Elucidation of the ty-5 resistance network in tomato against tomato yellow leaf curl virus reveals the involvement of AP2/ERF gene

Authors: Padmanabhan, Chellappan; MA, QIYUE - Boyce Thompson Institute; Shamimuzzaman, Md; Stewart, Kevin; Wilson, Jennifer; Hasegawa, Daniel; SHEKASTE-BAND, REZA - University Of Florida; HUTTON, SAMUEL - University Of Florida; SCOTT, JOHN - University Of Florida; Simmons, Alvin; FEI, ZHANGJUN - Boyce Thompson Institute; Ling, Kai Shu

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/17/2026
Publication Date: 4/15/2026
Citation: Padmanabhan, C., Ma, Q., Shamimuzzaman, M., Stewart, K.S., Wilson, J.R., Hasegawa, D.K., Shekaste-Band, R., Hutton, S.F., Scott, J.W., Simmons, A.M., Fei, Z., Ling, K. 2026. Elucidation of the ty-5 resistance network in tomato against tomato yellow leaf curl virus reveals the involvement of AP2/ERF gene. Frontiers in Plant Science. 17:1788099. https://doi.org/10.3389/fpls.2026.1788099.
DOI: https://doi.org/10.3389/fpls.2026.1788099

Interpretive Summary: Tomato is one of the most important vegetable crops in the world. During the past three decades, significant progress has been made in developing and incorporating resistance to tomato yellow leaf curl virus (TYLCV) into cultivated tomato. However, the limited level of resistance compels the need for more robust solution against this whitefly-transmitted virus. In this study, in collaboration with academic researchers, ARS scientists conducted a global transcriptome analysis of tomato plants responding to TYLCV in the context of the recessive ty-5 resistance gene via natural whitefly transmission. Our findings reveal that two major pathways, a canonical host-disease resistance pathway and RNA-directed DNA methylation, act together in driving gene upregulation in a virus-resistant tomato line. The knowledge and methodology from this study will aid the development of tomato germplasm with enhanced and more durable resistance against whitefly-transmitted viruses.

Technical Abstract: Introduction: Tomato yellow leaf curl virus (TYLCV, Begomovirus coheni), a whitefly-transmitted begomovirus, causes serious economic losses to tomato crops globally. Over the past three decades, several genetic sources of TYLCV resistance have been identified and incorporated into tomato breeding. Among these is a recessive source of resistance known as ty-5. Methods: In this study, we conducted a global transcriptome analysis to compare gene expression in a ty-5 near isogenic tomato line and its susceptible recurrent parent at various stages of TYLCV infection. Results: We identified 1,394 differentially expressed genes, including numerous defense-related genes and genes involved in RNA-mediated DNA methylation. In addition, the expression of key regulatory genes such as protein kinases (PKs) and transcription factors (TFs) was also significantly altered. To explore the function of one upregulated TF encoding an APETALA2/Ethylene Responsive Factor (AP2/ERF), tomato plants overexpressing this gene were generated and demonstrated to confer resistance to TYLCV. Discussion: These results lead us to hypothesize that ty-5-mediated TYLCV resistance not only involves a pelota gene but is a product of two major pathways acting in concert: a typical host-disease resistance pathway and RNA-directed DNA methylation. Understanding the mechanism underlying ty-5 resistance will facilitate the development of tomato germplasm with more durable TYLCV resistance.