Transposition and duplication of MADS-domain transcription factor genes in annual and perennialArabisspecies modulates flowering

Abstract

The timing of reproduction is an adaptive trait in many organisms. In plants, the timing, duration, and intensity of flowering differ between annual and perennial species. To identify interspecies variation in these traits, we studied introgression lines derived from hybridization of annual and perennial species,Arabis montbretianaandArabis alpina, respectively. Recombination mapping identified two tandemA. montbretianagenes encoding MADS-domain transcription factors that confer extreme late flowering onA. alpina. These genes are related to theMADS AFFECTING FLOWERING(MAF) cluster of floral repressors of other Brassicaceae species and were namedA. montbretiana(Am)MAF-RELATED(MAR) genes. AmMAR1but not AmMAR2prevented floral induction at the shoot apex ofA. alpina, strongly enhancing the effect of theMAFcluster, andMAR1is absent from the genomes of allA. alpinaaccessions analyzed. Exposure of plants to cold (vernalization) repressesAmMAR1transcription and overcomes its inhibition of flowering. Assembly of the tandem arrays ofMARandMAFgenes of sixA. alpinaaccessions and three related species using PacBio long-sequence reads demonstrated that theMARs arose within theArabisgenus by interchromosomal transposition of aMAF1-likegene followed by tandem duplication. Time-resolved comparative RNA-sequencing (RNA-seq) suggested thatAmMAR1may be retained inA. montbretianato enhance the effect of theAmMAFcluster and extend the duration of vernalization required for flowering. Our results demonstrate thatMAFgenes transposed independently in different Brassicaceae lineages and suggest that they were retained to modulate adaptive flowering responses that differ even among closely related species.