Gene regulatory networks controlled by FLOWERING LOCUS C that confer variation in seasonal flowering and life history

Abstract

Responses to environmental cues synchronize reproduction of higher plants to the changing seasons. The genetic basis of these responses has been intensively studied in the Brassicaceae. The MADS-domain transcription factor FLOWERING LOCUS C (FLC) plays a central role in the regulatory network that controls flowering of Arabidopsis thaliana in response to seasonal cues. FLC blocks flowering until its transcription is stably repressed by extended exposure to low temperatures in autumn or winter and, therefore, FLC activity is assumed to limit flowering to spring. Recent reviews describe the complex epigenetic mechanisms responsible for FLC repression in cold. We focus on the gene regulatory networks controlled by FLC and how they influence floral transition. Genome-wide approaches determined the in vivo target genes of FLC and identified those whose transcription changes during vernalization or in flc mutants. We describe how studying FLC targets such as FLOWERING LOCUS T, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 15, and TARGET OF FLC AND SVP 1 can explain different flowering behaviours in response to vernalization and other environmental cues, and help define mechanisms by which FLC represses gene transcription. Elucidating the gene regulatory networks controlled by FLC provides access to the developmental and physiological mechanisms that regulate floral transition.

Keywords: FT; SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 15; SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1; FLOWERING LOCUS C; Floral transition; MADS-domain; vernalization.

Fig. 1.

Schematic representation of the gene regulatory network controlled by FLC. (A) FLC is a master regulator of flowering that integrates cues from several flowering pathways in Arabidopsis. FLC expression is repressed by the cold-induced vernalization pathway. FLC directly represses the florigen-encoding gene FT and SQUAMOSA PROMOTER BINDING-LIKE PROTEIN 15 (SPL15). SPL15 is additionally post-translationally regulated by the gibberellin pathway via DELLA proteins and at the post-transcriptional level by the ageing pathway via miR156. The MADS-domain protein SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) is encoded by another direct target of FLC, and cooperates with SPL15 to activate target genes such as FRUITFULL and MIR172B. (B) A type II coherent feed-forward loop regulates expression of the positive floral regulator TARGET OF FLC AND SVP1 (TFS1). FLC and SVP directly repress TFS1 transcription and that of its positive activator SOC1. Activation of TFS1 expression in the inflorescence meristem also involves SPL9.

Fig. 2.

FLC and its orthologues in other species regulate flowering in response to vernalization by controlling two major floral-promoting pathways involving SPL15 and FT. In perennial Arabis alpina plants exposed to vernalization, FT expression is repressed by the FLC orthologue PEP1 both before and after vernalization, when PEP1 is reactivated by warm conditions (A and B). Therefore, flowering is dependent on the miR156/SPL15 module. When young meristems are vernalized, miR156 levels are high and repress floral transition by maintaining low SPL15 levels, so no flowering occurs (A). Only older meristems can flower during the vernalization period when the level of miR156 has fallen and SPL15 mRNA can increase during vernalization (B). In the winter-annual Arabidopsis thaliana, FLC is transcriptionally repressed during vernalization in short days in the cold and remains stably repressed in subsequent warm temperatures (C and D). This allows plants to flower by activation of FT transcription after cold treatment via the photoperiodic pathway irrespective of age, even when miRNA156 levels are high in young plants that are vernalized (C). Stable repression of FLC transcription in annuals therefore allows plants to flower independently of age through the FT pathway after vernalization, thus bypassing dependency on the miRNA156/SPL15 module. The graphs (A–D) depict the relative level of FLC, PEP1, SPL15, and FT mRNAs, and miRNA156 on the y-axis. V, vernalization; w, weeks; SD. short days; LD, long days. The blue box represents a vernalization treatment.