PEP1 of Arabis alpina Is Encoded by Two Overlapping Genes That Contribute to Natural Genetic Variation in Perennial Flowering

Abstract

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.

Divergence of annual and perennial species in the Brassicaceae and the contribution of cis‐acting variation at FLC orthologues

“…2009; Albani et al . 2012). Therefore, a mechanistic link might exist between complexity of the FLC / PEP1 gene and life history.…”

“…Pajares was the most complex locus incorporating a partial duplication that includes exon 1 and generates two overlapping transcripts (Albani et al . 2012). Furthermore, AmFLC and AiFLC from annual A. montbretiana and A. nova subsp.…”

“…2009; Albani et al . 2012). The FLC orthologues of annuals A. montbretiana and A. auriculata were also found to be stably repressed after vernalization, similar to the pattern of expression of FLC found in A. thaliana and contrasting with the perennial pattern of PEP1 regulation in A. alpina and A. nordmanniana .…”

“…PEP1 has a more complex structure than FLC , so that the first exon is duplicated in tandem along with the proximal promoter and part of the first intron giving rise to two overlapping transcripts (Albani et al . 2012). In perennial Arabidopsis lyrata, the FLC locus is tandemly duplicated, while in perennial Arabidopsis arenosa, it is partially triplicated (Nah & Chen 2010).…”

Winter Memory throughout the Plant Kingdom: Different Paths to Flowering

“…1C; Wang et al, 2009bWang et al, , 2011a. As the gene name suggests, pep1 mutants flower rapidly without vernalization, and allelic variation at PEP1 contributes to the natural variation in flowering responses that exists among different accessions of A. alpina (Wang et al, 2009b;Albani et al, 2012). Unlike FLC in Arabidopsis, the expression of PEP1 is only transiently repressed by cold, and the meristems that transition to flowering during cold become inflorescences, whereas meristems at an immature stage remain vegetative (Wang et al, 2009b).…”