O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat

Abstract

Vernalization, sensing of prolonged cold, is important for seasonal flowering in eudicots and monocots. While vernalization silences a repressor (FLC, MADS-box transcription factor) in eudicots, it induces an activator (TaVRN1, an AP1 clade MADS-box transcription factor) in monocots. The mechanism for TaVRN1 induction during vernalization is not well understood. Here we reveal a novel mechanism for controlling TaVRN1 mRNA accumulation in response to prolonged cold sensing in wheat. The carbohydrate-binding protein VER2, a jacalin lectin, promotes TaVRN1 upregulation by physically interacting with the RNA-binding protein TaGRP2. TaGRP2 binds to TaVRN1 pre-mRNA and inhibits TaVRN1 mRNA accumulation. The physical interaction between VER2 and TaGRP2 is controlled by TaGRP2 O-GlcNAc modification, which gradually increases during vernalization. The interaction between VER2 and O-GlcNAc-TaGRP2 reduces TaGRP2 protein accumulation in the nucleus and/or promotes TaGRP2 dissociation from TaVRN1, leading to TaVRN1 mRNA accumulation. Our data reveal a new mechanism for sensing prolonged cold in temperate cereals.

Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia

“…These results confirmed that TaGRP2 functions as a flowering repressor (21). Our REMSA results show that the presence of three SNPs in the RIP-3 VRN-D4 region is sufficient to disrupt the binding between TaGRP2 and its target site (Fig.…”

“…4). TaGRP2 binding to the VRN1 pre-mRNA is required for the inhibition of VRN1 expression (21), so the disruption of this interaction can explain the earlier expression of VRN-D4. This mechanism is also consistent with the spring growth habit associated with large deletions in the first intron of VRN1, including the RIP-3 region (20,68).…”

“…In the absence of cold, TaGRP2 binds to VRN1 premRNA and inhibits VRN1 expression. During vernalization, TaGRP2 is gradually modified (O-GlcNAcylation), allowing the interaction with a carbohydrate-binding protein called VER2, which reduces TaGRP2-mediated repression of VRN1 expression (21).…”

“…Mutation in the VRN1 promoter (17)(18)(19) or large deletions in the first intron (20) greatly reduce or eliminate the vernalization requirement, and wheat varieties carrying these alleles are classified as "spring wheats." A critical regulatory region in the VRN1 first intron is transcribed and contains binding sites for the RNA-binding protein TaGRP2 (21). TaGRP2 is homologous to the Arabidopsis GLYCINE-RICH RNA-BINDING PROTEIN7 (GRP7), which is a single-stranded Significance A precise regulation of flowering time is critical for plant reproductive success and for cereal crops to maximize grain production.…”

Direct links between the vernalization response and other key traits of cereal crops

“…Chromatin in the first intron of VRN1 has histone modifications that are thought to maintain an inactive transcriptional state, potentially explaining the role of the first intron in maintaining repression of VRN1 before winter 14 . Sequences in the first intron might also regulate processing of the VRN1 transcript 15 . Several active alleles of VRN1 with deletions or insertions in the first intron have been identified in barley [16][17][18][19] .…”