Trends in Plant Science
ReviewThe molecular basis of vernalization-induced flowering in cereals
Section snippets
Vernalization promotes flowering in cereals
Wheat (Triticum aestivum) and barley (Hordeum vulgare) are grown in temperate regions throughout the world and account for approximately a third of total world grain production. Flowering of these cereals can be accelerated by prolonged exposure to cold – vernalization. Vernalization occurs during winter when temperatures are between 0° and 10 °C 1, 2. A few weeks of cold are often sufficient to promote flowering, but longer periods can accelerate flowering to a greater extent, up to the point
VRN1 is induced by vernalization and promotes the transition to reproductive development
Vernalization accelerates flowering by promoting the switch from vegetative to reproductive development 2, 10. This transition is controlled by genes that regulate the identity of the shoot apical meristem to determine which organs are produced by the shoot apex [11]. During vegetative development the shoot apical meristem produces leaf primordia (Figure 1a,b). At the beginning of reproductive development the shoot apex acquires inflorescence meristem identity, and secondary meristems, known as
FT accelerates flowering in long days
Flowering of barley and wheat can be accelerated by long days. Day-lengths above a threshold, typically more than 10 h, are required to accelerate flowering. Longer day-lengths promote flowering to a greater extent, up to a limit, typically between 13 and 18 h, beyond which there is no further effect on flowering time [17]. Long days accelerate flowering by accelerating reproductive apex development 10, 17.
The day-length response is mediated by FT. FT encodes a polyethanolamine binding protein
VRN2 is a floral repressor that integrates the vernalization and day-length responses
Some day-length sensitive varieties have a strong requirement for vernalization, which is a pre-requisite for long-day induction of flowering 1, 17. In field conditions, crops sown in late summer or autumn are insensitive to long days and grow vegetatively until vernalized during winter. Following winter, plants are able to respond to long days, which accelerate reproductive apex development as days lengthen in spring (Figure 2).
VRN2 is a floral repressor that delays flowering until plants are
In vernalization-requiring varieties, VRN1, VRN2 and FT interact to promote spring flowering
We propose that regulatory interactions between VRN1, VRN2 and FT integrate vernalization and long-day responses. Plants sown in late summer or autumn do not flower before winter because both the vernalization and day-length response pathways are inactive; VRN1 expression is low and VRN2 activity represses long-day induction of FT. Low temperatures during winter slow shoot apex development and induce expression of VRN1. As temperatures rise towards the end of winter, the rate of apex
High basal levels of VRN1 expression can substitute for vernalization
Alleles of VRN1 that have high basal levels of VRN1 expression can substitute for vernalization 6, 7, 8. These alleles accelerate inflorescence initiation and are dominant to alleles that are expressed only after vernalization 1, 3. Alleles of VRN1 that have high basal expression levels also repress VRN2 29, 31. This might allow long days to induce expression of FT and further accelerate floral development in day-length-sensitive varieties. There are a range of dominant alleles of VRN1 with
Activation of the day-length response can overcome the vernalization requirement
Varieties of wheat or barley that lack a functional copy of VRN2 do not require vernalization to flower 1, 9. In T. monococcum, non-functional VRN2 alleles have a mutation that causes an amino acid substitution at a conserved arginine in the CCT domain [9]. In barley, there are naturally occurring deletions of VRN2 9, 35. These cause early flowering in long days, but not in short-days [36], consistent with the suggestion that VRN2 acts to block the promotion of flowering by long days [29]. FT
The molecular basis of spring flowering in Arabidopsis
Vernalization promotes spring flowering in many ecotypes of Arabidopsis. The central regulator of vernalization-induced flowering in Arabidopsis is a MADS box transcription factor gene, FLOWERING LOCUS C (FLC) 37, 38. FLC is a floral repressor that delays both the transition to reproductive apex development and long-day promotion of flowering until plants have experienced vernalization 37, 38.
FLC represses transcription of two floral promoters; FT and SUPPRESSOR OF OVER-EXPRESSION OF CONSTANS 1
Integration of vernalization and day-length responses occurs by a similar mechanism in Arabidopsis and cereals
The day-length response pathway is conserved in Arabidopsis and cereals: in both the monocot and dicot plants, CO up-regulates FT in inductive day-lengths to promote flowering 18, 19, 22, 23, 24, 25. The mechanism that integrates vernalization status and day-length responses is also similar; vernalization is required to allow long-day induction of FT (Figure 4). In Arabidopsis a single gene, FLC, represses FT to establish the vernalization requirement, and is down-regulated by prolonged cold to
Do conserved epigenetic mechanisms regulate the vernalization response in Arabidopsis and cereals?
In Arabidopsis, transcriptional repression of FLC by vernalization is mediated by protein complexes that chemically modify histones 46, 47. These deacetylate or methylate specific residues of histones at the FLC locus, and presumably trigger conformational changes in chromatin structure that limit access of transcriptional machinery to the FLC gene 46, 47. Histones bound to regions of the first intron of FLC are targets for histone deacetylation and histone methylation 46, 47, 48, 49, and these
Conclusions
The cloning of VRN1, VRN2 and FT has facilitated progress in understanding how flowering is regulated by vernalization and day-length in cereals. Further investigation of the function of these genes, using reverse genetics or reporter gene constructs in transgenic plants, should offer further insights into how flowering time is controlled in cereals. It will be possible to examine whether VRN1 is subject to epigenetic regulation during vernalization, and how VRN1 interacts with VRN2 to control
Update
Faure et al. [52] have recently described the expression patterns and chromosomal locations of four other barley FT-like genes and Shitsukawa et al. [53] have described mutant wheat that lacks VRN1 and does not flower.
Acknowledgments
We gratefully acknowledge the Commonwealth Scientific Research Organisation and the Grains Research and Development Corporation for supporting this research.
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