Skip to main content
Log in

Genetic architecture of the circadian clock and flowering time in Brassica rapa

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The circadian clock serves to coordinate physiology and behavior with the diurnal cycles derived from the daily rotation of the earth. In plants, circadian rhythms contribute to growth and yield and, hence, to both agricultural productivity and evolutionary fitness. Arabidopsis thaliana has served as a tractable model species in which to dissect clock mechanism and function, but it now becomes important to define the extent to which the Arabidopsis model can be extrapolated to other species, including crops. Accordingly, we have extended our studies to the close Arabidopsis relative and crop species, Brassica rapa. We have investigated natural variation in circadian function and flowering time among multiple B. rapa collections. There is wide variation in clock function, based on a robust rhythm in cotyledon movement, within a collection of B. rapa accessions, wild populations and recombinant inbred lines (RILs) derived from a cross between parents from two distinct subspecies, a rapid cycling Chinese cabbage (ssp. pekinensis) and a Yellow Sarson oilseed (ssp. trilocularis). We further analyzed the RILs to identify the quantitative trait loci (QTL) responsible for this natural variation in clock period and temperature compensation, as well as for flowering time under different temperature and day length settings. Most clock and flowering-time QTL mapped to overlapping chromosomal loci. We have exploited micro-synteny between the Arabidopsis and B. rapa genomes to identify candidate genes for these QTL.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733

    Article  PubMed  CAS  Google Scholar 

  • Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci USA 107:18724–18728

    Article  PubMed  CAS  Google Scholar 

  • Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH (2010) The role of recently derived FT paralogs in sunflower domestication. Curr Biol 20:629–635

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Holland JB, Bradbury P, Acharya C, Brown P, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz J, Goodman M, Harjes C, Guill K, Kroon D, Larsson S, Lepak N, Li H, Mitchell S, Pressoir G, Peiffer J, Rosas M, Rocheford T, Romay M, Romero S, Salvo S, Villeda H, da Silva H, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen M (2009) The genetic architecture of maize flowering time. Science 325:714–718

    Article  PubMed  CAS  Google Scholar 

  • Cheung F, Trick M, Drou N, Lim YP, Park JY, Kwon SJ, Kim JA, Scott R, Pires JC, Paterson AH, Town C, Bancroft I (2009) Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21:1912–1928

    Article  PubMed  CAS  Google Scholar 

  • Darrah C, Taylor BL, Edwards KD, Brown PE, Hall A, McWatters HG (2006) Analysis of phase of LUCIFERASE expression reveals novel circadian quantitative trait loci in Arabidopsis. Plant Physiol 140:1464–1474

    Article  PubMed  CAS  Google Scholar 

  • DeCoursey PJ, Walker JK, Smith SA (2000) A circadian pacemaker in free-living chipmunks: essential for survival? J Comp Physiol A 186:169–180

    Article  PubMed  CAS  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    Article  PubMed  CAS  Google Scholar 

  • Donovan LA, Ehleringer JR (1994) Carbon-isotope discrimination, water-use efficiency, growth, and mortality in a natural shrub population. Oecologia 100:347–354

    Article  Google Scholar 

  • Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ (2005) Natural allelic variation in the temperature compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170:387–400

    Article  PubMed  CAS  Google Scholar 

  • Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JCW, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–650

    Article  PubMed  CAS  Google Scholar 

  • Gardner GF, Feldman JF (1981) Temperature compensation of circadian period length in clock mutants of Neurospora crassa. Plant Physiol 68:1244–1248

    Article  PubMed  CAS  Google Scholar 

  • Gould PD, Locke JCW, Larue C, Southern MM, Davis SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar AJ, Hall A (2006) The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18:1177–1187

    Article  PubMed  CAS  Google Scholar 

  • Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci USA 107:9458–9463

    Article  PubMed  CAS  Google Scholar 

  • Green RM, Tingay S, Wang Z-Y, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584

    Article  PubMed  CAS  Google Scholar 

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377

    Article  PubMed  CAS  Google Scholar 

  • Huang ZJ, Curtin KD, Rosbash M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267:1169–1172

    Article  PubMed  CAS  Google Scholar 

  • Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89

    Article  PubMed  CAS  Google Scholar 

  • Iniguez-Luy FL, Lukens L, Farnham MW, Amasino RM, Osborn TC (2009) Development of public immortal mapping populations, molecular markers and linkage maps for rapid cycling Brassica rapa and B. oleracea. Theor Appl Genet 119:31–43

    Article  Google Scholar 

  • Johnson CH, Elliott J, Foster R, Honma K-I, Kronauer R (2004) Fundamental properties of circadian rhythms. In: Dunlap JC, Loros JJ, DeCoursey P (eds) Chronobiology: biological timekeeping. Sinauer, Sunderland, pp 67–105

    Google Scholar 

  • Kim JA, Yang T-J, Kim JS, Park JY, Kwon S-J, Lim M-H, Jin M, Lee SC, Lee SI, Choi B-S, Um S-H, Kim H-I, Chun C, Park B-S (2007) Isolation of circadian-associated genes in Brassica rapa by comparative genomics with Arabidopsis thaliana. Mol Cells 23:145–153

    PubMed  CAS  Google Scholar 

  • Kim H, Choi SR, Bae J, Hong CP, Lee SY, Hossain MJ, Van Nguyen D, Jin M, Park BS, Bang JW, Bancroft I, Lim YP (2009) Sequenced BAC anchored reference genetic map that reconciles the ten individual chromosomes of Brassica rapa. BMC Genomics 10:432

    Article  PubMed  Google Scholar 

  • 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 Res 16:311–323

    Article  PubMed  CAS  Google Scholar 

  • 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. J Exp Bot 58:4005–4016

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto A, Tomioka K, Chiba Y, Tanimura T (1999) tim rit lengthens circadian period in a temperature-dependent manner through suppression of PERIOD protein cycling and nuclear localization. Mol Cell Biol 19:4343–4354

    PubMed  CAS  Google Scholar 

  • McClung CR (2010) A modern circadian clock in the common angiosperm ancestor of monocots and eudicots. BMC Biol 8:55

    Article  PubMed  Google Scholar 

  • McClung CR, Gutiérrez RA (2010) Network news: prime time for systems biology of the plant circadian clock. Curr Opin Genet Dev 20:588–598

    Article  PubMed  CAS  Google Scholar 

  • McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151

    Article  PubMed  CAS  Google Scholar 

  • Mehra A, Shi M, Baker CL, Colot HV, Loros JJ, Dunlap JC (2009) A role for casein kinase 2 in the mechanism underlying circadian temperature compensation. Cell 137:749–760

    Article  PubMed  CAS  Google Scholar 

  • Michael TP, Salomé PA, Yu HJ, Spencer TR, Sharp EL, Alonso JM, Ecker JR, McClung CR (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053

    Article  PubMed  CAS  Google Scholar 

  • Mun J-H, Kwon S-J, Yang T-J, Seol Y-J, Jin M, Kim J-A, Lim M-H, Kim JS, Baek S, Choi B-S, Yu H-J, Kim D-S, Kim N, Lim K-B, Lee S-I, Hahn J-H, Lim YP, Bancroft I, Park B-S (2009) Genome-wide comparative analysis of the Brassica rapa gene space reveals genome shrinkage and differential loss of duplicated genes after whole genome triplication. Genome Biol 10:R111

    Article  PubMed  Google Scholar 

  • Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated Pseudo-Response Regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48:822–832

    Article  PubMed  CAS  Google Scholar 

  • Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N-H, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7 and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605

    Article  PubMed  CAS  Google Scholar 

  • Ni Z, Kim E-D, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  PubMed  CAS  Google Scholar 

  • Onai K, Okamoto K, Nishimoto H, Morioka C, Hirano M, Kami-ike N, Ishiura M (2004) Large-scale screening of Arabidopsis circadian clock mutants by a high-throughput real-time bioluminescence monitoring system. Plant J 40:1–11

    Article  PubMed  CAS  Google Scholar 

  • Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664

    Article  PubMed  CAS  Google Scholar 

  • Park JY, Koo DH, Hong CP, Lee SJ, Jeon JW, Lee SH, Yun PY, Park BS, Kim HR, Bang JW (2005) Physical mapping and microsynteny of Brassica rapa ssp. pekinensis genome corresponding to a 222 kbp gene-rich region of Arabidopsis chromosome 4 and partially duplicated on chromosome 5. Mol Gen Genomics 274:579–588

    Article  CAS  Google Scholar 

  • Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781

    Article  PubMed  CAS  Google Scholar 

  • Parzen E (1962) On estimation of a probability density function and mode. Ann Math Stat 33:1065–1076

    Article  Google Scholar 

  • Plautz JD, Straume M, Stanewsky R, Jamison CF, Brandes C, Dowse HB, Hall JC, Kay SA (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythms 12:204–217

    Article  PubMed  CAS  Google Scholar 

  • Pruneda-Paz JL, Kay SA (2010) An expanding universe of circadian networks in higher plants. Trends Plant Sci 15:259–265

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. Vienna, Austria

  • Rebetzke GJ, Condon AG, Farquhar GD, Appels R, Richards R (2008) Quantitative trait loci for carbon isotope discrimination are repeatable across environments and wheat mapping populations. Theor Appl Genet 118:123–137

    Article  PubMed  CAS  Google Scholar 

  • Rosenblatt M (1956) Remarks on some nonparametric estimates of a density function. Ann Math Stat 27:832–837

    Article  Google Scholar 

  • Salathia N, Davis SJ, Lynn JR, Michaels SD, Amasino RM, Millar AJ (2006) FLOWERING LOCUS C-dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways. BMC Plant Biol 6:10

    Article  PubMed  Google Scholar 

  • Salathia N, Lynn JR, Millar AJ, King GJ (2007) Detection and resolution of genetic loci affecting circadian period in Brassica oleracea. Theor Appl Genet 114:683–692

    Article  PubMed  Google Scholar 

  • Salomé PA, Weigel D, McClung CR (2010) The role of the Arabidopsis morning loop components CCA1, LHY, PRR7 and PRR9 in temperature compensation. Plant Cell 22:3650–3661

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Schranz M, Lysak M, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542

    Article  PubMed  CAS  Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    Article  PubMed  Google Scholar 

  • Stephenson P, Baker D, Girin T, Perez A, Amoah S, King GJ, Østergaard L (2010) A rich TILLING resource for studying gene function in Brassica rapa. BMC Plant Biol 10:62

    Article  PubMed  Google Scholar 

  • Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101:4712–4717

    Article  PubMed  CAS  Google Scholar 

  • Swarup K, Alonso-Blanco C, Lynn JR, Michaels SD, Amasino RM, Koornneef M, Millar AJ (1999) Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant J 20:67–77

    Article  PubMed  CAS  Google Scholar 

  • Takata N, Saito S, Saito CT, Uemura M (2010) Phylogenetic footprint of the plant clock system in angiosperms: evolutionary processes of Pseudo-Response Regulators. BMC Evol Biol 10:126

    Article  PubMed  Google Scholar 

  • Trick M, Kwon SJ, Choi SR, Fraser F, Soumpourou E, Drou N, Wang Z, Lee SY, Yang TJ, Mun JH, Paterson AH, Town CD, Pires JC, Lim YP, Park BS, Bancroft I (2009) Complexity of genome evolution by segmental rearrangement in Brassica rapa revealed by sequence-level analysis. BMC Genomics 10:539

    Article  PubMed  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of Florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  PubMed  CAS  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The Pseudo-Response Regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  PubMed  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng Z (2007) Windows Qtl Cartographer 2.5. N.C. State University, Bioinformatics Research Center, USA

    Google Scholar 

  • 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 (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323:930–934

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Xie Q, McClung CR (2010) Robust circadian rhythms of gene expression in Brassica rapa tissue culture. Plant Physiol 153:841–850

    Article  PubMed  CAS  Google Scholar 

  • Yerushalmi S, Yakir E, Green RM (2011) Circadian clocks and adaptation in Arabidopsis. Mol Ecol 20:1155–1165

    Article  PubMed  Google Scholar 

  • Zhang EE, Kay SA (2010) Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 11:764–776

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Paulo M-J, Jamar D, Lou P, Van Eeuwijk F, Bonnema G, Vreugdenhil D, Koornneef M (2007) Association mapping of leaf traits, flowering time, and phytate content in Brassica rapa. Genome 50:963–973

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a National Science Foundation grant (IOS 0605736) to C.R.M., C.W. and R.M. Amasino. We thank Fede Iñiguez-Luy (Temuco, Chile) for Brassica rapa IRRI RILs and linkage maps and the Centre for Genetic Resources, the Netherlands (CGN), for Brassica rapa accessions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. R. McClung.

Additional information

Communicated by C. Quiros.

P. Lou, Q. Xie and X. Xu contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 3890 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lou, P., Xie, Q., Xu, X. et al. Genetic architecture of the circadian clock and flowering time in Brassica rapa . Theor Appl Genet 123, 397–409 (2011). https://doi.org/10.1007/s00122-011-1592-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1592-x

Keywords

Navigation