Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis.

BACKGROUND: MADS-domain transcription factors play important roles during plant development. The Arabidopsis MADS-box gene SHORT VEGETATIVE PHASE (SVP) is a key regulator of two developmental phases. It functions as a repressor of the floral transition during the vegetative phase and later it contributes to the specification of floral meristems. How these distinct activities are conferred by a single transcription factor is unclear, but interactions with other MADS domain proteins which specify binding to different genomic regions is likely one mechanism. RESULTS: To compare the genome-wide DNA binding profile of SVP during vegetative and reproductive development we performed ChIP-seq analyses. These ChIP-seq data were combined with tiling array expression analysis, induction experiments and qRT-PCR to identify biologically relevant binding sites. In addition, we compared genome-wide target genes of SVP with those published for the MADS domain transcription factors FLC and AP1, which interact with SVP during the vegetative and reproductive phases, respectively. CONCLUSIONS: Our analyses resulted in the identification of pathways that are regulated by SVP including those controlling meristem development during vegetative growth and flower development whereas floral transition pathways and hormonal signaling were regulated predominantly during the vegetative phase. Thus, SVP regulates many developmental pathways, some of which are common to both of its developmental roles whereas others are specific to only one of them.

The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes.

During the initial stages of flower development, floral meristems increase in size without the formation of floral organs. When a critical meristem size is reached, the floral meristem begins to develop the floral organs. The first stages of flower development are characterized by the expression of genes such as Apetala 1 (AP1), cauliflower (CAL), AGAMOUS-LIKE 24 (AGL24) and short vegetative phase (SVP). We have shown that AP1, AGL24 and SVP act redundantly to control the identity of the floral meristem and to repress expression of class B, C and E genes. Recently, it was shown that class E gene repression was direct and established by two independent pathways. We show here that repression of class B and C genes is also directly established by a co-repressor complex that comprises LEUNIG (LUG), SEUSS (SEU) and the MADS box dimers AP1-AGL24 and AP1-SVP. Furthermore, we show that the distantly related suppressor of overexpression of CO 1 (SOC1) MADS box gene can complement for the loss of AGL24 and SVP activity; however, under normal conditions, this transcription factor does not play a role during the early stages of flower development.

AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis.

The formation of flowers starts when floral meristems develop on the flanks of the inflorescence meristem. In Arabidopsis the identity of floral meristems is promoted and maintained by APETALA1 (AP1) and CAULIFLOWER (CAL). In the ap1 cal double mutant the meristems that develop on the flanks of the inflorescence meristem are unable to establish floral meristem identity and develop as inflorescence meristems on which new inflorescence meristems subsequently proliferate. We demonstrate in contrast to previous models that AGAMOUS-LIKE 24 (AGL24) and SHORT VEGETATIVE PHASE (SVP) are also floral meristem identity genes since the ap1-10 agl24-2 svp-41 triple mutant continuously produces inflorescence meristems in place of flowers. Furthermore, our results explain how AP1 switches from a floral meristem identity factor to a component that controls floral organ identity.

AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis.

Loss-of-function alleles of AGAMOUS-LIKE24 (AGL24) and SHORT VEGETATIVE PHASE (SVP) revealed that these two similar MADS box genes have opposite functions in controlling the floral transition in Arabidopsis thaliana, with AGL24 functioning as a promoter and SVP as a repressor. AGL24 promotes inflorescence identity, and its expression is downregulated by APETALA1 (AP1) and LEAFY to establish floral meristem identity. Here, we combine the two mutants to generate the agl24 svp double mutant. Analysis of flowering time revealed that svp is epistatic to agl24. Furthermore, when grown at 30 degrees C, the double mutant was severely affected in flower development. All four floral whorls showed homeotic conversions due to ectopic expression of class B and C organ identity genes. The observed phenotypes remarkably resembled the leunig (lug) and seuss (seu) mutants. Protein interaction studies showed that dimers composed of AP1-AGL24 and AP1-SVP interact with the LUG-SEU corepressor complex. We provide genetic evidence for the role of AP1 in these interactions by showing that the floral phenotype in the ap1 agl24 svp triple mutant is significantly enhanced. Our data suggest that MADS box proteins are involved in the recruitment of the SEU-LUG repressor complex for the regulation of AGAMOUS.