Irwin, Judith A., Lister, Clare, Soumpourou, Eleni, Zhang, Yanwen, Howell, Elaine C., Teakle, Graham R. and Dean, Caroline. (2012) Functional alleles of the flowering time regulator FRIGIDA in the Brassica oleracea genome. BMC Plant Biology, Vol.12 (No.1). p. 21. ISSN 1471-2229

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Abstract

Background Plants adopt different reproductive strategies as an adaptation to growth in a range of climates. In Arabidopsis thaliana FRIGIDA (FRI) confers a vernalization requirement and thus winter annual habit by increasing the expression of the MADS box transcriptional repressor FLOWERING LOCUS C (FLC). Variation at FRI plays a major role in A. thaliana life history strategy, as independent loss-of-function alleles that result in a rapid-cycling habit in different accessions, appear to have evolved many times. The aim of this study was to identify and characterize orthologues of FRI in Brassica oleracea. Results We describe the characterization of FRI from Brassica oleracea and identify the two B. oleracea FRI orthologues (BolC.FRI.a and BolC.FRI.b). These show extensive amino acid conservation in the central and C-terminal regions to FRI from other Brassicaceae, including A. thaliana, but have a diverged N-terminus. The genes map to two of the three regions of B. oleracea chromosomes syntenic to part of A. thaliana chromosome 5 suggesting that one of the FRI copies has been lost since the ancient triplication event that formed the B. oleracea genome. This genomic position is not syntenic with FRI in A. thaliana and comparative analysis revealed a recombination event within the A. thaliana FRI promoter. This relocated A. thaliana FRI to chromosome 4, very close to the nucleolar organizer region, leaving a fragment of FRI in the syntenic location on A. thaliana chromosome 5. Our data show this rearrangement occurred after the divergence from A. lyrata. We explored the allelic variation at BolC.FRI.a within cultivated B. oleracea germplasm and identified two major alleles, which appear equally functional both to each other and A. thaliana FRI, when expressed as fusions in A. thaliana. Conclusions We identify the two Brassica oleracea FRI genes, one of which we show through A. thaliana complementation experiments is functional, and show their genomic location is not syntenic with A. thaliana FRI due to an ancient recombination event. This has complicated previous association analyses of FRI with variation in life history strategy in the Brassica genus.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany S Agriculture > SB Plant culture
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Arabidopsis thaliana -- Adaptation, Arabidopsis thaliana -- Genetics, Arabidopsis thaliana -- Flowering time, Cole crops -- Genetics
Journal or Publication Title:	BMC Plant Biology
Publisher:	BioMed Central Ltd.
ISSN:	1471-2229
Date:	2012
Volume:	Vol.12
Number:	No.1
Page Range:	p. 21
Identification Number:	10.1186/1471-2229-12-21
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	Great Britain. Dept. for Environment, Food & Rural Affairs (DEFRA), Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC)
Grant number:	HH3708SFV (DEFRA), HL0186 (DEFRA), IF0157 (DEFRA), HH3723XS (DEFRA)
References:	1. Simpson GG, Dean C: Flowering - Arabidopsis, the Rosetta stone of flowering time? Science 2002, 296:285-289. 2. Baurle I, Dean C: The timing of developmental transitions in plants. Cell 2006, 125:655-664. 3. Amasino R: Seasonal and developmental timing of flowering. Plant J 2010, 61:1001-1013. 4. Hayama R, Yokol S, Tamaki S, Yano M, Shimamoto K: Adaptation of photoperiodic control pathways produced short-day flowering in rice. Nature 2003, 422:719-722. 5. Franks SJ, Sim S, Weis AE: Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Natl Acad Sci (USA) 2007, 104:1278-1282. 6. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G, Welch SM, Schmitt J: Effects of Genetic Perturbation on Seasonal Life History Plasticity. Science 2009, 323:930-934. 7. Sandring S, Riihimaki MA, Savolainen O, Agren J: Selection on flowering time and floral display in an alpine and lowland population of Arabidopsis lyrata. J Evolution Biol 2007, 20:558-567. 8. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C: Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 2000, 290:344-347. 9. Gazzani S, Gendall AR, Lister C, Dean C: Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 2003, 132:1107-1114. 10. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D: Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genetics 2005, 1(1):e6. 11. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C: Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 2005, 138:1163-1173. 12. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES: The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci (USA) 2000, 97:3753-3758. 13. Michaels SD, Amasino RM: Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 2001, 13:935-941. 14. Le Corre V, Roux F, Reboud X: DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 2002, 19:1261-1271. 15. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M, Grimwood J, Schmutz J, Myres RM, Schluter D, Kingsley DM: Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 2005, 307:1928-1933. 16. Kuittinen H, Niittyvuopio A, Rinne P, Savolainen O: Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol Biol Evol 2008, 25:319-329. 17. Slotte T, Huang H, Lascoux M, Ceplitis A: Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 2008, 25:1472-1481. 18. Fang Q, Liu J, Xu Z, Song R: Cloning and characterization of a flowering time gene from Thellungiella halophila. Acta Bioch Bioph Sin 2008, 40:747-753. 19. Risk JM, Laurie RE, Macknight RC, Day CL: FRIGIDA and related proteins have a conserved central domain and family specific N- and C- terminal regions that are functionally important. Plant Mol Biol 2010, 73:493-505. 20. Keller SR, Levsen N, Ingvarsson PK, Olson MS, Tiffin P: Local selection across a latitudinal gradient shapes nucleotide diversity in Balsam Poplar, Populus balsamifera L. Genetics 2011, 188:941-952. 21. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, et al: A draft sequence of the rice genome (Oryza sativa L. ssp japonica). Science 2002, 296:92-100. 22. Wang N, Qian W, Suppanz I, Wei L, Mao B, Long Y, Meng J, Müller AE, Jung C: Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA.FRI.a. J Exp Bot 2011, 62:5641-5658. 23. Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ: Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 2005, 171:765-781. 24. Schranz ME, Lysak MA, Mitchell-Olds T: The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 2006, 11:535-542. 25. Trick M, Kwon SJ, Choi SR, Fraser F, Soumpourou E, Drou N, Wang Z, Lee SY, Yang TJ, Mun JH: Complexity of genome evolution by segmental rearrangement in Brassica rapa revealed by sequence-level analysis. BMC Genomics 2009, 10:539. 26. Mun JH, Kwon SJ, Kim JA, Jin M, Kim JS, Lim MH, Lee SI, Hong JK, Park TH, Lee SC, Kim BJ, Seo MS, Baek S, Lee MJ, Shin JY, Hahn JH, Hwang YJ, Lim KB, Park JY, Lee J, Yang TJ, Yu HJ, Choi IY, Choi BS, Choi SR, Ramchairy N, Lim YP, Fraser F, Drou N, Soumpourou E, et al: Sequence and structure of Brassica rapa chromosome A3. Genome Biol 2010, 11:R94. 27. Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Kondo M, Fujimura M, Nunome T, Fukuoka H, Hirai M, Matsumoto S: Simple sequence repeatbased comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 2006, 173:309-319. 28. Gao M, Li G, Yang B, Qiu D, Farnham M, Quiros C: High-density Brassica oleracea linkage map: identification of useful new linkages. Theor Appl Genet 2007, 115:277-287. 29. Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park BS: Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genome wide alignment with Arabidopsis. Genetics 2007, 177:2433. 30. Smooker AM, Wells R, Morgan C, Beaudoin F, Cho K, Fraser F, Bancroft I: The identification and mapping of candidate genes and QTL involved in the fatty acid desaturation pathway in Brassica napus. Theor App Genet 2011, 122:1075-1090. 31. Razi H, Howell EC, Newbury HJ, Kearsey MJ: Does sequence polymorphism of FLC paralogues underlie flowering time QTL in Brassica oleracea? Theor App Genet 2008, 116:179-192. 32. O’Neill CM, Bancroft I: Comparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homoeologous to sequenced regions of chromosomes 4 and 5 of Arabidopsis thaliana. Plant J 2000, 23:233-243. 33. Østergaard L, King GK: Standardized gene nomenclature for the Brassica genus. Plant Methods 2008, 4:10-13. 34. Lupas A, Van Dyke M, Stock J: Predicting Coiled Coils from Protein Sequences. Science 1991, 252:1162-1164. 35. Michaels SD, Bezerra IC, Amasino RM: FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA 2004, 101:3281-3285. 36. Bohuon EJR, Keith DJ, Parkin IAP, Sharpe AG, Lydiate DJ: Alignment of the conserved C genomes of Brassica oleracea and Brassica napus. Theor Appl Genet 1996, 93:833-839. 37. Sebastian RL, Kearsey MJ, King GJ: Identification of quantitative trait loci controlling developmental characteristics of Brassica oleracea L. Theor Appl Genet 2002, 104:601-609. 38. Bohuon EJR, Ramsay LD, Craft JA, Arthur AE, Marshall DF, Lydiate DJ, Kearsey MJ: The association of flowering time quantitative trait loci with duplicated regions and candidate loci in Brassica oleracea. Genetics 1998, 150:393-401. 39. Rae AM, Howell EC, Kearsey MJ: More QTL for flowering time revealed by substitution lines in Brassica oleracea. Heredity 1999, 83:586-596. 40. Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuki Y, Matsumoto S, Hirai M: Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theor Appl Genet 2007, 114:595-608. 41. Uptmoor R, Schrag T, Stützel H, Esch E: Crop model based QTL analysis across environments and QTL based estimation of time to floral induction and flowering in Brassica oleracea. Mol Breeding 2008, 21:205-216. 42. Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC: Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 2002, 162:1457-1468. 43. Nishioka M, Tamura K, Hayashi M, Fujimori Y, Ohkawa Y, Kuginuki Y, Harada K: Mapping of QTLs for bolting time in Brassica rapa (syn. campestris) under different environmental conditions. Breeding Sci 2005, 55:127-133. 44. Lou P, Zhao JJ, Kim JS, Shen SX, Del Carpio DP, Song XF, Jin MN, Vreugdenhil D, Wang XW, Koornneef M, Bonnema G: Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 2007, 58:4005-4016. 45. Yang X, Yu YJ, Zhang FL, Zou ZR, Zhao XY, Zhang DS, Xu JB: Linkage Map Construction and Quantitative Trait Loci Analysis for Bolting Based on a Double Haploid Population of Brassica rapa. J Integrative Plant Biol 2007, 49:664-671. 46. Zhao J, Kulkarni V, Liu N, Del Carpio DP, Bucher J, Bonnema G: BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa. J Exp Bot 2010, 61:1817-1825. 47. Axelsson T, Shavorskaya O, Lagercrantz U: Multiple flowering time QTLs within several Brassica species could be the result of duplicated copies of one ancestral gene. Genome 2001, 44:856-864. 48. Osterberg MK, Shavorskaya O, Lascoux M, Lagercrantz U: Naturally occurring indel variation in the Brassica nigra COL1 gene is associated with variation in flowering time. Genetics 2002, 161:299-306. 49. Pires JC, Zhao JW, Schranz ME, Leon EJ, Quijada PA, Lukens LN, Osborn TC: Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc 2004, 82:675-688. 50. Kuittinen H, de Haan AA, Vogl C, Oikarinen S, Leppala J, Koch M, Mitchell- Olds T, Langley CH, Savolainen O: Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana. Genetics 2004, 168:1575-1584. 51. Beaulieu J, Belzile F, Jean M: Linkage maps for Arabidopsis lyrata subsp. lyrata and Arabidopsis lyrata subsp. petraea combining anonymous and Arabidopsis thaliana-derived markers. Genome 2007, 50:142-150. 52. Yogeeswaran K, Frary A, York TL, Amenta A, Lesser AH, Nasrallah JB, Tanksley SD, Nasrallah ME: Comparative genome analyses of Arabidopsis spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Res 2005, 15:505-515. 53. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Yang L, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KFX, Van De Peer Y, Grigoriev IV, Nordborg M, Weigel D, Guo YL: The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 2011, 43:476-481. 54. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Wdimayer P, Gruissem W, Zimmermann P: Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Advances in Bioinformatics 2008, 420747.q. 55. Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S: Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci (USA) 2010, 107:18724-18728. 56. Koch MA, Matschinger M: Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci (USA) 2007, 104:6272-6277. 57. Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I: Mechanisms of chromsome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci (USA) 2006, 103:5224-5229. 58. Sung SB, Amasino RM: Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 2004, 427:159-164. 59. Town CD, Cheung F, Maiti R, Crabtree J, Haas BJ, Wortman JR, Hine EE, Althoff R, Arbogast TS, Tallon LJ, Vigouroux M, Trick M, Bancroft I: Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 2006, 18:1348-1359. 60. Allender CJ, Allainguillaume J, Lynn J, King GJ: Simple sequence repeats reveal uneven distribution of genetic diversity in chloroplast genomes of Brassica oleracea L. and (n = 9) wild relatives. Theor Appl Genet 2007, 114:609-618. 61. Schmidt R, West J, Cnops G, Love K, Balestrazzi A, Dean C: Detailed description of four YAC contigs representing 17 Mb of chromosome 4 of Arabidopsis thaliana ecotype Columbia. Plant J 1996, 9:755-765. 62. Raybould AF, Mogg RJ, Clarke RT, Gliddon CJ, Gray AJ: Variation and population structure at microsatellite and isozyme loci in wild cabbage (Brassica oleracea L.) in Dorset (UK). Genet Resour Crop Ev 1999, 46:351-360. 63. Sharpe AG, Parkin IAP, Keith DJ, Lydiate DJ: Frequent non-reciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 1995, 38:1112-1121. 64. van Ooijen JW, Voorrips RE: JoinMap version 3.0: Software for the calculation of genetic linkage map. Wageningen: Plant Research International; 2001. 65. Howell EC, Barker GC, Jones GH, Kearsey MJ, King GJ, Kop EP, Ryder CD, Teakle GR, Vicente JG, Armstrong SA: Integration of the cytogenetic and genetic linkage maps of Brassica oleracea. Genetics 2002, 161:1225-1234. 66. Gerlach WL, Bedbrook JR: Cloning and characterisation of ribosomal genes from wheat and barley. Nucleic Acids Res 1979, 7:1869-1885. 67. Salathia NS: Regulation of Biological clocks i Brassica olerace and Arabidopsis thalian. University of Warwick: PhD Dissertation; 2003. 68. Figurski DH, Helinski DR: Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci (USA) 1979, 76:1648-1652. 69. Bechtold N, Ellis J, Pelleteir G: In planta Agrobacterium mediated gene transfer by infltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris Life Sci 1993, 316:1194-1199.
URI:	http://wrap.warwick.ac.uk/id/eprint/49406

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