Proteasome-Mediated Degradation of FRIGIDA Modulates Flowering Time in Arabidopsis during Vernalization

Abstract

Winter-annual accessions of Arabidopsis thaliana require either exposure to cold stress or vernalization to initiate flowering via FRIGIDA (FRI). FRI acts as a scaffold protein to recruit several chromatin modifiers that epigenetically modify flowering genes. Here, we report that proteasome-mediated FRI degradation regulates flowering during vernalization in Arabidopsis. Our genetic and biochemical experiments demonstrate that FRI directly interacts with the BTB (Bric-a-Brac/Tramtrack/Broad Complex) proteins LIGHT-RESPONSE BTB1 (LRB1) and LRB2 as well as the CULLIN3A (CUL3A) ubiquitin-E3 ligase in vitro and in vivo, leading to proteasomal degradation of FRI during vernalization. The degradation of FRI is accompanied by an increase in the levels of the long noncoding RNA ColdAIR, which reduces the level of histone H3Lys4 trimethylation (H3K4me3) in FLOWERING LOCUS C chromatin to promote flowering. Furthermore, we found that the cold-induced WRKY34 transcription factor binds to the W-box in the promoter region of CUL3A to modulate CUL3A expression. Deficiency of WRKY34 suppressed CUL3A transcription to enhance FRI protein stability and led to late flowering after vernalization. Conversely, overexpression of WRK34 promoted FRI degradation and early flowering through inducing CUL3A accumulation. Together, these data suggest that WRKY34-induced and CUL3A-dependent proteolysis of FRI modulate flowering in response to vernalization.

DELLA proteins interact with FLC to repress flowering transition

“…There are several regulatory pathways that converge to regulate FLC: the FRIGIDA pathway activates FLC expression, the autonomous pathway down regulates FLC , and vernalization epigenetically silences FLC in response to prolonged cold. All of these pathways involve a set of antisense transcripts, collectively named as COOLAIR (Swiezewski et al ; Hornyik et al ; Liu et al ) and COLDAIR (Heo and Sung ; Hu et al ). Epigenetic regulation of FLC by proteins and long noncoding RNAs in transcription levels have been extensively studied (Bastow et al ; Sung and Amasino ; Margueron et al ; Sung et al ; Schmitz and Amasino ; Choi et al ; Heo and Sung ; Jeon and Kim ; Kim and Sung ).…”

OsCUL3a Negatively Regulates Cell Death and Immunity by Degrading OsNPR1 in Rice

“…Previous studies in plants have demonstrated that the ubiquitin/proteasome pathway is an essential component of the regulatory networks controlling many important cellular processes, including growth and development (Figueroa et al, 2005;Hu et al, 2014), as well as defense responses (Zeng et al, 2004). Among the three major enzymes in this pathway, the E3 ubiquitin ligases are responsible for controlling the specificity of target protein recognition and degradation via the 26S proteasome.…”

Functions of plants long non-coding RNAs

“…It is not known whether COLDAIR may have roles in the autonomous pathway so far. Interestingly, recently data showed that COLDAIR is involved in FRIGIDA pathway [73], and a putative histone methyltransferase SDG7, which is essential for cold induction of VIN3, can elevate the expression levels of COLDAIR, as well as COOLAIR [74]. Considering the partial temporal overlap of expression patterns during vernalization between two lncRNAs [51], it would be interesting to investigate the possible connection between the sense COLDAIR and antisense COOLAIR induction, and how they integrate to coordinate FLC silencing during vernalization.…”