A Flowering Locus C Homolog Is a Vernalization-Regulated Repressor in Brachypodium and Is Cold Regulated in Wheat

Abstract

Winter cereals require prolonged cold to transition from vegetative to reproductive development. This process, referred to as vernalization, has been extensively studied in Arabidopsis (Arabidopsis thaliana). In Arabidopsis, a key flowering repressor called FLOWERING LOCUS C (FLC) quantitatively controls the vernalization requirement. By contrast, in cereals, the vernalization response is mainly regulated by the VERNALIZATION genes, VRN1 and VRN2. Here, we characterize ODDSOC2, a recently identified FLC ortholog in monocots, knowing that it belongs to the FLC lineage. By studying its expression in a diverse set of Brachypodium accessions, we find that it is a good predictor of the vernalization requirement. Analyses of transgenics demonstrated that BdODDSOC2 functions as a vernalization-regulated flowering repressor. In most Brachypodium accessions BdODDSOC2 is down-regulated by cold, and in one of the winter accessions in which this down-regulation was evident, BdODDSOC2 responded to cold before BdVRN1. When stably down-regulated, the mechanism is associated with spreading H3K27me3 modifications at the BdODDSOC2 chromatin. Finally, homoeolog-specific gene expression analyses identify TaAGL33 and its splice variant TaAGL22 as the FLC orthologs in wheat (Triticum aestivum) behaving most similar to Brachypodium ODDSOC2. Overall, our study suggests that ODDSOC2 is not only phylogenetically related to FLC in eudicots but also functions as a flowering repressor in the vernalization pathway of Brachypodium and likely other temperate grasses. These insights could prove useful in breeding efforts to refine the vernalization requirement of temperate cereals and adapt varieties to changing climates.

Genome‐wide analysis of MIKC‐type MADS‐box genes in wheat: pervasive duplications, functional conservation and putative neofunctionalization

“…Likewise, the flowering time regulatory genes of the VRN1 ( TaAP1‐1 ) triad are in the D‐suppressed or A‐dominant category (Figs c, S5). This is in line with data showing that the VRN1 allele conferring spring growth habit and hence expected to be expressed most strongly (Loukoianov et al ., ; Chen & Dubcovsky, ) is VRN‐A1 ( TaAP1‐A1 ) in the cv Azhurnaya (Sharma et al ., ).…”

Successive evolutionary steps drove Pooideae grasses from tropical to temperate regions

“…S9a) and ODDSOC2 ‐like genes (Bradi4g30081, Bradi2g59119, and Bradi2g59191) (Fig. S9b; Yan et al ., ; Greenup et al., 2010; Woods et al ., ; Sharma et al ., ), were long‐term cold responsive. Finally, the majority of Pooideae‐specific genes (69) were downregulated with long‐term cold, including those involved in photosynthesis and growth based on their annotation as chloroplast‐ and metabolism‐related (Table S9).…”

Pleiotropy in developmental regulation by flowering‐pathway genes: is it an evolutionary constraint?

“…Sometimes homologous genes act in the same pathway, but the order of those genes differs, and sometimes they differ in the immediate interacting partners. For instance, the homolog of AtCO in Brachypodium (BdVRN2) and wheat (TaVRN2), and the orthologs of AtFT in wheat and barley, VRN3, have the function that AtFLC has in the A. thaliana flowering pathway (Yan et al, 2004(Yan et al, , 2006Sharma et al, 2017). Similarly, the homolog of AtAP1 in Brachypodium (BdVRN1) has the function that AtVRN1 has in A. thaliana (Feng et al, 2017).…”