InDel variation and contraction of the C-repeat binding factor family contribute to cold sensitivity in Betula fujianensis

Abstract Betula species exhibit exceptional cold tolerance, yet the evolutionary drivers of their cold adaptation remain unclear. Betula fujianensis, a subtropical member of this genus, is an ideal model to investigate the evolution of cold adaptation. Here, we present a nearly telomere-to-telomere genome assembly and identify a 10-fold reduction in nucleotide diversity in the extant B. fujianensis population compared to its temperate relatives (Betula pendula and Betula platyphylla). This decrease in nucleotide diversity was driven by 2 historical population declines during global cooling periods. B. fujianensis exhibits heightened sensitivity to low temperatures, associated with a contracted C-repeat binding factor (CBF) gene family and a 185 bp insertion in the DREB and EAR motif protein 1 (DEAR1) promoter, which enhances its expression. We demonstrate that DEAR1 is a negative regulator of CBF expression in a negative feedback loop. Collectively, our results identify the DEAR1–CBF interplay as an important regulatory module for cold adaptation. Our findings shed light on plant cold adaptation mechanisms and provide critical genomic resources to guide conservation strategies for this climate-vulnerable species under global climate change.