Evolutionary Reconstruction of Hormone-bHLH Regulatory Networks in Solanaceae: Phylogenomic Insights from PSTVd-Tomato Interactions

Abstract

The evolutionary reconstruction of transcriptional regulatory networks play a crucial role in plant adaptation to biotic stress. In Solanaceae, basic helix-loop-helix (bHLH) transcription factors (TFs) regulate hormone signaling pathways that balance growth and defense responses. In this study, we investigated the phylogenomic evolution of bHLH-mediated hormone networks in response to Potato Spindle Tuber Viroid (PSTVd) infection in tomato (Solanum lycopersicum) and its wild relatives. Among them, the JA-associated bHLH Solyc08g076930, IA3/MYC2 exhibits strong evolutionary conservation across Solanaceae, whereas the auxin regulator Solyc03g113560 miP-bHLH-ARF8 is a tomato-specific gene raising from an ancestral duplication, indicating neofunctionalization. Under PSTVd infection, we observe extensive regulatory rewiring, with bHLH hubs assuming dominant control over target genes typically regulated by multiple TFs in healthy conditions. The JA regulon undergoes the most pronounced shift, with Solyc08g076930 directly regulating 91 genes, compared to shared regulation with over a thousand TFs in healthy plants. This rewiring reflects the adaptive plasticity of bHLH TFs in coordinating stress responses through hormonal crosstalk. These findings reveal key evolutionary pressures shaping Solanaceae stress responses, offering insights for improving viroid tolerance and crop resilience.