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Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea

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Abstract

The FLC gene product is an inhibitor of flowering in Arabidopsis. FLC homologs in Brassica species are thought to control vernalization. We cloned four FLC homologs (BoFLCs) from Brassica oleracea. Three of these, BoFLC1, BoFLC3 and BoFLC5, have been previously characterized. The fourth novel sequence displayed 98% sequence homology to the previously identified gene BoFLC4, but also showed 91% homology to BrFLC2 from Brassica rapa. Phylogenetic analysis showed that this clone belongs to the FLC2 clade. Therefore, we designated this gene BoFLC2. Based on the segregation of RFLP, SRAP, CAPS, SSR and AFLP loci, a detailed linkage map of B. oleracea was constructed in the F2 progeny obtained from a cross of B. oleracea cv. Green Comet (broccoli; non-vernalization type) and B. oleracea cv. Reiho (cabbage; vernalization type), which covered 540 cM, 9 major linkage groups. Six quantitative trait loci (QTL) controlling flowering time were detected. BoFLC1, BoFLC3 and BoFLC5 were not linked to the QTLs controlling flowering time. However, the largest QTL effect was located in the region where BoFLC2 was mapped. Genotyping of F2 plants at the BoFLC2 locus showed that most of the early flowering plants were homozygotes of BoFLC-GC, whereas most of the late- and non-flowering plants were homozygotes of BoFLC-Rei. The BoFLC2 homologs present in plants of the non-vernalization type were non-functional, due to a frameshift in exon 4. Moreover, duplications and deletions of BoFLC2 were detected in broccoli and a rapid cycling line, respectively. These results suggest that BoFLC2 contributes to the control of flowering time in B. oleracea.

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References

  • Amasino R (2004) Vernalization, competence, and the epigenetic memory of Winter. Plant Cell 16:2553–2559

    Article  PubMed  CAS  Google Scholar 

  • Axelsson T, Shavorskaya O, Lagercranyz U (2001) Multiple flowering time QTLs within of duplicated copies of one ancestral gene. Genome 44:856–864

    Article  CAS  Google Scholar 

  • Baggett JR, Kean D (1989) Inheritance of annual flowering in Brassica oleracea. HortScience 24:662–664

    Google Scholar 

  • Baggett JR, Wahlert WK (1975) Annual flowering and growth habit in cabbage–Broccoli crosses. HortScience 10:170–172

    Google Scholar 

  • Basten CJ, Weir BS, Zeng ZB (2002) QTL cartographer: a reference manual and tutorial for QTL mapping. North Caroline State University, Department of Statistics, Raleigh

    Google Scholar 

  • Bohuon EJR, Ramsay LD, Craft JA, Arthur AE, Mashall DF, Lydiate DJ, Kearsey MJ (1998) The association of flowering time quantitative trait loci with duplicated regions and candidate loci in Brassica oleracea. Genetics 150:393–401

    PubMed  CAS  Google Scholar 

  • Camargo LEA, Osborn TC (1996) Mapping loci controlling flowering time in Brassica oleracea. Theor Appl Genet 92:610–616

    Article  CAS  Google Scholar 

  • Devlin PF, Kay SA (2000) Flower arranging in Arabidopsis. Science 288:1600–1602

    Article  PubMed  CAS  Google Scholar 

  • Ferreira ME, Williams PH, Osborn TC (1994) RFLP mapping of Brassica napus using double haploid lines. Theor Appl Genet 89:615–621

    Article  CAS  Google Scholar 

  • Fujime Y (1988) A difference of response to low temperature between cauliflower and broccoli. Acta Hort 218:141–151

    Google Scholar 

  • Friend DJC (1985) Brassica. In: Halevy AH (ed) Handbook of flowering, vol 2. CRC Press, Boca Raton, pp 48–77

  • Inoue H, Nishio T (2004) Efficiency of PCR-RF-SSCP marker production in Brassica oleracea using Brassica EST sequences. Euphytica 137:233–242

    Article  CAS  Google Scholar 

  • Ito H, Saito T, Hatakeyama T (1966) Time and temperature factors for the flower formation in cabbage. II The site of vernalization and the nature of vernalization sensitivity. Tohoku J Agric Res 17:1–15

    Google Scholar 

  • Kim JS, Chung TY, King GJ, Jin M, Yang TJ, Jin YM, Kim HI, Park BS (2006) A sequence-tagged limkage map of Brassica rapa. Genetics 174:29–39

    Article  PubMed  CAS  Google Scholar 

  • 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. Theor Appl Genet 102:425–430

    Article  CAS  Google Scholar 

  • Kuittinen H, Aguade M, Charlesworth D, Haan ADE, Lauga B, Mitchell-Olds T, Oikarinen S, Ramos-Onsins S, Stranger B, Van Tienderen P, Savolainen O (2002) Primers for 22 candidate genes for ecological adaptations in Brassicaceae. Mol Ecol Notes 2:258–262

    Article  CAS  Google Scholar 

  • Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–1228

    PubMed  CAS  Google Scholar 

  • Lagercrantz U, Lydiate D (1996) Comparative genome mapping in Brassica. Genetics 144:1903–1910

    PubMed  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine scale collinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    Article  PubMed  CAS  Google Scholar 

  • Li G, Quiros CF (2001) Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor Appl Genet 103:455–461

    Article  CAS  Google Scholar 

  • Li G, Gao M, Yang B, Quiros CF (2003) Gene for gene alignment between the Brassica and Arabidopsis genomes by direct transcriptome mapping. Theor Appl Genet 107:168–180

    Article  PubMed  CAS  Google Scholar 

  • Lin SI, Wang JG, Poon SY, Su CL, Wang SS, Chiou TJ (2005) Differential regulation of Flowering Locus C expressed by vernalization in Cabbage and Arabidopsis. Plant Physiol 137:1037–1048

    Article  PubMed  CAS  Google Scholar 

  • Lukens L, Zou F, Lydiate D, Parkin I, Osborn T (2003) Comparison of a Brassica oleracea Genetic map with the genome of Arabidopsis thaliana. Genetics 164:359–372

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high-molecular-weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell:S111-S130

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Parkin IAP, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38:1122–1131

    CAS  PubMed  Google Scholar 

  • Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2006) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sebastian RL, Howell EC, King GJ, Marshall DF, Kearsey MJ, (2000) An integrated AFLP and RFLP Brassica oleracea linkage map from two morphologically distinct double-haploid mapping populations. Theor Appl Genet 100:75–81

    Article  CAS  Google Scholar 

  • Sebastian RL, Kearsey MJ, King GJ (2002) Identification of quantitative trait loci controlling developmetal characteristics of Brassica oleracea L. Theor Appl Genet 104:601–609

    Article  PubMed  CAS  Google Scholar 

  • Sharp AG, Parkin AP, Keith DJ, Lydiate DJ (1995) Frequent non reciprocal translocations in the amphidiploid Brassica napus (oil-seed rape). Genome 38:1122–1131

    Google Scholar 

  • 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. Plant Cell 11:445–458

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of Flowering Locus C (FLC). Proc Natl Acad Sci USA 97:3753–3758

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Finnegan EJ, Dennis ES, Peacock WJ (2006) Quantitative effects of vernalization on FLC and SOC1 expression. Plant J 45:871–883

    Article  PubMed  CAS  Google Scholar 

  • Suwabe K, Iketani H, Nunome T, Kage T, Hirai M (2002) Isolation and characterization of microsatellites in Brassica rapa L. Theor Appl Genet 104:1092–1098

    Article  PubMed  CAS  Google Scholar 

  • Suwabe K, Iketani H, Nunome T, Ohyama A, Hirai M, Fukuoka H (2004) Characteristics of microsatellites in Brassica rapa genome and their potential utilization for comparative genomics in Cruciferae. Breed Sci 54:85–90

    Article  CAS  Google Scholar 

  • Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Kondo M, Fujimura M, Nunome T, Fukuoka H, Hirai M, Matsumoto S (2006) SSR-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173:309–319

    Article  PubMed  CAS  Google Scholar 

  • Tadege M, Sheldon CC, Helliwell CA, Stoutjesdijk P, Dennis ES, Peacock WJ (2001) Control of flowering time by FLC orthologues in Brassica napus. Plant J 28:545–553

    Article  PubMed  CAS  Google Scholar 

  • Teutonico RA, Osborn TC (1995) Mapping loci controlling vernalization requirement in Brassica rapa. Theor Appl Genet 91:1279–1283

    Article  CAS  Google Scholar 

  • Udall JA, Quijada P, Osborn TC (2005) Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L. Genetics 169:967–979

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps (user manual). University of Wageningen, The Netherlands

    Google Scholar 

  • Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2000). MapQTL 4.0: software for the calculation of QTL positions on genetic maps (user manual). University of Wageningen, The Netherlands

    Google Scholar 

  • Walkof C (1963) A mutant annual cabbage. Euphytica 12:77–80

    Google Scholar 

  • Wurr DCE, Fellows JR (2000) Temperature influences on the plant development of different maturity types of cauliflower. Acta Hort 539:69–74

    Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors sincerely thank Prof. T. C. Osborn from the University of Wisconsin, USA and the National Institute of Vegetable and Tea Science, Japan, for kindly providing Brassica clones and DH lines, respectively. This work was supported in part by a Grant-in-Aid for Scientific Research (No. 13660005) from the Ministry of Education, Culture, Sports, Science and Technology, Japan and in part by a grant for the Promotion of Niigata University Research Projects.

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Authors and Affiliations

  1. Faculty of Agriculture, Niigata University, Niigata, 950-2181, Japan

    K. Okazaki, R. Kikuchi & E. Togashi

  2. Takii Plant Breeding Experiment Station, Shiga, 520-3231, Japan

    K. Sakamoto & A. Saito

  3. Asahi Noen Seed Co., Ltd., Aichi, 495-0001, Japan

    Y. Kuginuki

  4. National Institute of Vegetable and Tea Science, 360 Kusawa, Ano, Mie, 514-2392, Japan

    S. Matsumoto

  5. Faculty of Agriculture, Kyoto Prefectural University, Kyoto, 606-8522, Japan

    M. Hirai

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  1. K. Okazaki
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  2. K. Sakamoto
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  3. R. Kikuchi
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  4. A. Saito
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  8. M. Hirai
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Correspondence to K. Okazaki.

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Communicated by H. C. Becker.

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Okazaki, K., Sakamoto, K., Kikuchi, R. et al. Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea . Theor Appl Genet 114, 595–608 (2007). https://doi.org/10.1007/s00122-006-0460-6

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