[en] Perception of seasonal cues is critical for reproductive success in many plants. Exposure to winter cold is a cue that can confer competence to flower in the spring via a process known as vernalization. In certain grasses, exposure to short days is another winter cue that can lead to a vernalized state. In Brachypodium distachyon, we find that natural variation for the ability of short days to confer competence to flower is due to allelic variation of the FLOWERING LOCUS T (FT1) paralog FT-like9 (FTL9). An active FTL9 allele is required for the acquisition of floral competence, demonstrating a novel role for a member of the FT family of genes. Loss of the short- day vernalization response appears to have arisen once in B. distachyon and spread through diverse lineages indicating that this loss has adaptive value, perhaps by delaying spring flowering until the danger of cold damage to flowers has subsided.
Bouché F, Woods DP, Amasino RM. 2017. Winter memory throughout the plant kingdom: different paths to flowering. Plant Physiology 173:27–35. DOI: https://doi.org/10.1104/pp.16.01322, PMID: 27756819
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. DOI: https://doi.org/10.1093/bioinformatics/btm308, PMID: 17586829
Casao MC, Karsai I, Igartua E, Gracia MP, Veisz O, Casas AM. 2011a. Adaptation of barley to mild winters: a role for PPDH2. BMC Plant Biology 11:164. DOI: https://doi.org/10.1186/1471-2229-11-164, PMID: 22098798
Casao MC, Igartua E, Karsai I, Lasa JM, Gracia MP, Casas AM. 2011b. Expression analysis of vernalization and day-length response genes in barley (Hordeum vulgare L.) indicates that VRNH2 is a repressor of PPDH2 (HvFT3) under long days. Journal of Experimental Botany 62:1939–1949. DOI: https://doi.org/10.1093/jxb/erq382, PMID: 21131547
Chouard P. 1960. Vernalization and its relations to dormancy. Annual Review of Plant Physiology 11:191–238. DOI: https://doi.org/10.1146/annurev.pp.11.060160.001203
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033. DOI: https://doi.org/10.1126/science.1141752, PMID: 17446353
Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L. 2006. Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Molecular Biology 60:469–480. DOI: https://doi.org/10.1007/s11103-005-4814-2, PMID: 16525885
Evans LT. 1987. Short day induction of inflorescence initiation in some winter wheat varieties. Functional Plant Biology 14:277–286. DOI: https://doi.org/10.1071/PP9870277
Faure S, Higgins J, Turner A, Laurie DA. 2007. The flowering locus T-like gene family in barley (Hordeum vulgare). Genetics 176:599–609. DOI: https://doi.org/10.1534/genetics.106.069500, PMID: 17339225
Fjellheim S, Boden S, Trevaskis B. 2014. The role of seasonal flowering responses in adaptation of grasses to temperate climates. Frontiers in Plant Science 5:431. DOI: https://doi.org/10.3389/fpls.2014.00431, PMID: 25221560
Gordon SP, Contreras-Moreira B, Woods DP, Des Marais DL, Burgess D, Shu S, Stritt C, Roulin AC, Schackwitz W, Tyler L, Martin J, Lipzen A, Dochy N, Phillips J, Barry K, Geuten K, Budak H, Juenger TE, Amasino R, Caicedo AL, et al. 2017. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nature Communications 8:2184. DOI: https://doi.org/10.1038/s41467-017-02292-8, PMID: 29259172
Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27:221–224. DOI: https://doi.org/10.1093/molbev/msp259, PMID: 19854763
Halliwell J, Borrill P, Gordon A, Kowalczyk R, Pagano ML, Saccomanno B, Bentley AR, Uauy C, Cockram J. 2016. Systematic Investigation of flowering locus t-like poaceae gene families identifies the short-day expressed flowering pathway gene, TaFT3 in Wheat (Triticum aestivum L.). Frontiers in Plant Science 7:857. DOI: https://doi.org/10.3389/fpls.2016.00857, PMID: 27458461
Heide OM. 1994. Control of flowering and reproduction in temperate grasses. New Phytologist 128:347–362. DOI: https://doi.org/10.1111/j.1469-8137.1994.tb04019.x
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. DOI: https://doi.org/10.1371/journal. pone.0010065, PMID: 20419097 Kikuchi R, Kawahigashi H, Ando T, Tonooka T, Handa H. 2009. Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiology 149:1341–1353. DOI: https://doi.org/10.1104/pp.108.132134, PMID: 19168644 Laurie DA, Pratchett N, Snape JW, Bezant JH. 1995. RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. Genome 38:575–585. DOI: https://doi.org/10.1139/g95-074, PMID: 18470191 Lazakis CM, Coneva V, Colasanti J. 2011. ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. Journal of Experimental Botany 62: 4833–4842. DOI: https://doi.org/10.1093/jxb/err129, PMID: 21730358 Le Corre V, Roux F, Reboud X. 2002. DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Molecular Biology and Evolution 19:1261–1271. DOI: https://doi.org/10.1093/oxfordjournals.molbev.a004187, PMID: 12140238 Lomax A, Woods DP, Dong Y, Bouché F, Rong Y, Mayer KS, Zhong X, Amasino RM. 2018. An ortholog of CURLY LEAF/ENHANCER OF ZESTE like-1 is required for proper flowering in Brachypodium distachyon. The Plant Journal: For Cell and Molecular Biology 93:871–882. DOI: https://doi.org/10.1111/tpj.13815, PMID: 29314414 Lv B, Nitcher R, Han X, Wang S, Ni F, Li K, Pearce S, Wu J, Dubcovsky J, Fu D. 2014. Characterization of FLOWERING LOCUS T1 (FT1) gene in Brachypodium and wheat. PLOS ONE 9:e94171. DOI: https://doi.org/10. 1371/journal.pone.0094171, PMID: 24718312 Lyons E, Freeling M. 2008. How to usefully compare homologous plant genes and chromosomes as DNA sequences. The Plant Journal 53:661–673. DOI: https://doi.org/10.1111/j.1365-313X.2007.03326.x, PMID: 1826 9575
Mann DG, Lafayette PR, Abercrombie LL, King ZR, Mazarei M, Halter MC, Poovaiah CR, Baxter H, Shen H, Dixon RA, Parrott WA, Neal Stewart C. 2012. Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species. Plant Biotechnology Journal 10:226– 236. DOI: https://doi.org/10.1111/j.1467-7652.2011.00658.x, PMID: 21955653
Meng X, Muszynski MG, Danilevskaya ON. 2011. The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. The Plant Cell 23:942–960. DOI: https://doi.org/10.1105/tpc.110. 081406, PMID: 21441432
Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, Dugas DV, Klein PE, Mullet JE. 2011. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. PNAS 108:16469–16474. DOI: https://doi.org/10.1073/pnas.1106212108, PMID: 21930 910
Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B. 2009. Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. PNAS 106:8386–8391. DOI: https://doi.org/10.1073/pnas.0903566106, PMID: 19416817
Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400. DOI: https://doi.org/10.1126/science.1197004, PMID: 21127254
Preston JC, Kellogg EA. 2008. Discrete developmental roles for temperate cereal grass VERNALIZATION1/ FRUITFULL-like genes in flowering competency and the transition to flowering. Plant Physiology 146:265–276. DOI: https://doi.org/10.1104/pp.107.109561, PMID: 18024551
Purvis ON, Gregory FG. 1937. Studies in vernalisation of cereals: I. A Comparative Study of Vernalisation of Winter Rye by Low Temperature and by Short Days. Annals of Botany 1:1–26. DOI: https://doi.org/10.1093/oxfordjournals.aob.a083490
Ream TS, Woods DP, Amasino RM. 2012. The molecular basis of vernalization in different plant groups. Cold Spring Harbor Symposia on Quantitative Biology 77:105–115. DOI: https://doi.org/10.1101/sqb.2013.77. 014449, PMID: 23619014
Ream TS, Woods DP, Schwartz CJ, Sanabria CP, Mahoy JA, Walters EM, Kaeppler HF, Amasino RM. 2014. Interaction of photoperiod and vernalization determines flowering time of brachypodium distachyon. Plant Physiology 164:694–709. DOI: https://doi.org/10.1104/pp.113.232678
Sampson DR, Burrows VD. 1972. Influence of photoperiod, short-day vernalization, and cold vernalization on days to heading in avena species and cultivars. Canadian Journal of Plant Science 52:471–482. DOI: https://doi.org/10.4141/cjps72-077
Sancho R, Cantalapiedra CP, López-Alvarez D, Gordon SP, Vogel JP, Catalán P, Contreras-Moreira B. 2018. Comparative plastome genomics and phylogenomics of Brachypodium: flowering time signatures, introgression and recombination in recently diverged ecotypes. New Phytologist 218:1631–1644. DOI: https://doi.org/10. 1111/nph.14926, PMID: 29206296
Sasani S, Hemming MN, Oliver SN, Greenup A, Tavakkol-Afshari R, Mahfoozi S, Poustini K, Sharifi HR, Dennis ES, Peacock WJ, Trevaskis B. 2009. The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). Journal of Experimental Botany 60:2169– 2178. DOI: https://doi.org/10.1093/jxb/erp098, PMID: 19357429
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036. DOI: https://doi.org/10.1126/science.1141753, PMID: 17446351
Trevaskis B, Hemming MN, Dennis ES, Peacock WJ. 2007. The molecular basis of vernalization-induced flowering in cereals. Trends in Plant Science 12:352–357. DOI: https://doi.org/10.1016/j.tplants.2007.06.010, PMID: 1762 9542
Vogel J, Hill T. 2008. High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Reports 27:471–478. DOI: https://doi.org/10.1007/s00299-007-0472-y, PMID: 17 999063
Whittaker C, Dean C. 2017. The FLC Locus: A platform for discoveries in epigenetics and adaptation. Annual Review of Cell and Developmental Biology 33:555–575. DOI: https://doi.org/10.1146/annurev-cellbio-100616-060546, PMID: 28693387
Wolabu TW, Zhang F, Niu L, Kalve S, Bhatnagar-Mathur P, Muszynski MG, Tadege M. 2016. Three FLOWERING LOCUS T-like genes function as potential florigens and mediate photoperiod response in sorghum. New Phytologist 210:946–959. DOI: https://doi.org/10.1111/nph.13834, PMID: 26765652
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. Molecular Biology and Evolution 28:2147–2159. DOI: https://doi.org/10.1093/molbev/msr036, PMID: 21297156
Woods DP, Ream TS, Amasino RM. 2014a. Memory of the vernalized state in plants including the model grass Brachypodium distachyon. Frontiers in Plant Science 5:99. DOI: https://doi.org/10.3389/fpls.2014.00099, PMID: 24723926
Woods DP, Ream TS, Minevich G, Hobert O, Amasino RM. 2014b. PHYTOCHROME C is an essential light receptor for photoperiodic flowering in the temperate grass, Brachypodium distachyon. Genetics 198:397–408. DOI: https://doi.org/10.1534/genetics.114.166785, PMID: 25023399
Woods DP, Amasino RM. 2015. Dissecting the Control of Flowering Time in Grasses Using Brachypodium Distachyon. In: Vogel PJ (Ed). Genetics and Genomics of Brachypodium. Cham, Switzerland: Springer International. DOI: https://doi.org/10.1007/7397_2015_10
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 Physiology 170:2124–2135. DOI: https://doi.org/10.1104/pp.15.01279, PMID: 26848096
Woods DP, Ream TS, Bouché F, Lee J, Thrower N, Wilkerson C, Amasino RM. 2017b. Establishment of a vernalization requirement in brachypodium distachyon requires repressor of vernalization1. PNAS 114:6623– 6628. DOI: https://doi.org/10.1073/pnas.1700536114, PMID: 28584114
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics 40:761–767. DOI: https://doi.org/10.1038/ng.143, PMID: 18454147
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J. 2003. Positional cloning of the wheat vernalization gene VRN1. PNAS 100:6263–6268. DOI: https://doi.org/10.1073/pnas.0937399100, PMID: 12730378
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J. 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644. DOI: https://doi.org/10.1126/science.1094305, PMID: 15016992
Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J. 2006. The wheat and barley vernalization gene VRN3 is an orthologue of FT. PNAS 103:19581–19586. DOI: https://doi. org/10.1073/pnas.0607142103, PMID: 17158798