[en] A requirement for vernalization, the process by which prolonged cold exposure provides competence to flower, is an important adaptation to temperate climates that ensures flowering does not occur before the onset of winter. In temperate grasses, vernalization results in the up-regulation of VERNALIZATION1 (VRN1) to establish competence to flower; however, little is known about the mechanism underlying repression of VRN1 in the fall season, which is necessary to establish a vernalization requirement. Here, we report that a plant-specific gene containing a bromo-adjacent homology and transcriptional elongation factor S-II domain, which we named REPRESSOR OF VERNALIZATION1 (RVR1), represses VRN1 before vernalization in Brachypodium distachyon. That RVR1 is upstream of VRN1 is supported by the observations that VRN1 is precociously elevated in an rvr1 mutant, resulting in rapid flowering without cold exposure, and the rapid-flowering rvr1 phenotype is dependent on VRN1. The precocious VRN1 expression in rvr1 is associated with reduced levels of the repressive chromatin modification H3K27me3 at VRN1, which is similar to the reduced VRN1 H3K27me3 in vernalized plants. Furthermore, the transcriptome of vernalized wild-type plants overlaps with that of nonvernalized rvr1 plants, indicating loss of rvr1 is similar to the vernalized state at a molecular level. However, loss of rvr1 results in more differentially expressed genes than does vernalization, indicating that RVR1 may be involved in processes other than vernalization despite a lack of any obvious pleiotropy in the rvr1 mutant. This study provides an example of a role for this class of plant-specific genes.
National Science Foundation (Grant IOS-1258126; to RMA); Department of Energy Great Lakes Bioenergy Research Center (DOE BER Office of Science DE-FCO2-07ER64494) (to R.M.A. and C.W.); Wallonie-Bruxelles International fellowships (to F.B.); National Institutes of Health-sponsored predoctoral training fellowship to the University of Wisconsin Genetics Training program (to D.P.W.); Gordon and Betty Moore Foundation and the Life Sciences Research Foundation for their postdoctoral fellowship (T.S.R.).
Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:191-238.
Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001-1013.
Shrestha R, Gómez-Ariza J, Brambilla V, Fornara F (2014) Molecular control of seasonal flowering in rice, Arabidopsis and temperate cereals. Ann Bot (Lond) 114: 1445-1458.
Fjellheim S, Boden S, Trevaskis B (2014) The role of seasonal flowering responses in adaptation of grasses to temperate climates. Front Plant Sci 5:431.
Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178-184.
Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot (Lond) 103:1165-1172.
Distelfeld A, Dubcovsky J (2010) Characterization of the maintained vegetative phase deletions from diploid wheat and their effect on VRN2 and FT transcript levels. Mol Genet Genomics 283:223-232.
Corbesier L, et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030-1033.
Yan L, et al. (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581-19586.
Sasani S, et al. (2009) The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). J Exp Bot 60:2169-2178.
Yan L, et al. (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640-1644.
Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147:355-366.
Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANSlike gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855-1867.
Dubcovsky J, et al. (2006) Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol 60:469-480.
Chen A, Dubcovsky J (2012) Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet 8:e1003134.
Yan L, et al. (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263-6268.
Preston JC, Kellogg EA (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174:421-437.
Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661-2675.
Shimada S, et al. (2009) A genetic network of flowering-time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J 58:668-681.
Deng W, et al. (2015) Direct links between the vernalization response and other key traits of cereal crops. Nat Commun 6:5882.
Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B (2009) Vernalizationinduced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Natl Acad Sci USA 106:8386-8391.
Distelfeld A, Tranquilli G, Li C, Yan L, Dubcovsky J (2009) Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol 149:245-257.
Brutnell TP, Bennetzen JL, Vogel JP (2015) Brachypodium distachyon and Setaria viridis: Model genetic systems for the grasses. Annu Rev Plant Biol 66:465-485.
Higgins JA, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS One 5:e10065.
Woods DP, Amasino RM (2015) Dissecting the control of flowering time in grasses using Brachypodium distachyon. Genetics and Genomics of Brachypodium, ed Vogel PJ (Springer International, Cham, Switzerland), pp 259-273.
Woods DP, et al. (2017) Genetic architecture of flowering-time variation in Brachypodium distachyon. Plant Physiol 173:269-279.
Bettgenhaeuser J, et al. (2017) Natural variation in Brachypodium links vernalization and flowering time loci as major flowering determinants. Plant Physiol 173:256-268.
Ream TS, et al. (2014) Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol 164:694-709.
Lv B, et al. (2014) Characterization of FLOWERING LOCUS T1 (FT1) gene in Brachypodium and wheat. PLoS One 9:e94171.
Woods DP, McKeown MA, Dong Y, Preston JC, Amasino RM (2016) Evolution of VRN2/Ghd7-like genes in vernalization-mediated repression of grass flowering. Plant Physiol 170:2124-2135.
Woods DP, Ream TS, Amasino RM (2014) Memory of the vernalized state in plants including the model grass Brachypodium distachyon. Front Plant Sci 5:99.
Ream TS, Woods DP, Amasino RM (2012) The molecular basis of vernalization in different plant groups. Cold Spring Harb Symp Quant Biol 77:105-115.
Woods DP, Ream TS, Minevich G, Hobert O, Amasino RM (2014) PHYTOCHROME C is an essential light receptor for photoperiodic flowering in the temperate grass, Brachypodium distachyon. Genetics 198:397-408.
Minevich G, Park DS, Blankenberg D, Poole RJ, Hobert O (2012) CloudMap: A cloudbased pipeline for analysis of mutant genome sequences. Genetics 192:1249-1269.
Callebaut I, Courvalin JC, Mornon JP (1999) The BAH (bromo-adjacent homology) domain: A link between DNA methylation, replication and transcriptional regulation. FEBS Lett 446:189-193.
Su Z, Denu JM (2016) Reading the combinatorial histone language. ACS Chem Biol 1:564-574.
Yang N, Xu R-M (2013) Structure and function of the BAH domain in chromatin biology. Crit Rev Biochem Mol Biol 48:211-221.
Kim B, et al. (2007) The transcription elongation factor TFIIS is a component of RNA polymerase II preinitiation complexes. Proc Natl Acad Sci USA 104:16068-16073.
Johanson U, et al. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344-347.
Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949-956.
Bouché F, Woods DP, Amasino RM (2017) Winter memory throughout the plant kingdom: Different paths to flowering. Plant Physiol 173:27-35.
Ruelens P, et al. (2013) FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nat Commun 4:2280.
Wood CC, et al. (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103:14631-14636.
De Lucia F, Crevillen P, Jones AME, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831-16836.
Woods DP, Hope CL, Malcomber ST (2011) Phylogenomic analyses of the BARREN STALK1/LAX PANICLE1 (BA1/LAX1) genes and evidence for their roles during axillary meristem development. Mol Biol Evol 28:2147-2159.
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221-224.
Haring M, et al. (2007) Chromatin immunopreciptation: Optimization, quantitative analysis and data normalization. Plant Methods 3:11.
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550.