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 montbretiana and Arabis alpina, respectively. Recombination mapping identified two tandem A. montbretiana genes encoding MADS-domain transcription factors that confer extreme late flowering on A. alpina These genes are related to the MADS AFFECTING FLOWERING (MAF) cluster of floral repressors of other Brassicaceae species and were named A. montbretiana (Am) MAF-RELATED (MAR) genes. AmMAR1 but not AmMAR2 prevented floral induction at the shoot apex of A. alpina, strongly enhancing the effect of the MAF cluster, and MAR1 is absent from the genomes of all A. alpina accessions analyzed. Exposure of plants to cold (vernalization) represses AmMAR1 transcription and overcomes its inhibition of flowering. Assembly of the tandem arrays of MAR and MAF genes of six A. alpina accessions and three related species using PacBio long-sequence reads demonstrated that the MARs arose within the Arabis genus by interchromosomal transposition of a MAF1-like gene followed by tandem duplication. Time-resolved comparative RNA-sequencing (RNA-seq) suggested that AmMAR1 may be retained in A. montbretiana to enhance the effect of the AmMAF cluster and extend the duration of vernalization required for flowering. Our results demonstrate that MAF 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.

Highlights

  • The timing of reproduction is an adaptive trait in many organisms

  • Each line was self-fertilized and the progeny were scored for flowering time and genotyped using molecular markers designed on the basis of polymorphisms between A. alpina and A. montbretiana (Fig. 1C and Dataset S1)

  • These data indicated that IL31 and IL22 were homozygous for the locus causing late flowering, whereas IL41 was heterozygous and IL30 did not contain the locus (Fig. 1C)

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Summary

Introduction

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. Gene regulatory networks can diverge rapidly through duplication or deletion of genes that encode central regulators of phenotypic traits [13, 14] This has not been described in the context of annual and perennial species, the reduction in genome size and genomic alterations that occurred during the evolution of annual Arabidopsis thaliana. We hybridized closely related annual and perennial plants and used genetics, transgenesis, and genomics to characterize differences in the activity and function of their flowering-time genes. We identify a gene encoding a transcription factor that moved between chromosomes and is retained in the annual but absent from the perennial This gene strongly delays flowering, and we propose that it has been retained in the annual to compensate for reduced activity of closely related genes.

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