Dynamic evolution of FLC/MAF-like genes accompanying Brassicaceae radiation

Understanding the molecular basis of rapid species radiation remains challenging in evolutionary biology. In angiosperms, Brassicaceae exemplifies rapid radiation following the At-α whole-genome duplication (At-α WGD) event ∼35 million years ago (Mya). However, the molecular features associated with the early Brassicaceae radiation have not been fully elucidated, particularly due to lack of high-quality genomes from the super-tribe Hesperodae (clade E).

Utilizing recently released genomes from Arabodae (clade D) and Hesperodae (clade E), along with 36 additional Brassicaceae species representing all super-tribes of Brassicoideae and Aethionemoideae, we performed phylogenomic analyses to identify patterns of gene family expansion and contraction at key nodes during early radiation. We further investigated genomic synteny and gene expression, with a particular focus on the dynamic expansion of the FLOWERING LOCUS C/MADS-AFFECTING FLOWERING (FLC/MAF) gene family in response to artificial temperature fluctuations.

Dating back to the Oligocene-Miocene transition and following the uplift of the Qinghai-Tibet Plateau, Brassicaceae underwent significant radiation with ∼540 expanded gene families, in which 66 genes were involved in flowering time regulation. FLC was first duplicated via the At-α WGD into MAF2/3, which is present in Brassicaceae. Subsequent tandem duplications gave rise to MAF4/5 in core Brassicaceae. Additional random duplications led to FLOWERING LOCUS M (FLM or MAF1) in certain species of the Camelinodae (clade A). These duplicated MAFs exhibit significant diversified expression patterns under turbulent temperature conditions.

Our analyses reveal a dynamic, Brassicaceae-specific retention and expansion of FLC/MAFs along with other flowering time regulators during species radiation and historical environmental adaptation, highlighting the role of flowering diversity in Brassicaceae radiation. This work thus provides a valuable model for studying species evolution and diversification in other angiosperm families.