Genome-wide expression atlas of tomato flower buds revealed the SllncERF162 - SlERF162 module associated with basal thermotolerance

Abstract High temperatures impair pollen viability and reduce fruit set, ultimately affecting the yield of crops. Understanding the genetic components involved in the heat stress (HS) response is essential for developing climate-resilient crop varieties. However, the regulatory mechanisms governing HS responses during pollen development in tomato (Solanum lycopersicum) remain unexplored. In this study, we identified the microspore mother cell stage as the most heat-sensitive phase in tomato pollen development. Furthermore, we generated a comprehensive RNA expression profile of tomato flower buds under HS, encompassing 8051 mRNAs, 5738 lncRNAs, 62 circRNAs, and 24 miRNAs. Comparative analysis of these RNAs revealed three distinct response phases, early, late, and dual, and enabled the identification of coexpression modules comprising both coding and noncoding transcripts. Among these, SlERF162 was identified as a key regulatory gene that promotes pollen thermotolerance. We further identified the lncRNA TCONS_00023929 (designated SllncERF162) as a positive regulator of SlERF162 expression. Both SlERF162 and SllncERF162 contributed to maintaining pollen viability under HS. Additional experiments demonstrated that the SllncERF162–SlERF162 regulatory module enhances basal thermotolerance by directly targeting and activating the heat-responsive genes SlHsfB1 and SlsHSP. Overall, this study provides a high-resolution expression atlas of RNAs under HS and uncovers a novel noncoding RNA-mediated regulatory network that promotes thermotolerance during tomato pollen development.