The genome assembly of Chimonanthus praecox var. concolor and comparative genomic analysis highlight the genetic basis underlying conserved and variable floral traits of wintersweet

Wintersweet (Chimonanthus praecox), a classical winter-blooming magnoliids species with great aesthetic value highlighting the on the brilliant yellow flower and pleasant floral aroma, possesses diverse varieties mainly classified in three groups (Concolor, Patens, and Rubrum group) with the most striking variation in the tepal color. The recent release of the genome in two wintersweet varieties belonging to Patens and Rubrum group successfully elucidated the molecular mechanisms underlying some ornamental traits highlighting the flowering time, floral scent and tepal color. In this study, the chromosome-scale genome of C. praecox var. concolor was assembled to further verify the placement of magnoliids and exploit the genetic variation underscoring the diverse flowering traits among different wintersweet groups. Phylogenomic analyses placed magnoliids including C. praecox var. concolor as the sister to eudicots. The C. praecox var. concolor’s genome experienced two rounds of whole genome duplication (WGD). Multiple gene families involved in floral development including ANR1 and PI genes were retained and expanded during these WGD events. The expansion and expression pattern of SVP and FUL genes suggest their pivotal role in unique character of winter-flowering. With the pleasant fragrance as the aesthetic characteristics, linalool and benzyl acetate were identified as the top abundant constituents in the floral scent of Concolor wintersweet. Integrating metabolic, genomic, and transcriptomic analyses with enzyme assays led to the identification of CpTPS3 (CpLIS) and CpBAHD2 (CpBEAT), which are responsible for the biosynthesis of linalool and benzyl acetate, respectively, in the Concolor variety. Taken together, the assembled genome of C. praecox var. concolor enables the comparative analysis of the genetic basis underlying both conserved and variable floral traits and provides a useful foundation for variety improvements by molecular breeding in wintersweet.