Theoretical and Applied Genetics

, Volume 123, Issue 3, pp 397–409 | Cite as

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

  • P. Lou
  • Q. Xie
  • X. Xu
  • C. E. Edwards
  • M. T. Brock
  • C. Weinig
  • C. R. McClung
Original Paper

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.

Supplementary material

122_2011_1592_MOESM1_ESM.pdf (3.8 mb)
Supplementary material 1 (PDF 3890 kb)

References

  1. 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 115:721–733PubMedCrossRefGoogle Scholar
  2. 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 107:18724–18728PubMedCrossRefGoogle Scholar
  3. Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH (2010) The role of recently derived FT paralogs in sunflower domestication. Curr Biol 20:629–635PubMedCrossRefGoogle Scholar
  4. 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 325:714–718PubMedCrossRefGoogle Scholar
  5. 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 21:1912–1928PubMedCrossRefGoogle Scholar
  6. 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 140:1464–1474PubMedCrossRefGoogle Scholar
  7. DeCoursey PJ, Walker JK, Smith SA (2000) A circadian pacemaker in free-living chipmunks: essential for survival? J Comp Physiol A 186:169–180PubMedCrossRefGoogle Scholar
  8. 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 309:630–633PubMedCrossRefGoogle Scholar
  9. Donovan LA, Ehleringer JR (1994) Carbon-isotope discrimination, water-use efficiency, growth, and mortality in a natural shrub population. Oecologia 100:347–354CrossRefGoogle Scholar
  10. 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 170:387–400PubMedCrossRefGoogle Scholar
  11. 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 18:639–650PubMedCrossRefGoogle Scholar
  12. Gardner GF, Feldman JF (1981) Temperature compensation of circadian period length in clock mutants of Neurospora crassa. Plant Physiol 68:1244–1248PubMedCrossRefGoogle Scholar
  13. 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 18:1177–1187PubMedCrossRefGoogle Scholar
  14. 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 107:9458–9463PubMedCrossRefGoogle Scholar
  15. Green RM, Tingay S, Wang Z-Y, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584PubMedCrossRefGoogle Scholar
  16. Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377PubMedCrossRefGoogle Scholar
  17. Huang ZJ, Curtin KD, Rosbash M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267:1169–1172PubMedCrossRefGoogle Scholar
  18. Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89PubMedCrossRefGoogle Scholar
  19. 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 119:31–43CrossRefGoogle Scholar
  20. 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 67–105Google Scholar
  21. 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 23:145–153PubMedGoogle Scholar
  22. 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 10:432PubMedCrossRefGoogle Scholar
  23. 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 16:311–323PubMedCrossRefGoogle Scholar
  24. 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 58:4005–4016PubMedCrossRefGoogle Scholar
  25. 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 19:4343–4354PubMedGoogle Scholar
  26. McClung CR (2010) A modern circadian clock in the common angiosperm ancestor of monocots and eudicots. BMC Biol 8:55PubMedCrossRefGoogle Scholar
  27. McClung CR, Gutiérrez RA (2010) Network news: prime time for systems biology of the plant circadian clock. Curr Opin Genet Dev 20:588–598PubMedCrossRefGoogle Scholar
  28. 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 12:1137–1151PubMedCrossRefGoogle Scholar
  29. 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 137:749–760PubMedCrossRefGoogle Scholar
  30. 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 302:1049–1053PubMedCrossRefGoogle Scholar
  31. 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:R111PubMedCrossRefGoogle Scholar
  32. 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 48:822–832PubMedCrossRefGoogle Scholar
  33. 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 22:594–605PubMedCrossRefGoogle Scholar
  34. 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 457:327–331PubMedCrossRefGoogle Scholar
  35. 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 40:1–11PubMedCrossRefGoogle Scholar
  36. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664PubMedCrossRefGoogle Scholar
  37. 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 274:579–588CrossRefGoogle Scholar
  38. 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 171:765–781PubMedCrossRefGoogle Scholar
  39. Parzen E (1962) On estimation of a probability density function and mode. Ann Math Stat 33:1065–1076CrossRefGoogle Scholar
  40. 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 12:204–217PubMedCrossRefGoogle Scholar
  41. Pruneda-Paz JL, Kay SA (2010) An expanding universe of circadian networks in higher plants. Trends Plant Sci 15:259–265PubMedCrossRefGoogle Scholar
  42. R Development Core Team (2009) R: A language and environment for statistical computing. Vienna, AustriaGoogle Scholar
  43. 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 118:123–137PubMedCrossRefGoogle Scholar
  44. Rosenblatt M (1956) Remarks on some nonparametric estimates of a density function. Ann Math Stat 27:832–837CrossRefGoogle Scholar
  45. 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 6:10PubMedCrossRefGoogle Scholar
  46. Salathia N, Lynn JR, Millar AJ, King GJ (2007) Detection and resolution of genetic loci affecting circadian period in Brassica oleracea. Theor Appl Genet 114:683–692PubMedCrossRefGoogle Scholar
  47. 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 22:3650–3661PubMedCrossRefGoogle Scholar
  48. 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 162:1457–1468PubMedGoogle Scholar
  49. 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 11:535–542PubMedCrossRefGoogle Scholar
  50. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454PubMedCrossRefGoogle Scholar
  51. 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 10:62PubMedCrossRefGoogle Scholar
  52. 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 101:4712–4717PubMedCrossRefGoogle Scholar
  53. 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 20:67–77PubMedCrossRefGoogle Scholar
  54. 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 10:126PubMedCrossRefGoogle Scholar
  55. 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 10:539PubMedCrossRefGoogle Scholar
  56. Turck F, Fornara F, Coupland G (2008) Regulation and identity of Florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594PubMedCrossRefGoogle Scholar
  57. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The Pseudo-Response Regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedCrossRefGoogle Scholar
  58. Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  59. Wang S, Basten CJ, Zeng Z (2007) Windows Qtl Cartographer 2.5. N.C. State University, Bioinformatics Research Center, USAGoogle Scholar
  60. 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 323:930–934PubMedCrossRefGoogle Scholar
  61. Xu X, Xie Q, McClung CR (2010) Robust circadian rhythms of gene expression in Brassica rapa tissue culture. Plant Physiol 153:841–850PubMedCrossRefGoogle Scholar
  62. Yerushalmi S, Yakir E, Green RM (2011) Circadian clocks and adaptation in Arabidopsis. Mol Ecol 20:1155–1165PubMedCrossRefGoogle Scholar
  63. Zhang EE, Kay SA (2010) Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 11:764–776PubMedCrossRefGoogle Scholar
  64. 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 50:963–973PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • P. Lou
    • 1
  • Q. Xie
    • 1
  • X. Xu
    • 1
    • 3
  • C. E. Edwards
    • 2
  • M. T. Brock
    • 2
  • C. Weinig
    • 2
  • C. R. McClung
    • 1
  1. 1.Department of Biological Sciences, 6044 Gilman LaboratoriesDartmouth CollegeHanoverUSA
  2. 2.Department of BotanyUniversity of WyomingLaramieUSA
  3. 3.Hebei Key Laboratory of Molecular Cell Biology, College of Biological SciencesHebei Normal UniversityShijiazhuangChina

Personalised recommendations