented network approaches to identify master transcription regulators and their differentially expressed targets in tomato infected with mild and severe variants of PSTVd. Our approach integrates root and leaf transcriptomic data, gene regulatory network analysis, and identification of affected biological processes. Our results reveal that specific bHLH, MYB, and ERF transcription factors regulate genes involved in molecular mechanisms underlying critical signaling pathways. Functional enrichment of regulons shows that bHLH-MTRs are linked to metabolism and plant defense, while MYB-MTRs are involved in signaling regulation and hormone-related processes. Strikingly, a member of the bHLH-TF family has a specific potential role as a microprotein involved in the post-translational regulation of hormone signaling events. We found that ERF-MTRs are characteristic of severe symptoms, while ZNF-TF, tf3a-TF, BZIP-TFs, and NAC-TF act as unique MTRs. Altogether, our results lay a foundation for further research on the PSTVd and host genome interaction, providing evidence for identifying potential key genes that influence symptoms during development in tomato plants.