Abstract
INTRODUCTION: Lonicera caerulea L. (blue honeysuckle) is a noteworthy fleshy-fruited tree and a prominent medicinal plant, which possesses notable characteristics such as exceptional resilience to winter conditions and early maturation, and the richest source of functional anthocyanins, particularly cyanidin-3-glucoside. The molecular mechanisms responsible for its freezing tolerance and anthocyanin biosynthesis remain largely unknown. OBJECTIVES: Here, a chromosome-scale genome of L. caerulea was presented, aiming to examine the genetic foundations that underlie these characteristics of blue honeysuckle. METHODS: The PacBio HiFi reads and Hi-C data were used to construct high-quality genome of blue honeysuckle. Comparative genomic and transcriptomic analyses were conducted to elucidate the molecular mechanisms of freezing tolerance and anthocyanin biosynthesis. RESULTS: Comparative genomics analysis between L. caerulea and L. japonica revealed that the dynamic changes of duplicated genes contributed to their phytochemical reconstruction and environmental adaptation. Moreover, the ABA and ICE-CBF-COR signaling pathways were closely correlated to the freezing tolerance of L. caerulea. Genome-wide identification and biochemical function indicated that three anthocyanin 3',5'-O-methyltransferases (LcOMT2, LcOMT14, and LcOMT20) and two 3'-O-glycosyltransferases (LcUGT78X1 and LcUGT95P1) were responsible for anthocyanin biosynthesis. In addition, LcUGT78X1 was regarded as the potent glycosyltransferase for the accumulation of cyanidin-3-glucoside in L. caerulea. CONCLUSION: This research elucidates the crucial roles of the ABA and ICE-CBF-COR signaling pathways in enhancing freezing tolerance, while also identifying highly efficient anthocyanin biosynthetic enzymes in L. caerulea. These findings advance the understanding of environmental adaptation and phytochemical production in Lonicera species.