A circadian repressor promotes flowering via dual repression: PtTOC suppresses the floral inhibitor PtTFL2 in Pinus tabuliformis

Abstract The Response Regulator (RR) gene family functions as a molecular “switch” in plant signal transduction, with TOC1 (PRR1) frequently acting as a transcriptional repressor that integrates both internal and external signals. While RR homologs in gymnosperms differ from those in angiosperms, research on their function remains sparse. This study presents a genome-wide analysis of the RR gene family in Pinus tabuliformis, identifying 35 RR genes that are grouped into three subfamilies: A-type ARRs (17 genes), B-type ARRs (16 genes), and pseudo-RRs (2 genes). Except for PtPRR43, these genes are distributed across various chromosomes, with 16 displaying broad expression in multiple organs. Our findings revealed that PtTOC indirectly promotes flowering by suppressing PtTFL2, a floral repressor, suggesting its role in balancing circadian rhythms and environmental signals. Additionally, PtTOC overexpression reduces cold tolerance, likely through the downregulation of cold-responsive pathways, suggesting a trade-off between promoting flowering and stress resilience. Subcellular localization analysis suggests PtTOC undergoes phosphorylation-regulated phase transitions, highlighting its dynamic role in cellular signaling and adaptation. Collectively, these results position PtTOC as a central integrator of environmental signals and circadian regulation, offering insights into strategies for enhancing reproductive performance and resilience in gymnosperms.