Vernalisation

Abstract

Vernalisation is the response to a period of prolonged cold required by many plants to switch from vegetative to reproductive growth. Variation in the requirement for, and the response to, a period of weeks or months of cold underpins life history variation in both wild and crop species and ensures flowering occurs in the more optimal conditions in spring. In monocots and dicots three key players – a gene activated by cold, a repressor, and an integrator – have been identified within the vernalisation regulatory network. However, the relative importance of allelic variation at these genes to variation in vernalisation response differs between the two subdivisions of flowering plants. Genetic and molecular analysis of this variation has revealed a mechanism with core epigenetic components in the exemplar Angiosperm lineages Brassicaceae and Poaceae.

Key Concepts

  • Plants utilise the memory of winter to align flowering with the favourable conditions of spring.
  • Vernalisation promotes competence to flower in response to a prolonged period of cold.
  • Epigenetic regulation is a stable change in gene expression (through multiple mitotic and sometimes meiotic divisions) without a change in the underlying DNA sequence.
  • In both monocots and dicots three key players – a gene activated by cold, a repressor and an integrator – have been identified as components of the vernalisation network.
  • FLOWERING LOCUS C (FLC) is the key regulator of vernalisation in the Brassicaceae.
  • VERNALIZATION 1 (VRN1) is the main regulator of vernalisation in the Poaceae.
  • Polycomb proteins are conserved across kingdoms.

Keywords: vernalisation; epigenetic; monocot; dicot; winter; FLC; VRN1; FT; floral transition; PRC2

Figure 1. Key genes in vernalisation in Monocots (example Triticum aestivum). (a) The major regulator and activator of vernalisation in monocots is the MADS‐box transcription factor VERNALISATION 1 (VRN1). Variation in VRN1 underlies natural variation in the vernalisation response. Most studies have focused on the most highly expressed homeologous copy with the major mutations in VRN‐A1 only highlighted in this figure, additional mutations have been found in VRN‐B1 and VRN‐D1. Mutations which cause over‐expression (promoter and intron 1 deletions) removes vernalisation requirement (Spring habit). SNPs in exon 4 and 7 lead to changes in expression levels which alter the rate of vernalisation. Copy number variation of VRN‐A1 also alters the level of vernalisation required. The GRP2 binding domain is also highlighted which is involved in the regulation of pre‐mRNA VRN1 transcript. Beyond the three homeologous copies on the A, B and D genomes a translocation of VRN‐A1 has occurred to 5D, which confers spring habit. (b) VERNALISATION 2 (VRN2) is a repressor which contains a CCT domain. It exists as a duplication, with additional copy number variation occurring on the 5B homoeologue in some grasses. As a recessive repressor of the response VRN2 was initially identified in diploid wheat with the identification of mutations in the CCT‐domains resulting in spring growth habit. VRN2 expression decreases under low temperatures and is activated by warm temperatures under long‐day photoperiods. ODDSOC2 is a MADS‐box transcription factor the expression of which decreases under low temperatures and rise in subsequent warm temperatures. It was first identified through a study of MADS‐box expression responses to cold temperatures. (c) FT1 is the major integrator of a number of flowering time pathways in T. aestivum, including the vernalisation and photoperiod responses. FT1 expression is low before vernalisation and only starts to be expressed when plants are transitioning through the inflorescence meristem development stages. FT1 is expressed in the leaf. See also: Floral Meristems
Figure 2. Key genes in vernalisation in Brassicaceae. (a) The cold‐responsive element in Arabidopsis thaliana and other Brassicaceae is the PHD fibronectin domain protein VERNALISATION INSENSITIVE3 (VIN3). Variation at VIN3 may underlie natural variation in vernalisation response in A. thaliana. During the cold, it activates the POLYCOMB REPRESSIVE COMPLEX 2 to downregulate and epigenetically silence FLC. First graph – VIN3 expression is under circadian regulation. Second graph – VIN3 is upregulated slowly over weeks in response to cold but downregulated rapidly over hours in response to warm conditions. (b) FLC is a major repressor of flowering in the Brassicaceae, and in A. thaliana nonfunctional alleles or the absence of the activator FRI result in loss of vernalisation requirement. Graph: FLC is downregulated by prolonged cold, a process that involves lncRNAs. Epigenetic silencing, triggered in the cold by VIN3, ensures the repression of FLC after the end of cold. A. thaliana gene model – the lncRNAs are produced from the FLC locus itself and include the conserved antisense COOLAIR transcripts (orange), and two reported sense lncRNAs, COLDAIR (grey) and COLDWRAP (yellow). Epigenetic silencing requires the presence of two elements in the first intron of FLC, RY sites (red triangles) in the first intron of FLC, to which the B3‐binding protein VAL1 binds, and a region known as the Vernalisation Response Element (VRE, blue box), which includes the COLDAIR promoter. In Arabidopsis, polymorphisms (coloured triangles) form distinct haplotypes that generate rapid (RV) or slow vernalisation (SV) responses through diverse mechanisms, such as changing the splicing of COOLAIR to generate a less repressive form (SV3, COOLAIR variant with green outline) or causing reactivation of the FLC allele after vernalisation (SV1 – see blue line on graph). Other gene models: COOLAIR transcripts and secondary structure, the VRE and RY binding sites are conserved at FLC throughout the Brassicaceae. In A. lyrata and Brassica rapa, FLC copies have multiplied, either through tandem duplication or whole genome duplications, resulting in multiple functional copies. In the perennial species Arabis alpina, the FLC homologue PERPETUAL FLOWERING1 is required both for vernalisation response and for the seasonal cessation of flowering. In all these species, variation at FLC homologues affects vernalisation response. (c) FT is the major integrator of several flowering time pathways in A. thaliana, including the vernalisation, ambient temperature and photoperiod responses. FLC represses FT expression, as well as other floral identity genes, directly until it is downregulated by the prolonged cold. Graph; after FLC has been downregulated, FT can be upregulated in the warm by long photoperiods in the leaves. The protein then travels to the shoot apical meristem to promote the floral transition.
Figure 3. Regulation of FLC during vernalisation in Arabidopsis thaliana. (a) Before vernalisation. During embryogenesis, the presence of an active version of the FRIGIDA (FRI) protein promotes formation of the FRI‐complex (FRI‐c, purple tripod) at the FLC promoter. The complex includes several orthologues of FRI and binds a specific DNA element in the promoter through the protein SUF4. FRI‐c recruits several chromatin remodelling complexes which covalently modify histone proteins to promote transcription at FLC, including; histone acetylases, the SWR1‐complex (dark blue ovals, promotes H2A.Z deposition); the COMPASS/TRITHORAX complex (blue circles, promotes H3K4me3 methylation); and SDG8 (dark blue circle within COMPASS, H3K36me3 methylation). SDG8 interacts with the demethylase ELF6, which removes repressive H3K27me3 marks, and with the PAF1‐complex (blue circles), which promotes transcription of FLC through association with RNA Polymerase II. FRI‐c also recruits the Cap‐binding Complex (green circles) so that this transcription is more likely to result in the production of capped, mature FLC transcripts (black transcript). This upregulation is opposed by several factors collectively referred to as the ‘autonomous pathway’, which downregulate FLC in the absence of FRI in Arabidopsis. Several of these, such as FCA and FY, form part of the polyadenylation machinery (orange circles), which act not on FLC directly but instead promote use of a proximal polyadenylation site during transcription of the antisense lncRNA COOLAIR (orange transcripts), increasing the balance of the short Class I transcripts relative to the distally polyadenylated Class II transcripts. This creates a repressive chromatin environment at FLC by promoting the action of the H3K4 demethylase FLD, which associates with histone deacetylases (HDAs), as does another autonomous pathway member, FVE, to remove marks that promote transcription and promote the presence of silencing marks instead. Transparency of the transcripts indicates a relative number of transcripts. Epigenetic marks side panel: in a FRI background, the balance of activities of FRI‐c and the autonomous pathway results in a peak of promotive H3K36me3 and H3K4me3 at the start of intron 1 in FLC (blue graph) and a low level of the silencing H3K27me3 mark (red graph), and FLC transcription from most cells within the plant (white nuclei in green cells). (b) During Cold. First day to weeks; FLC transcripts (grey) are downregulated in response to cold, anticorrelating with the upregulation of COOLAIR transcripts (orange; especially Class I transcripts), which are mutually exclusive with FLC at the same locus. Promotive H3K36me3 and H3K4‐me2 and ‐me3 marks start to decrease at the FLC locus. Over weeks, this decrease in promotive marks continues. In opposition to this, transcriptional upregulation of the PHD‐domain protein VIN3 in the cold (grey pacman) allows it to multimerise with its constitutively expressed homologue VRN5 (grey pointer) and together they activate the already‐present Polycomb Repressive Complex2 (brown circles) at the nucleation region, which methylates H3K27me3 via SWN to repress transcription of both FLC and COOLAIR. They are recruited to this region by VAL1 (red oval), which binds to RY elements (red triangles) in intron I through its B3 domain. Epigenetic marks side panel: measurement of chromatin marks at the multicellular tissue level shows the loss of promotive chromatin marks (e.g. H3K36me3) and increase of H3K27me3 at the nucleation region in a quantitative manner over time, which correlates with FLC transcription. However, at the level of individual loci, this switch from productive transcription to epigenetically silenced is digital, going from ON to OFF, so that individual cells within the tissue stochastically silence cell‐autonomously (red nuclei in green cells), resulting in a patchwork of cells expressing FLC in which more and more silence over time. (c) After cold. PRC2‐mediated silencing of FLC remains on the return to the warm, even when VIN3 is absent, and is stable, and stabilised, through mitosis. This is mediated by spreading of the active PRC2 complex from the nucleation region across the whole FLC locus, and a change in the composition of the core PRC2 components, in which the methylase homologue SWN, predominant in the cold, is replaced by the CLF methylase in the warm. Spreading the silencing H3K27me3 mark from just the nucleation region to many more nucleosomes across the gene ensures it is more likely to be inherited when nucleosomes are divided between daughter DNA strands during mitosis. This spreading process also requires a protein called LHP1. Epigenetic marks side panel: Spreading of the PRC2 spreads H3K27me3 across the FLC locus, maintaining cells in a silenced state.
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Further Reading

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Dixon, Laura E, Hepworth, Jo, and Irwin, Judith A(Aug 2019) Vernalisation. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002048.pub4]