Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

The role of FLOWERING LOCUS C in vernalization of Brassica: the importance of vernalization research in the face of climate change

Daniel J. Shea A , Etsuko Itabashi B , Satoko Takada C , Eigo Fukai A , Tomohiro Kakizaki B , Ryo Fujimoto C D and Keiichi Okazaki A D
+ Author Affiliations
- Author Affiliations

A Graduate School of Science and Technology, Niigata University, Ikarashi-ninocho, Niigata 950-2181, Japan.

B Institute of Vegetable and Floriculture Science, NARO, Kusawa, Ano, Tsu, Mie 514-2392, Japan.

C Graduate School of Agricultural Science, Kobe University, Rokkodai, Nada-ku, Kobe 657-8501, Japan.

D Corresponding authors. Emails: leo@people.kobe-u.ac.jp; okazaki@agr.niigata-u.ac.jp

Crop and Pasture Science 69(1) 30-39 https://doi.org/10.1071/CP16468
Submitted: 26 December 2016  Accepted: 10 April 2017   Published: 19 June 2017

Abstract

As climatic changes occur over the coming decades, our scientific understanding of plant responses to environmental cues will become an increasingly important consideration in the breeding of agricultural crops. This review provides a summary of the literature regarding vernalization research in Brassicaceae, covering both the historical origins of vernalization research and current understanding of the molecular mechanisms behind the regulatory pathways involved in vernalization and subsequent inflorescence. We discuss the evolutionarily conserved biology between the model organism Arabidopsis thaliana and the Brassica genus of crop cultivars and contrast the differences between the genera to illustrate the importance of Brassica-specific research into vernalization.

Additional keywords: epigenetics, flowering time, histone modification.


References

Aikawa S, Kobayashi MJ, Satake A, Shimizu KK, Kudoh H (2010) Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proceedings of the National Academy of Sciences of the United States of America 107, 11632–11637.
Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1eksbc%3D&md5=483f2cf5a8b7630fbac13eb22de0107eCAS |

Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. The Plant Cell 16, 2553–2559.
Vernalization, competence, and the epigenetic memory of winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVSiu70%3D&md5=88dd6e9d9bf0b15285b422d79abeec54CAS |

Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiology 154, 516–520.
The timing of flowering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCkt73P&md5=79f0535a19ca6db7d7f9391946241791CAS |

Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105–108.
A Polycomb-based switch underlying quantitative epigenetic memory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlaksb4%3D&md5=efaeb8c56b02bc218f72cc671207f489CAS |

Axelsson T, Shavorskaya O, Lagercrantz U (2001) Multiple flowering time QTLs within several Brassica species could be the result of duplicated copies of one ancestral gene. Genome 44, 856–864.
Multiple flowering time QTLs within several Brassica species could be the result of duplicated copies of one ancestral gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos12ls7o%3D&md5=d7bc1cc796a345375ba6a574ea34448aCAS |

Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167.
Vernalization requires epigenetic silencing of FLC by histone methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFOnug%3D%3D&md5=5c2fa834a6ea538fecffe37d949ced2fCAS |

Buzas DM, Tamada Y, Kurata T (2012) FLC: a hidden polycomb response element shows up in silence. Plant & Cell Physiology 53, 785–793.
FLC: a hidden polycomb response element shows up in silence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntVSjtL8%3D&md5=3bcd00708878605e0680d2bfd910efa9CAS |

Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953.
Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOmsr%2FK&md5=1a8efabc0ad3089b351cba8f65b3c609CAS |

Cheng F, Wu J, Wang X (2014) Genome triplication drove the diversification of Brassica plants. Horticulture Research 1, 14024
Genome triplication drove the diversification of Brassica plants.Crossref | GoogleScholarGoogle Scholar |

Choi K, Kim J, Hwang HJ, Kim S, Park C, Kim SY, Lee I (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. The Plant Cell 23, 289–303.
The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCksro%3D&md5=9935e07877d8a7f8cb3473572f20ddd1CAS |

Chouard P (1960) Vernalization and its relations to dormancy. Annual Review of Plant Physiology 11, 191–238.
Vernalization and its relations to dormancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXntFenug%3D%3D&md5=c185780536b1de02a2ff6650e87832d5CAS |

Coustham V, Li P, Strange A, Lister C, Song J, Dean C (2012) Quantitative modulation of Polycomb silencing underlies natural variation in vernalization. Science 337, 584–587.
Quantitative modulation of Polycomb silencing underlies natural variation in vernalization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWhsbbN&md5=6e237da6494b37ac0d6d90bebaa943faCAS |

Crevillén P, Dean C (2011) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Current Opinion in Plant Biology 14, 38–44.
Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context.Crossref | GoogleScholarGoogle Scholar |

Csorba T, Questa JI, Sun Q, Dean C (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proceedings of the National Academy of Sciences of the United States of America 111, 16160–16165.
Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVWmsLzF&md5=64c0830da2fc9fba7e16da47ec02823bCAS |

Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. The Plant Cell 19, 74–83.
Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFynsbc%3D&md5=ad535de1ebc70b4e6bedc6d4454ce5a4CAS |

Fadina OA, Khavkin EE (2014) The vernalization gene FRIGIDA in cultivated Brassica species. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 61, 309–317.
The vernalization gene FRIGIDA in cultivated Brassica species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntFCqs7k%3D&md5=a319c5ea4a62d534f9961a4d56bd1cc5CAS |

Feng W, Jacob Y, Veley KM, Ding L, Yu X, Choe G, Michaels SD (2011) Hypomorphic alleles reveal FCA-independent roles for FY in the regulation of FLOWERING LOCUS C. Plant Physiology 155, 1425–1434.
Hypomorphic alleles reveal FCA-independent roles for FY in the regulation of FLOWERING LOCUS C.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFOrtb0%3D&md5=a0de9a90de4fc39261f4b56103e52c10CAS |

Franks SJ, Perez-Sweeney B, Strahl M, Nowogrodzki A, Weber JJ, Lalchan R, Jordan KP, Litt A (2015) Variation in the flowering time orthologs BrFLC and BrSOC1 in a natural population of Brassica rapa. PeerJ 3, e1339
Variation in the flowering time orthologs BrFLC and BrSOC1 in a natural population of Brassica rapa.Crossref | GoogleScholarGoogle Scholar |

Fujimoto R, Nishio T (2007) Self-incompatibility. Advances in Botanical Research 45, 139–154.
Self-incompatibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot12ktbw%3D&md5=35dcd4b8ef40d90fdaa0d20713421b01CAS |

Gassner G (1918) Beiträge zur physiologischen Charakteristik sommer und winteranueller Gewächse, insbesondere der Getreidepflanzen. Zeitschr Botanik 10, 417–480.

Geraldo N, Bäurle I, Kidou S, Hu X, Dean C (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiology 150, 1611–1618.
FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFeru7Y%3D&md5=7a96b8bf666f6c65674fe3bcdf0ed5bbCAS |

Groover AT (2005) What genes make a tree a tree? Trends in Plant Science 10, 210–214.
What genes make a tree a tree?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFelurg%3D&md5=705b02a9c6e332829400be9d9b885906CAS |

Härer L (1950) Die Vererbung des Blühalters früher und später sommereinjähriger Rassen von Arabidopsis thaliana (L.) Heynh. Beitraege zur Biologie der Pflanzen 28, 135

Hatfield J, Takle G (2014) Agriculture. In ‘Climate change impacts in the United States. The Third National Climate Assessment’. Ch. 6, pp. 150–174. (U.S. Global Change Research Program: Washington, DC)

He Y (2012) Chromatin regulation of flowering. Trends in Plant Science 17, 556–562.
Chromatin regulation of flowering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVejtLc%3D&md5=a72d1065bb56b0f26c47d58724b48172CAS |

He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes & Development 18, 2774–2784.
PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCjt7%2FP&md5=0ebcce4925948997c0bf0ce7558aa37dCAS |

Helliwell CA, Wood CC, Robertson M, Peacock WJ, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. The Plant Journal 46, 183–192.
The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVWntrw%3D&md5=7979e38ab90e298d94dbdaa9efa68f84CAS |

Helliwell CA, Robertson M, Finnegan EJ, Buzas DM, Dennis ES (2011) Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS One 6, e21513
Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFalsLc%3D&md5=9d71440a23dc4dfe4c16f67482f5b953CAS |

Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76–79.
Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpslej&md5=f9803167ffec8104ed815fbe325a4c31CAS |

Hong JK, Kim SY, Kim JS, Kim JA, Park BS, Lee YH (2011) Promoters of three Brassica rapa FLOWERING LOCUS C differentially regulate gene expression during growth and development in Arabidopsis. Genes & Genomics 33, 75–82.
Promoters of three Brassica rapa FLOWERING LOCUS C differentially regulate gene expression during growth and development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVKrur4%3D&md5=95d68f8d5f8d669b48303b34f4da3bcdCAS |

Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138, 4117–4129.
The control of developmental phase transitions in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOgsr3P&md5=696bae4d65ca36b2a70c6a83efb7cc26CAS |

Ietswaart R, Wu Z, Dean C (2012) Flowering time control: another window to the connection between antisense RNA and chromatin. Trends in Genetics 28, 445–453.
Flowering time control: another window to the connection between antisense RNA and chromatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSgurrF&md5=de6e0044c1b9142126c18b940f227f31CAS |

Irwin JA, Lister C, Soumpourou E, Zhang Y, Howell EC, Teakle G, Dean C (2012) Functional alleles of the flowering time regulator FRIGIDA in the Brassica oleracea genome. BMC Plant Biology 12, 21
Functional alleles of the flowering time regulator FRIGIDA in the Brassica oleracea genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xlt12isbw%3D&md5=09333b53db7225e42762102c450f91d3CAS |

Irwin JA, Soumpourou E, Lister C, Ligthart JD, Kennedy S, Dean C (2016) Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas. The Plant Journal 87, 597–605.
Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtF2htLfP&md5=31336e54ba39d5fabda5074f11e306b1CAS |

Jiang D, Wang Y, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS One 3, e3404
Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components.Crossref | GoogleScholarGoogle Scholar |

Jiang D, Gu X, He Y (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. The Plant Cell 21, 1733–1746.
Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFOks78%3D&md5=34adcde243e040c7fe1df4a03364c940CAS |

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVGiurw%3D&md5=aa07f1321759081c1b81061dc0278934CAS |

Kakizaki T, Kato T, Fukino N, Ishida M, Hatakeyama K, Matsumoto S (2011) Identification of quantitative trait loci controlling late bolting in Chinese cabbage (Brassica rapa L.) parental line Nou 6 gou. Breeding Science 61, 151–159.
Identification of quantitative trait loci controlling late bolting in Chinese cabbage (Brassica rapa L.) parental line Nou 6 gou.Crossref | GoogleScholarGoogle Scholar |

Kawanabe T, Osabe K, Itabashi E, Okazaki K, Dennis ES, Fujimoto R (2016) Development of primer sets that can verify the enrichment of histone modifications, and their application to examining vernalization-mediated chromatin changes in Brassica rapa L. Genes & Genetic Systems 91, 1–10.
Development of primer sets that can verify the enrichment of histone modifications, and their application to examining vernalization-mediated chromatin changes in Brassica rapa L.Crossref | GoogleScholarGoogle Scholar |

Kim DH, Sung S (2012) Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Current Opinion in Plant Biology 15, 51–56.
Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFCrsLs%3D&md5=fcbcc3ff76ff79ee3af928e83ac258a5CAS |

Kim SY, Park BS, Kwon SJ, Kim J, Lim MH, Park YD, Kim DY, Suh SC, Jin YM, Ahn JH, Lee YH (2007) Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Cell Reports 26, 327–336.
Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L. ssp. pekinensis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1CksLo%3D&md5=591b90223e3c12235eb11bad97016246CAS |

Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annual Review of Cell and Developmental Biology 25, 277–299.
Vernalization: winter and the timing of flowering in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVKisbvN&md5=370ccb231505fd752bd1a1f3a86d7b10CAS |

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=16f12429e9703844ca0bd6664e14f3dfCAS |

Kitamoto N, Yui S, Nishikawa K, Takahata Y, Yokoi S (2014) A naturally occurring long insertion in the first intron in the Brassica rapa FLC2 gene causes delayed bolting. Euphytica 196, 213–223.
A naturally occurring long insertion in the first intron in the Brassica rapa FLC2 gene causes delayed bolting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslylsrzE&md5=756b12b6425b3e4aa57ecf17f9ad1ffdCAS |

Kole C, Quijada P, Michaels SD, Amasino RM, Osborn TC (2001) Evidence for homology of flowering-time genes VFR2 from Brassica rapa and FLC from Arabidopsis thaliana. Theoretical and Applied Genetics 102, 425–430.
Evidence for homology of flowering-time genes VFR2 from Brassica rapa and FLC from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisVynsbs%3D&md5=445213cb1059182dee4966fa280037acCAS |

Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular & General Genetics 229, 57–66.
A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MznsFCmsw%3D%3D&md5=b183ad16346178c1aaea05ea2b711856CAS |

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=3836e6649a96bdacb261b7dad12c98d9CAS |

Li F, Kitashiba H, Inaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Research 16, 311–323.
A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2jsb%2FF&md5=4ae55febbafc782badbe1c6a82c09f9cCAS |

Li P, Filiault D, Box MS, Kerdaffrec E, van Oosterhout C, Wilczek AM, Schmitt J, McMullan M, Bergelson J, Nordborg M, Dean C (2014) Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes & Development 28, 1635–1640.
Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVWrtLrI&md5=ebc8e75201f5b568902776e967df6b8fCAS |

Li P, Tao Z, Dean C (2015) Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR. Genes & Development 29, 696–701.
Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXns1antLg%3D&md5=82f5347b192472b6c9c9ca5a1d61bf59CAS |

Li X, Zhang S, Bai J, He Y (2016) Tuning growth cycles of Brassica crops via natural antisense transcripts of BrFLC. Plant Biotechnology Journal 14, 905–914.
Tuning growth cycles of Brassica crops via natural antisense transcripts of BrFLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XjsFaqtb0%3D&md5=566942967550f2e87e6b6830fcc332edCAS |

Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Molecular Cell 28, 398–407.
The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC.Crossref | GoogleScholarGoogle Scholar |

Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3ʹ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327, 94–97.
Targeted 3ʹ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WksrfO&md5=84c7601d9186c6dc641ac3a60da510a5CAS |

Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IAP, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee TH, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nature Communications 5, 3930

Lou P, Zhao J, Kim JS, Shen S, Del Carpio DP, Song X, Jin M, Vreugdenhil D, Wang X, Koornneef M, Bonnema G (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. Journal of Experimental Botany 58, 4005–4016.
Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVSr&md5=dec8b767997de70838670994508799f7CAS |

Marquardt S, Boss PK, Hadfield J, Dean C (2006) Additional targets of the Arabidopsis autonomous pathway members, FCA and FY. Journal of Experimental Botany 57, 3379–3386.
Additional targets of the Arabidopsis autonomous pathway members, FCA and FY.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yqt7%2FL&md5=7a1f0ccc836dd1ff8275f7b4aa490cdaCAS |

Mateos JL, Madrigal P, Tsuda K, Rawat V, Richter R, Romera-Branchat M, Fornara F, Schneeberger K, Krajewski P, Coupland G (2015) Combinatorial activities of SHORT VEGETATIVE PHASE and FLOWERING LOCUS C define distinct modes of flowering regulation in Arabidopsis. Genome Biology 16, 31
Combinatorial activities of SHORT VEGETATIVE PHASE and FLOWERING LOCUS C define distinct modes of flowering regulation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C (2011) Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiology 157, 1942–1955.
Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. The Plant Cell 11, 949–956.
FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVajsLc%3D&md5=bfe1146a0e09b88903e416c0df49a94eCAS |

Müller R, Goodrich J (2011) Sweet memories: epigenetic control in flowering. F1000 Biology Reports 3, 13

Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L, Bernatavichute YV, Jacobsen SE, Fransz P, Dean C (2006) LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proceedings of the National Academy of Sciences of the United States of America 103, 5012–5017.
LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVGlsLk%3D&md5=01e93e46f704660e4ad605fb75d63b04CAS |

Noh Y, Amasino RM (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. The Plant Cell 15, 1671–1682.
PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslWkur4%3D&md5=e4ad32760e8d0c36929ae9407d63d9f0CAS |

Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuki Y, Matsumoto S, Hirai M (2007) Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theoretical and Applied Genetics 114, 595–608.
Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ygsrk%3D&md5=7710eaf1311d4a1a3d712a099f446a82CAS |

Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, Lydiate DJ, Trick M (1997) Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146, 1123–1129.

Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires CJ, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biology 15, R77
Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea.Crossref | GoogleScholarGoogle Scholar |

Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2016) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant, Cell & Environment 39, 1228–1239.
Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnslWhsbw%3D&md5=2cd9527de3c19f536e530e49b66f403aCAS |

Ridge S, Brown PH, Hecht V, Driessen RG, Weller JL (2015) The role of BoFLC2 in cauliflower (Brassica oleracea var. botrytis L.) reproductive development. Journal of Experimental Botany 66, 125–135.
The role of BoFLC2 in cauliflower (Brassica oleracea var. botrytis L.) reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXisFeju74%3D&md5=2fee2554e6e6bb6aa8a6433468327b59CAS |

Schiessl S, Iniguez-Luy F, Qian W, Snowdon RJ (2015) Diverse regulatory factors associate with flowering time and yield responses in winter-type Brassica napus. BMC Genomics 16, 737
Diverse regulatory factors associate with flowering time and yield responses in winter-type Brassica napus.Crossref | GoogleScholarGoogle Scholar |

Schmitz RJ, Amasino RM (2007) Vernalization: A model for investigating epigenetics and eukaryotic gene regulation in plants. Biochimica et Biophysica Acta 1769, 269–275.
Vernalization: A model for investigating epigenetics and eukaryotic gene regulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlSnsL0%3D&md5=c079796d4e69a248e70108820df8c7c6CAS |

Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162, 1457–1468.

Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. The Plant Cell 11, 445–458.
The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlehsL4%3D&md5=0e81a033a844d7c7e5345e220cb4eb88CAS |

Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. The Plant Cell 14, 2527–2537.
Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFelsLs%3D&md5=5fe2c59216dec863d87ed8641831f201CAS |

Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nature Reviews. Molecular Cell Biology 10, 697–708.

Song J, Angel A, Howard M, Dean C (2012) Vernalization—a cold-induced epigenetic switch. Journal of Cell Science 125, 3723–3731.
Vernalization—a cold-induced epigenetic switch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Onu7jK&md5=ccab53429e746eaac0d852c16df0c086CAS |

Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619–621.
R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslWksbo%3D&md5=1c66aab5d880cb24f8eb883e3a511777CAS |

Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164.
Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFOnsA%3D%3D&md5=419b1f29c5cbed69e756ca6d1ef910f3CAS |

Sung S, Amasino RM (2005) REMEMBERING WINTER: Toward a molecular understanding of vernalization. Annual Review of Plant Biology 56, 491–508.
REMEMBERING WINTER: Toward a molecular understanding of vernalization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaqsrg%3D&md5=c71fa525d5ad9bcaf4e62d0047ffe43aCAS |

Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799–802.
Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFersrvM&md5=6aaf311127a001ef48b232e4673cf825CAS |

Tadege M, Sheldon CC, Helliwell CA, Stoutjesdijk P, Dennis ES, Peacock WJ (2001) Control of flowering time by FLC orthologues in Brassica napus. The Plant Journal 28, 545–553.
Control of flowering time by FLC orthologues in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVCnsg%3D%3D&md5=b20b19bbbdae7e1fb4c3ed62f42046eaCAS |

Tamada Y, Yun JY, Woo SC, Amasino RM (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. The Plant Cell 21, 3257–3269.
ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOgsLjL&md5=ee4425681c7caeba462887bcad4e0163CAS |

Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689–693.
Long noncoding RNA as modular scaffold of histone modification complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps1ehtb0%3D&md5=1852aed68ccc05c62ffe83580e46860fCAS |

Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLOS Genetics 3, e86
Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27.Crossref | GoogleScholarGoogle Scholar |

U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese Journal of Botany 7, 389–452.

Wang J, Long Y, Wu B, Liu J, Jiang C, Shi L, Zhao J, King GJ, Meng J (2009a) The evolution of Brassica napus FLOWERING LOCUS T paralogues in the context of inverted chromosomal duplication blocks. BMC Evolutionary Biology 9, 271
The evolution of Brassica napus FLOWERING LOCUS T paralogues in the context of inverted chromosomal duplication blocks.Crossref | GoogleScholarGoogle Scholar |

Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009b) PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423–427.
PEP1 regulates perennial flowering in Arabis alpina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksFemu78%3D&md5=8a89d5d6bc95717568af1073203619a3CAS |

Wang N, Qian W, Suppanz I, Wei L, Mao B, Long Y, Meng J, Müller AE, Jung C (2011a) Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA.FRI.a. Journal of Experimental Botany 62, 5641–5658.
Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA.FRI.a.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCit7zP&md5=09964532a8cace7cba2b25c3542209a3CAS |

Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IAP, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011b) The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43, 1035–1039.
The genome of the mesopolyploid crop species Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gtrbL&md5=05695d7ea614b936d5dab41e8ae9d47eCAS |

Warwick SI, Francis A, Al-Shehbaz IA (2006) Brassicaceae: Species checklist and database on CD-Rom. Plant Systematics and Evolution 259, 249–258.
Brassicaceae: Species checklist and database on CD-Rom.Crossref | GoogleScholarGoogle Scholar |

Wu J, Wei K, Cheng F, Li S, Wang Q, Zhao J, Bonnema G, Wang X (2012) A naturally occurring InDel variation in BraA.FLC.b (BrFLC2) associated with flowering time variation in Brassica rapa. BMC Plant Biology 12, 151
A naturally occurring InDel variation in BraA.FLC.b (BrFLC2) associated with flowering time variation in Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslals7zN&md5=96ea7e4357da042c6da76045b9264a4eCAS |

Xiao D, Zhao JJ, Hou XL, Basnet RK, Carpio DP, Zhang NW, Bucher J, Lin K, Cheng F, Wang XW, Bonnema G (2013) The Brassica rapa FLC homologue FLC2 is a key regulator of flowering time, identified through transcriptional co-expression networks. Journal of Experimental Botany 64, 4503–4516.
The Brassica rapa FLC homologue FLC2 is a key regulator of flowering time, identified through transcriptional co-expression networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1ygs7fF&md5=c39ac9c4db422f431d8125cdd7656863CAS |

Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proceedings of the National Academy of Sciences of the United States of America 100, 6263–6268.
Positional cloning of the wheat vernalization gene VRN1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOksr4%3D&md5=b67434f254e724d5cbe6f689665de9f4CAS |

Yang H, Howard M, Dean C (2014) Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Current Biology 24, 1793–1797.
Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ags7nP&md5=710985139987c05b924693c5129771c1CAS |

Young MD, Willson TA, Wakefield MJ, Trounson E, Hilton DJ, Blewitt ME, Oshlack A, Majewski IJ (2011) ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Research 39, 7415–7427.
ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eitLbK&md5=041e343cf5d5e9ecc0b1de99eb1eae19CAS |

Yuan YX, Wu J, Sun RF, Zhang XW, Xu DH, Bonnema G, Wang XW (2009) A naturally occurring splicing site mutation in the Brassica rapa FLC1 gene is associated with variation in flowering time. Journal of Experimental Botany 60, 1299–1308.
A naturally occurring splicing site mutation in the Brassica rapa FLC1 gene is associated with variation in flowering time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShsbk%3D&md5=966a41353bd1ba599f2d9323b011c373CAS |

Zhao J, Kulkarni V, Liu N, Del Carpio DP, Bucher J, Bonnema G (2010) BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa. Journal of Experimental Botany 61, 1817–1825.
BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvVOgsL8%3D&md5=b7accde201aface57efc8dac0f45c7cfCAS |

Zou X, Suppanz I, Raman H, Hou J, Wang J, Long Y, Jung C, Meng J (2012) Comparative analysis of FLC homologues in Brassicaceae provides insight into their role in the evolution of oilseed rape. PLoS One 7, e45751
Comparative analysis of FLC homologues in Brassicaceae provides insight into their role in the evolution of oilseed rape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2jtbjJ&md5=d69bcdd4c1cd73cd8a3fcd26c63f06cbCAS |