Transposition and duplication of MADS-domain transcription factor genes in annual and perennial <i>Arabis</i> species 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, <i>Arabis montbretiana</i> and <i>Arabis alpina</i>, respectively. Recombination mapping identified two tandem <i>A. montbretiana</i> genes encoding MADS-domain transcription factors that confer extreme late flowering on <i>A. alpina</i> These genes are related to the <i>MADS AFFECTING FLOWERING</i> (<i>MAF</i>) cluster of floral repressors of other Brassicaceae species and were named <i>A. montbretiana</i> (Am) <i>MAF-RELATED</i> (<i>MAR</i>) genes. Am<i>MAR1</i> but not Am<i>MAR2</i> prevented floral induction at the shoot apex of <i>A. alpina</i>, strongly enhancing the effect of the <i>MAF</i> cluster, and <i>MAR1</i> is absent from the genomes of all <i>A. alpina</i> accessions analyzed. Exposure of plants to cold (vernalization) represses <i>AmMAR1</i> transcription and overcomes its inhibition of flowering. Assembly of the tandem arrays of <i>MAR</i> and <i>MAF</i> genes of six <i>A. alpina</i> accessions and three related species using PacBio long-sequence reads demonstrated that the <i>MAR</i>s arose within the <i>Arabis</i> genus by interchromosomal transposition of a <i>MAF1-like</i> gene followed by tandem duplication. Time-resolved comparative RNA-sequencing (RNA-seq) suggested that <i>AmMAR1</i> may be retained in <i>A. montbretiana</i> to enhance the effect of the <i>AmMAF</i> cluster and extend the duration of vernalization required for flowering. Our results demonstrate that <i>MAF</i> genes transposed independently in different Brassicaceae lineages and suggest that they were retained to modulate adaptive flowering responses that differ even among closely related species.