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, FLOW-ERING 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.FRIGIDA ͉ vernalization ͉ winter annual ͉ natural variation I dentification of the genetic mechanisms that underlie differences in life history is key to understanding the evolution of adaptive traits. Many plants species occur over a wide range of latitudes, and within a species, accessions from different regions can differ substantially in flowering behavior (1). As an adaptation to seasonal fluctuations in temperature experienced in temperate climates, flowering in many species is promoted by prolonged exposure to cold temperatures (vernalization) (2). Many accessions of Arabidopsis from temperate climates are relatively late flowering unless vernalized (3). This vernalization requirement prevents flowering before winter and promotes rapid flowering in the spring, and thus these accessions behave as winter annuals. Summer-annual Arabidopsis accessions, in contrast, flower rapidly in the absence of vernalization, and these accessions predominate in warmer climates that do not experience the cold temperatures required for vernalization (3).The late-flowering phenotype of winter-annual accessions of Arabidopsis is created by the interaction of two genes, FLOW-ERING LOCUS C (FLC) and FRIGIDA (FRI) (2). FLC encodes a MADS domain-containing transcription factor whose expression is sufficient to inhibit flowering (4, 5); however, the native FLC gene is only expressed to high levels in the presence of FRI, which encodes a plant-specific gene of unknown biochemical activity ...

Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat

“…In recent years, intronic regulatory elements (IREs; Yutzey et al 1989) have been identified which function as enhancers, repressors and promoters of gene transcription (Busch et al 1999;Deyholos and Sieburth 2000;Kapranov et al 2001;Fiume et al 2004). In many cases, IREs reside within the first intron (Wang et al 2002;Gazzani et al 2003;Michaels et al 2003;Fiume et al 2004). …”

“…An example of an IRE that is relevant for our discussion is provided by the Arabidopsis FLOWERING LOCUS C (FLC) gene (Sheldon et al 2002;Gazzani et al 2003;Michaels et al 2003). This gene encodes a MADS-box transcription factor that plays a central role in the vernalization pathway in Arabidopsis (Michaels and Amasino 1999;Sheldon et al 1999).…”

Functional Redundancy and New Roles for Genes of the Autonomous Floral-Promotion Pathway

“…A previous study has examined genetic interactions among Arabidopsis flowering-time mutants (Koornneef et al, 1998). This work, however, was performed in a Landsberg erecta (Ler) background that contains an atypical weak allele of FLC (Koornneef et al, 1994;Lee et al, 1994b;Gazzani et al, 2003;Michaels et al, 2003) and did not include fld, flk, or ld mutants. Therefore, double mutants were created between fpa and fca, fld, flk, fve, and ld in a Col background, which contains a strong allele of FLC.…”

“…Rapid-cycling accessions, in contrast, are early flowering in the absence of vernalization. This is most often due to naturally occurring mutations in FRI, in which case FLC expression is not activated, or to mutations in FLC itself (Johanson et al, 2000;Gazzani et al, 2003;Michaels et al, 2003). Therefore, rapid-cycling accessions appear to have evolved from winter annuals through loss-or reduction-of-function mutations in FRI or FLC.…”

Signalling for developmental plasticity

“…Winterannual accessions are late flowering because the FRIGIDA (FRI, Accession number AF228499) locus promotes the expression of the MADS box transcription factor FLOWERING LOCUS C (FLC, Accession number AF537203), a negative regulator of flowering, and vernalization accelerates flowering by down-regulating the expression of FLC. Null alleles of FRI [5] and natural allelic variation at the FLC locus [6] have allowed the evolution of summer-annual accessions that flower early even in the absence of vernalization. Several of these FRI and FLC alleles have appeared independently during the course of evolution.…”