Developmental transitions in plants are aligned with specific seasons to maximise reproductive success. A major seasonal cue used to time the transition to flowering is temperature (Hancock et al., 2011; Andrés and Coupland, 2012; Manzano-Piedras et al., 2014). Many plants overwinter in a vegetative form and flower in spring. This alignment of the floral transition with spring is achieved through a process called vernalization, in which flowering is accelerated by previous exposure to prolonged winter cold. In Arabidopsis thaliana and its relatives, FLOWERING LOCUS C (FLC), a MADS-box transcription factor, delays the transition to flowering in warm temperatures until its expression is downregulated by exposure to cold (Michaels and Amasino, 1999; Sheldon et al., 1999). On return to warm, spring-like conditions, FLC remains epigenetically silenced, permitting expression of FT and floral meristem identity genes that trigger the floral transition (Helliwell et al., 2006; Searle et al., 2006).

The vernalization mechanism has been genetically dissected using controlled laboratory conditions (Song et al., 2013; Bloomer and Dean, 2017; Whittaker and Dean, 2017). FLC expression is upregulated by the coiled-coil protein FRIGIDA (FRI), which establishes an active transcription state at FLC through interactions with chromatin modifiers including the H3K36 methyltransferase SET DOMAIN GROUP8 (SDG8) (Choi et al., 2011; Hyun et al., 2017; Li et al., 2018). This upregulation is antagonised by the autonomous pathway, a group of interacting RNA-processing factors, (eg. FCA and FY) and chromatin modifying factors (eg. FLD and FVE). These promote a low expression state at FLC through interactions with the long non-coding antisense transcript group, COOLAIR (Ausín et al., 2004; Liu et al., 2007; Wu et al., 2016; Wu et al., 2020). A high FLC transcription state is associated with plants that overwinter before flowering. Cold transcriptionally downregulates FLC, and the locus is maintained in an epigenetically silenced state by a Polycomb Repressive Complex 2 (PRC2) mechanism (Gendall et al., 2001; Bastow et al., 2004; Sung and Amasino, 2004; Greb et al., 2007; Helliwell et al., 2011; Hepworth et al., 2018). This PRC2 mechanism requires the temperature-integrating accessory protein, VERNALIZATION INSENSITIVE3 (VIN3) (Sung and Amasino, 2004; Bond et al., 2009a; Antoniou-Kourounioti et al., 2018). Cold-induction of VIN3 expression leads to formation of a PHD-PRC2 complex that also contains the PHD protein VERNALIZATION5 (VRN5) and the specific Su(z)12 component VRN2 (Sung et al., 2006a; Greb et al., 2007; De Lucia et al., 2008). This complex is nucleated at FLC by the B3-binding protein VP1/ABI3-LIKE 1 (VAL1) (Qüesta et al., 2016; Yuan et al., 2016). The PHD-PRC2 methylates histone H3 lysine 27 residues in a ~ 3 nucleosome domain at FLC to epigenetically ‘switch’ each allele off in a stochastic manner that over the population of cells produces a quantitative memory of the length of cold (Angel et al., 2011; Yang et al., 2014; Angel et al., 2015; Yang et al., 2017). When plants return to warm conditions, the PHD-PRC2 spreads over the locus to maintain long-term epigenetic memory, and this requires the action of LIKE HETEROCHROMATIN1 (LHP1) (Mylne et al., 2006; Sung et al., 2006b; Berry et al., 2017; Yang et al., 2017).

FLC expression and memory is influenced by natural non-coding cis polymorphism at the locus (Lempe et al., 2005; Shindo et al., 2006; Coustham et al., 2012; Li et al., 2015; Qüesta et al., 2020). Different Arabidopsis accessions need different lengths of cold to epigenetically silence FLC, and this requirement is determined by non-coding SNPs at FLC (Shindo et al., 2006; Coustham et al., 2012). Indeed, within the Arabideae tribe, cis regulation of FLC orthologues contributes to perennial-vs.-annual flowering differences (Kiefer et al., 2017). Within the worldwide Arabidopsis thaliana population, non-coding variation defines a small number of FLC haplotypes, which confer quantitatively different flowering time responses to different lengths of vernalization in constant cold in the laboratory (Li et al., 2014). These haplotypes appear to have been maintained in the A. thaliana population due to their contributions to life history diversity (Sánchez-Bermejo et al., 2012; Li et al., 2014; Méndez-Vigo et al., 2016), and they show different geographic distributions, suggesting that they are adapted to different climates (Méndez-Vigo et al., 2011; Li et al., 2014).

Recent work has shown the importance of analysing flowering in natural field conditions (Figure 1A), ‘in natura’ (Kudoh, 2016). Such studies have highlighted how the influence of genes of major effect, including FLC, changes depending on the field environment (Wilczek et al., 2009; Fournier-Level et al., 2011; Duncan et al., 2015; Ågren et al., 2017; Taylor et al., 2019). In particular, the investigation of RNA levels in natura has identified genetic mechanisms in the field that were previously unknown from laboratory observations (Antoniou-Kourounioti et al., 2018; Song et al., 2018; Nagano et al., 2019). For example, field work in Sweden and the UK with the vernalization reference genotype Col FRI^SF2 and mutants in VIN3 (vin3-4) has shown that initial VIN3-independent FLC downregulation requires cold temperatures, whereas VIN3-mediated epigenetic silencing requires the absence of daily temperatures above 15°C (Hepworth et al., 2018). Autumn conditions greatly influence when epigenetic silencing initiates, sometimes leading to temporal separation of the two phases, which in laboratory constant-condition experiments and some natural environments occur concurrently (Hepworth et al., 2018).

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Here, we exploit field studies in three climatically distinct locations, over two years, to define the roles of FLC cis polymorphism and known genetic regulators of FLC in VIN3-dependent and -independent phases of the vernalization response under natural conditions (Figure 2A). We hypothesised that accessions bearing different FLC haplotypes would show different flowering time responses to winter environments, and that this would be due, at least in part, to variation in the downregulation and silencing of FLC itself, arising from the cis polymorphism at FLC. Moreover, we expected variation in the FLC epigenetic silencing mechanism would play a particularly important role, as this mechanism has previously been shown to vary in natural accessions (Coustham et al., 2012; Wollenberg and Amasino, 2012; Duncan et al., 2015).

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Our results demonstrate how in the field the major FLC haplotypes, differing only through non-coding variation, have different starting FLC levels and rates of response to autumn cold, but show more similar epigenetic silencing rates in winter. This results in effective repression of FLC by midwinter and post-winter flowering in most years, across haplotypes and climates. Our experiments also reveal effects of the FLC haplotypes on prevention of precocious flowering in warm years, and on reproductive success after winter via effects on branching and silique number. By studying gene expression across years and climates, we have been able to dissect how non-coding cis variation at FLC modulates flowering time and fitness in response to different natural fluctuating environments.

Investigation of the dynamics of key floral integrators in the field has recently led to important insights into their molecular response to natural environments (Antoniou-Kourounioti et al., 2018; Song et al., 2018). Here, we integrated experiments on the expression of FLC in field conditions with investigation on how natural genetic variation and induced mutation interact in distinct climates to affect phenotype and fitness. In our previous work, we found that, as expected from laboratory studies, FLC was repressed and VIN3 was induced by winter cold (Antoniou-Kourounioti et al., 2018; Hepworth et al., 2018). However, in 2014–5, winter conditions in Norwich generated a subtly different response to those in Sweden, activating the VIN3-independent transcriptional shutdown before the VIN3-dependent epigenetic pathway (delay in VIN3 onset and slow then fast shutdown of FLC in Norwich, Figure 2—figure supplement 1). In the following season, this pattern was triggered again, not only in Norwich, but also in North Sweden, implying that this is a common occurrence that plants must adjust to across climates, although with different frequencies at different locations (Figure 3—figure supplement 1).

We find that variation in FLC mRNA levels in both accessions and NILs is largely due to differences in both the starting FLC level and the VIN3-independent rate of shutdown (collectively called autumnal expression), which vary widely between accessions but not between field sites or years (Figure 5). This variation in rate of response, as well as absolute levels of FLC, partly explains why FLC levels measured at any one time may not correlate with the final flowering time phenotype in different accessions (Sasaki et al., 2018).

In Norwich, we investigated the mechanisms of the responses. Mutants of the autonomous pathway, which increase FLC expression in fri plants in laboratory conditions (Ausín et al., 2004; Liu et al., 2010; Wu et al., 2016), generally behaved in a similar manner to Col FRI in terms of vernalization response (Figure 4). However, the reduced response of the fve mutants in the VIN3-independent phase, though not significant in each year, may be worth further investigation, as FVE has been implicated in intermittent cold-sensing through histone deacetylation at FLC, independently of vernalization (Kim et al., 2004; Jung et al., 2013).

All three factors that set FLC levels in the field (starting levels, VIN3-independent and VIN3-dependent phases) require chromatin modifiers for their correct function. The VIN3-independent phase involves chromatin-modifier regulation of transcription, with the VIN3-dependent phase using a similar set of modifiers. These chromatin regulators are rarely found in genome-wide-association studies for flowering time, likely because their alteration would have pleiotropic effects. In the natural accessions we find that the VIN3-dependent (epigenetic) phase is indeed the least variable (Figure 5). This may explain why so much variation in vernalization maps to FLC itself (Lempe et al., 2005; Sánchez-Bermejo et al., 2012; Dittmar et al., 2014; Sasaki et al., 2015; Bloomer and Dean, 2017; Sasaki et al., 2018). Nevertheless, we did observe variation in VIN3 expression in Var2-6, which seems to derive from differences in circadian regulation (Figure 3—figure supplement 3), and QTLs over the VIN3 region have previously been found to affect flowering (Dittmar et al., 2014; Méndez-Vigo et al., 2016; Ågren et al., 2017). Variation in VIN3 expression in the other accessions we tested was more complex than the general downregulation in Var2-6. Given the intricate regulation of VIN3 induction (Antoniou-Kourounioti et al., 2018), identifying the source of this difference will require detailed investigation.

The importance of FLC variation in adaptation for natural populations is well established (Méndez-Vigo et al., 2011; Sánchez-Bermejo et al., 2012; Dittmar et al., 2014; Li et al., 2014; Duncan et al., 2015; Ågren et al., 2017; Bloomer and Dean, 2017). However, we found that even in a challengingly warm year, vernalization requirement saturated before midwinter across three climates (Figure 6). This response had been seen previously in North Sweden in the locally-adapted Löv-1 accession as a reaction to the extreme winters (Duncan et al., 2015). However, we find that this is a general response in all our tested accessions. The principle exceptions were the vin3 and vrn mutants, which had notably delayed flowering in both years at the Norwich site. The consequences of incomplete vernalization are severe – in our 2016–7 transfer experiments this led to delayed flowering and reduced fecundity (Figure 6, Figure 6—figure supplement 7), and several field experiments have found a general trend towards earlier flowering promoting fitness in environments with warmer winters (Ågrena et al., 2013; Fournier-Level et al., 2013; Grillo et al., 2013; Dittmar et al., 2014; Ågren et al., 2017; Exposito-Alonso et al., 2018). In 2014–5, the high synchronicity of flowering in all the accessions and NILs after winter and the fact that flowering aligned with spring across our field sites (Figure 6—figure supplement 2), suggests that in most plants vernalization has adapted to reduce the delaying effect of FLC on flowering as early as possible.

Nevertheless, we observed that the Swedish, cold-winter-adapted accessions and FLC haplotypes associated with slow vernalization expressed the highest FLC levels throughout autumn and early winter (Figures 2 and 3, Figure 2—figure supplement 1, Figure 3—figure supplement 1). In North Sweden in 2016–7, we captured behaviour for a warmer growing season that revealed an adaptive role for these high FLC expression levels. There was a relatively warm September that year with a long period with less precipitation (Swedish Meteorological and Hydrological Institute, 2020, www.smhi.se/data/meteorologi/ladda-ner-meteorologiska-observationer), which required us to water the plants to avoid drought stress. This, in combination with the earlier sowing (warmer and longer days) meant that the equivalent period of growing time for the plants (relative to their germination time) was more inductive to growth and flowering. This allowed us to capture a different behaviour. Plants are exposed to both types of the years we recorded, since the timing of both sowing dates was within the natural germination range, although in natural environments seed dormancy has a strong influence on phenology and is highly responsive to temperature and microclimate, and affected by FLC itself (Springthorpe and Penfield, 2015; Kerdaffrec et al., 2016; Marcer et al., 2018). In our experiments, in plants with a haplotype characteristic of a slow-vernalizing accession, including the locally-adapted Swedish accessions, the higher level of FLC expression protected against precocious flowering and its consequent reduced survival (Figure 7, Figure 7—figure supplement 2). These rare, but highly selective occurrences, may play a role in local adaptation, although we do not know the reason behind the high mortality in this year. However, that the effects of these haplotypes are only revealed occasionally is a logical consequence of the fact that the flowering time genes can have strong or weak effects depending on the environment (Wilczek et al., 2009; Sasaki et al., 2015; Burghardt et al., 2016; Fournier-Level et al., 2016; Sasaki et al., 2018; Taylor et al., 2019).

FLC also controls fecundity as well as survival (Ågrena et al., 2013). Li et al., 2014 found that FLC haplotypes from SV accessions produced lower seed weight compared to those from RV accessions in non-saturating vernalization conditions, though the mechanism for this effect is unknown. In the field, silique production is closely linked to branch production (Figure 7; Taylor et al., 2019). In Arabidopsis, saturation of vernalization requirement is known to increase flowering branch production, particularly rosette branch production, and this effect is linked to FLC (Figure 1—figure supplements 1–2; Huang et al., 2013; de Jong et al., 2019). As expected, FLC levels in autumn did not correlate with branch production in spring (Figure 7—figure supplement 2H), and in Norwich 2014–5, there was little variation in branch production. However, we found that under the conditions in the field in North Sweden, branch production was negatively related to a factor we named ‘FLC post-vern’, which encoded the relationship between FLC levels and subsequent flowering in warm controlled conditions (Figure 7). Variation in this factor probably derives from regulatory differences at FLC post-cold, such as the reactivation phenotype of the Löv-1 FLC allele (Shindo et al., 2006; Coustham et al., 2012; Duncan et al., 2015; Qüesta et al., 2020), allowing FLC repression of flowering to saturate at the shoot apical and axillary meristems at different rates, a phenomenon that occurs in the perennial relative Arabis alpina (Wang et al., 2009; Lazaro et al., 2018). Why the field conditions in Sweden, but not Norwich, revealed this effect is not yet clear.

In summary, our detailed analysis of the different phases of FLC silencing through winters in distinct climates, over multiple years, has shed light on adaptive aspects of the vernalization mechanism. Autumnal FLC expression, made up from FLC starting levels and early phases of FLC silencing, is the major determinant for variation in FLC levels during vernalization (Figure 5). FLC downregulation aligns flowering response to spring and non-coding variation affects this alignment in different climatic conditions and year-on-year fluctuations in natural temperature profiles. In a changing climate, understanding the complex genotype-by- environment interactions that govern timing mechanisms will become ever more important.

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

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Author details

1. Jo Hepworth

   Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

   Contribution

   Data curation, Formal analysis, Supervision, Investigation, Visualization, Methodology, Writing - original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4621-8414

2. Rea L Antoniou-Kourounioti

   Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom

   Contribution

   Data curation, Formal analysis, Supervision, Investigation, Visualization, Writing - original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5226-521X

3. Kristina Berggren

   Department of Natural Sciences, Mid Sweden University, Sundsvall, Sweden

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7859-9928

4. Catja Selga

   Department of Biology, Lund University, Lund, Sweden

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8683-1291

5. Eleri H Tudor

   Crop Genetics, John Innes Centre, Norwich, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

6. Bryony Yates

   Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

   Contribution

   Investigation

   Competing interests

   No competing interests declared

7. Deborah Cox

   Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

   Contribution

   Investigation

   Competing interests

   No competing interests declared

8. Barley Rose Collier Harris

   Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5745-1812

9. Judith A Irwin

   Crop Genetics, John Innes Centre, Norwich, United Kingdom

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology

   Competing interests

   No competing interests declared

10. Martin Howard

    Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-7670-0781

11. Torbjörn Säll

    Department of Biology, Lund University, Lund, Sweden

    Contribution

    Conceptualization, Supervision, Funding acquisition, Investigation, Methodology, Writing - review and editing

    Competing interests

    No competing interests declared

12. Svante Holm

    Department of Natural Sciences, Mid Sweden University, Sundsvall, Sweden

    Contribution

    Conceptualization, Supervision, Funding acquisition, Investigation, Methodology, Writing - review and editing

    For correspondence

    Svante.Holm@miun.se

    Competing interests

    No competing interests declared

13. Caroline Dean

    Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom

    Contribution

    Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Project administration, Writing - review and editing

    For correspondence

    caroline.dean@jic.ac.uk

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-6555-3525

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