Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis

Abstract

Plant species have evolved a wide variety of flowering habits, each adapted to maximize reproductive success in their local environment. Even within a species, accessions from different environments can exhibit markedly different flowering behavior. In Arabidopsis , some accessions are rapid-cycling summer annuals, whereas others accessions are late flowering and vernalization responsive and thus behave as winter annuals. Two genes, FLOWERING LOCUS C ( FLC ) and FRIGIDA ( FRI ), interact synergistically to confer the winter-annual habit. Previous work has shown that many summer-annual accessions contain null mutations in the FRI gene; thus it appears that these summer-annual accessions have arisen from winter-annual ancestors by losing FRI function. In this work we demonstrate that naturally occurring allelic variation in FLC has provided another route to the evolution of summer-annual flowering behavior in Arabidopsis . We have identified two summer-annual accessions, Da (1)-12 and Shakhdara, that contain functional alleles of FRI , but are early flowering because of weak alleles of FLC . We have also determined that the weak allele of FLC found in Landsberg erecta is naturally occurring. Unlike accessions that have arisen because of loss-of-function mutations in FRI , the FLC alleles from Da (1)-12, Shakhdara, and Landsberg erecta are not nulls; however, they exhibit lower steady-state mRNA levels than strong alleles of FLC . Sequence analysis indicates that these weak alleles of FLC have arisen independently at least twice during the course of evolution.