Crosstalk between Cold Response and Flowering in Arabidopsis Is Mediated through the Flowering-Time Gene SOC1 and Its Upstream Negative Regulator FLC

Abstract

The appropriate timing of flowering is pivotal for reproductive success in plants; thus, it is not surprising that flowering is regulated by complex genetic networks that are fine-tuned by endogenous signals and environmental cues. The Arabidopsis thaliana flowering-time gene SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) encodes a MADS box transcription factor and is one of the key floral activators integrating multiple floral inductive pathways, namely, long-day, vernalization, autonomous, and gibberellin-dependent pathways. To elucidate the downstream targets of SOC1, microarray analyses were performed. The analysis revealed that the soc1-2 knockout mutant has increased, and an SOC1 overexpression line has decreased, expression of cold response genes such as CBFs (for CRT/DRE binding factors) and COR (for cold regulated) genes, suggesting that SOC1 negatively regulates the expression of the cold response genes. By contrast, overexpression of cold-inducible CBFs caused late flowering through increased expression of FLOWERING LOCUS C (FLC), an upstream negative regulator of SOC1. Our results demonstrate the presence of a feedback loop between cold response and flowering-time regulation; this loop delays flowering through the increase of FLC when a cold spell is transient as in fall or early spring but suppresses the cold response when floral induction occurs through the repression of cold-inducible genes by SOC1.

Cross-Repressive Interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the Control of Greening, Cold Tolerance, and Flowering Time in Arabidopsis

“…During such cold periods, SOC1 expression is reduced and the concomitant delay in flowering correlates with an increase in the expression of cold-regulated genes such as C-REPEAT/DROUGHT-RESPONSIVE ELEMENT-BIND-ING FACTOR (CBF) and cold-response marker genes such as COLD-REGULATED15a (COR15a) and COR15b. Inversely, SOC1 overexpression results in the inverse regulation of cold-regulated genes, and this supports experimental data that indicate that SOC1 is a direct regulator of cold-regulated genes (Seo et al, 2009).…”

“…Here, we observed a suppression of the increased cold tolerance of soc1 in the absence of GNC and GNL as well as an increase in cold tolerance when the two GATAs are overexpressed. It was proposed that the antagonistic regulation of cold tolerance and flowering time by SOC1 may be relevant during short periods of cold temperature as they can be experienced by plants during cold periods in spring (Seo et al, 2009). Two studies have recently reported the genome-wide identification of direct SOC1 targets using ChIP (Immink et al, 2012;Tao et al, 2012).…”

“…Besides its prominent role in the regulation of flowering time, SOC1 was previously also shown to interfere with cold tolerance (Seo et al, 2009). Interestingly, a qRT-PCR analysis of mock-and cold-treated 10-d-old seedlings revealed that GNC and GNL are regulated by cold temperatures, pointing at a putative role of the two genes in cold response (Fig.…”

“…6A). Since increased cold tolerance is also a phenotype of soc1 mutants (Seo et al, 2009), we reasoned that the elevated GNC and GNL transcript levels in soc1 may be causative for the cold tolerance phenotype of this mutant. In support of this hypothesis, we found that the increased cold tolerance phenotype of soc1 is strongly suppressed in the soc1 gnc gnl triple mutant (Fig.…”

“…SOC1 expression and flowering are also repressed in response to short periods of cold that plants experience, such as during a cold spring season (Seo et al, 2009). During such cold periods, SOC1 expression is reduced and the concomitant delay in flowering correlates with an increase in the expression of cold-regulated genes such as C-REPEAT/DROUGHT-RESPONSIVE ELEMENT-BIND-ING FACTOR (CBF) and cold-response marker genes such as COLD-REGULATED15a (COR15a) and COR15b.…”