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Transposition and duplication of MADS-domain transcription factor genes in annual and perennial Arabis 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, 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.

SUBMITTER: Madrid E

PROVIDER: S-EPMC8488671 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Transposition and duplication of MADS-domain transcription factor genes in annual and perennial Arabis species modulates flowering.

Madrid Eva E Severing Edouard E de Ansorena Elisa E Kiefer Christiane C Brand Luise L Martinez-Gallegos Rafael R Woetzel Stefan S Kemi Ulla U Jiao Wen-Biao WB Schneeberger Korbinian K Coupland George G

Proceedings of the National Academy of Sciences of the United States of America 20210901 39

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 th ...[more]

PMID: 34548402

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Project description:Higher plants exhibit a variety of different life histories. Annual plants live for less than a year and after flowering produce seeds and senesce. By contrast perennials live for many years, dividing their life cycle into episodes of vegetative growth and flowering. Environmental cues control key check points in both life histories. Genes controlling responses to these cues exhibit natural genetic variation that has been studied most in short-lived annuals. We characterize natural genetic variation conferring differences in the perennial life cycle of Arabis alpina. Previously the accession Pajares was shown to flower after prolonged exposure to cold (vernalization) and only for a limited period before returning to vegetative growth. We describe five accessions of A. alpina that do not require vernalization to flower and flower continuously. Genetic complementation showed that these accessions carry mutant alleles at PERPETUAL FLOWERING 1 (PEP1), which encodes a MADS box transcription factor orthologous to FLOWERING LOCUS C in the annual Arabidopsis thaliana. Each accession carries a different mutation at PEP1, suggesting that such variation has arisen independently many times. Characterization of these alleles demonstrated that in most accessions, including Pajares, the PEP1 locus contains a tandem arrangement of a full length and a partial PEP1 copy, which give rise to two full-length transcripts that are differentially expressed. This complexity contrasts with the single gene present in A. thaliana and might contribute to the more complex expression pattern of PEP1 that is associated with the perennial life-cycle. Our work demonstrates that natural accessions of A. alpina exhibit distinct life histories conferred by differences in PEP1 activity, and that continuous flowering forms have arisen multiple times by inactivation of the floral repressor PEP1. Similar phenotypic variation is found in other herbaceous perennial species, and our results provide a paradigm for how characteristic perennial phenotypes might arise.

Dataset Information

Transposition and duplication of MADS-domain transcription factor genes in annual and perennial Arabis species modulates flowering.

Publications

Transposition and duplication of MADS-domain transcription factor genes in annual and perennial <i>Arabis</i> species modulates flowering.

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