#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The Flowering Repressor Underlies a Novel QTL Interacting with the Genetic Background


The timing of flowering initiation is a fundamental trait for the adaptation of annual plants to different environments. Large amounts of intraspecific quantitative variation have been described for it among natural accessions of many species, but the molecular and evolutionary mechanisms underlying this genetic variation are mainly being determined in the model plant Arabidopsis thaliana. To find novel A. thaliana flowering QTL, we developed introgression lines from the Japanese accession Fuk, which was selected based on the substantial transgression observed in an F2 population with the reference strain Ler. Analysis of an early flowering line carrying a single Fuk introgression identified Flowering Arabidopsis QTL1 (FAQ1). We fine-mapped FAQ1 in an 11 kb genomic region containing the MADS transcription factor gene SHORT VEGETATIVE PHASE (SVP). Complementation of the early flowering phenotype of FAQ1-Fuk with a SVP-Ler transgen demonstrated that FAQ1 is SVP. We further proved by directed mutagenesis and transgenesis that a single amino acid substitution in SVP causes the loss-of-function and early flowering of Fuk allele. Analysis of a worldwide collection of accessions detected FAQ1/SVP-Fuk allele only in Asia, with the highest frequency appearing in Japan, where we could also detect a potential ancestral genotype of FAQ1/SVP-Fuk. In addition, we evaluated allelic and epistatic interactions of SVP natural alleles by analysing more than one hundred transgenic lines carrying Ler or Fuk SVP alleles in five genetic backgrounds. Quantitative analyses of these lines showed that FAQ1/SVP effects vary from large to small depending on the genetic background. These results support that the flowering repressor SVP has been recently selected in A. thaliana as a target for early flowering, and evidence the relevance of genetic interactions for the intraspecific evolution of FAQ1/SVP and flowering time.


Vyšlo v časopise: The Flowering Repressor Underlies a Novel QTL Interacting with the Genetic Background. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003289
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003289

Souhrn

The timing of flowering initiation is a fundamental trait for the adaptation of annual plants to different environments. Large amounts of intraspecific quantitative variation have been described for it among natural accessions of many species, but the molecular and evolutionary mechanisms underlying this genetic variation are mainly being determined in the model plant Arabidopsis thaliana. To find novel A. thaliana flowering QTL, we developed introgression lines from the Japanese accession Fuk, which was selected based on the substantial transgression observed in an F2 population with the reference strain Ler. Analysis of an early flowering line carrying a single Fuk introgression identified Flowering Arabidopsis QTL1 (FAQ1). We fine-mapped FAQ1 in an 11 kb genomic region containing the MADS transcription factor gene SHORT VEGETATIVE PHASE (SVP). Complementation of the early flowering phenotype of FAQ1-Fuk with a SVP-Ler transgen demonstrated that FAQ1 is SVP. We further proved by directed mutagenesis and transgenesis that a single amino acid substitution in SVP causes the loss-of-function and early flowering of Fuk allele. Analysis of a worldwide collection of accessions detected FAQ1/SVP-Fuk allele only in Asia, with the highest frequency appearing in Japan, where we could also detect a potential ancestral genotype of FAQ1/SVP-Fuk. In addition, we evaluated allelic and epistatic interactions of SVP natural alleles by analysing more than one hundred transgenic lines carrying Ler or Fuk SVP alleles in five genetic backgrounds. Quantitative analyses of these lines showed that FAQ1/SVP effects vary from large to small depending on the genetic background. These results support that the flowering repressor SVP has been recently selected in A. thaliana as a target for early flowering, and evidence the relevance of genetic interactions for the intraspecific evolution of FAQ1/SVP and flowering time.


Zdroje

1. AndersonJT, WillisJH, Mitchell-OldsT (2011) Evolutionary genetics of plant adaptation. Trends Genet 27: 258–266.

2. RouxF, TouzetP, CuguenJ, Le CorreV (2006) How to be early flowering: an evolutionary perspective. Trends Plant Sci 11: 375–381.

3. JungC, MullerAE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14: 563–573.

4. AndresF, CouplandG (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13: 627–639.

5. AusinI, Alonso-BlancoC, Martinez-ZapaterJM (2005) Environmental regulation of flowering. Int J Dev Biol 49: 689–705.

6. KobayashiY, WeigelD (2007) Move on up, it's time for change–mobile signals controlling photoperiod-dependent flowering. Genes Dev 21: 2371–2384.

7. KimD-H, DoyleMR, SungS, AmasinoRM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25: 277–299.

8. Mitchell-OldsT, SchmittJ (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: 947–952.

9. Alonso-BlancoC, AartsMG, BentsinkL, KeurentjesJJ, ReymondM, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877–1896.

10. WeigelD (2012) Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol 158: 2–22.

11. HoffmannMH (2002) Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). J Biogeogr 29: 125–134.

12. StinchcombeJR, WeinigC, UngererM, OlsenKM, MaysC, et al. (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci U S A 101: 4712–4717.

13. CaicedoAL, StinchcombeJR, OlsenKM, SchmittJ, PuruggananMD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci U S A 101: 15670–15675.

14. BalasubramanianS, SureshkumarS, AgrawalM, MichaelTP, WessingerC, et al. (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat Genet 38: 711–715.

15. Mendez-VigoB, PicoFX, RamiroM, Martinez-ZapaterJM, Alonso-BlancoC (2011) Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiol 157: 1942–1955.

16. SamisKE, MurrenCJ, BossdorfO, DonohueK, FensterCB, et al. (2012) Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecol Evol 2: 1162–1180.

17. RédeiG (1970) Arabidopsis thaliana (L.) Heynh. A review of the genetics and biology. Bibliogr Genet 1–151.

18. MichaelsSD, AmasinoRM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949–956.

19. JohansonU, WestJ, ListerC, MichaelsS, AmasinoR, et al. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344–347.

20. SaloméPA, BombliesK, LaitinenRA, YantL, MottR, et al. (2011) Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188: 421–433.

21. El-LithyME, BentsinkL, HanhartCJ, RuysGJ, RovitoD, et al. (2006) New arabidopsis recombinant inbred line populations genotyped using SNPWave and their use for mapping flowering-time quantitative trait loci. Genetics 172: 1867–1876.

22. SimonM, LoudetO, DurandS, BerardA, BrunelD, et al. (2008) Quantitative trait loci mapping in five new large recombinant inbred line populations of Arabidopsis thaliana genotyped with consensus single-nucleotide polymorphism markers. Genetics 178: 2253–2264.

23. O'NeillC, MorganC, KirbyJ, TschoepH, DengP, et al. (2008) Six new recombinant inbred populations for the study of quantitative traits in Arabidopsis thaliana. Theor Appl Genet 116: 623–634.

24. SchwartzC, BalasubramanianS, WarthmannN, MichaelTP, LempeJ, et al. (2009) Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183: 723–732.

25. BrachiB, FaureN, HortonM, FlahauwE, VazquezA, et al. (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6: e1000940 doi:10.1371/journal.pgen.1000940.

26. Mendez-VigoB, de AndresMT, RamiroM, Martinez-ZapaterJM, Alonso-BlancoC (2010) Temporal analysis of natural variation for the rate of leaf production and its relationship with flowering initiation in Arabidopsis thaliana. J Exp Bot 61: 1611–1623.

27. Sanchez-BermejoE, Mendez-VigoB, PicoFX, Martinez-ZapaterJM, Alonso-BlancoC (2012) Novel natural alleles at FLC and LVR loci account for enhanced vernalization responses in Arabidopsis thaliana. Plant Cell Environ 35: 1672–1684.

28. KeurentjesJJ, BentsinkL, Alonso-BlancoC, HanhartCJ, Blankestijn-De VriesH, et al. (2007) Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175: 891–905.

29. TörjékO, MeyerRC, ZehnsdorfM, TeltowM, StrompenG, et al. (2008) Construction and analysis of 2 reciprocal arabidopsis introgression line populations. J Hered 99: 396–406.

30. KoverPX, ValdarW, TrakaloJ, ScarcelliN, EhrenreichIM, et al. (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet 5: e1000551 doi:10.1371/journal.pgen.1000551.

31. HuangX, PauloMJ, BoerM, EffgenS, KeizerP, et al. (2011) Analysis of natural allelic variation in Arabidopsis using a multiparent recombinant inbred line population. Proc Natl Acad Sci U S A 108: 4488–4493.

32. AtwellS, HuangYS, VilhjalmssonBJ, WillemsG, HortonM, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.

33. LiY, HuangY, BergelsonJ, NordborgM, BorevitzJO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107: 21199–21204.

34. MalmbergRL, MauricioR (2005) QTL-based evidence for the role of epistasis in evolution. Genet Res 86: 89–95.

35. KoornneefM, Blankestijn-de VriesH, HanhartCJ, SoppeW, PeetersAJM (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J 6: 911–919.

36. LeeI, MichaelsSD, MasshardtAS, AmasinoRM (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J 6: 903–909.

37. FensterCB, GallowayLF, ChaoL (1997) Epistasis and its consequences for the evolution of natural populations. Trends Ecol Evol 12: 282–286.

38. BenfeyPN, Mitchell-OldsT (2008) From genotype to phenotype: Systems biology meets natural variation. Science 320: 495–497.

39. PhillipsPC (2008) Epistasis–the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855–867.

40. Jimenez-GomezJM, WallaceAD, MaloofJN (2010) Network analysis identifies ELF3 as a QTL for the shade avoidance response in Arabidopsis. PLoS Genet 6: e1001100 doi:10.1371/journal.pgen.1001100.

41. RosloskiSM, JaliSS, BalasubramanianS, WeigelD, GrbicV (2010) Natural diversity in flowering responses of Arabidopsis thaliana caused by variation in a tandem gene array. Genetics 186: 263–276.

42. MichaelsSD, HeY, ScortecciKC, AmasinoRM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci U S A 100: 10102–10107.

43. CousthamV, LiP, StrangeA, ListerC, SongJ, et al. (2012) Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337: 584–587.

44. Le CorreV, RouxF, ReboudX (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 19: 1261–1271.

45. GazzaniS, GendallAR, ListerC, DeanC (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132: 1107–1114.

46. LempeJ, BalasubramanianS, SureshkumarS, SinghA, SchmidM, et al. (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1: e6 doi:10.1371/journal.pgen.0010006.

47. WernerJD, BorevitzJO, UhlenhautNH, EckerJR, ChoryJ, et al. (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170: 1197–1207.

48. ShindoC, AranzanaMJ, ListerC, BaxterC, NichollsC, et al. (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138: 1163–1173.

49. ToomajianC, HuTT, AranzanaMJ, ListerC, TangC, et al. (2006) A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biol 4: e137 doi:10.1371/journal.pbio.0040137.

50. HartmannU, HohmannS, NettesheimK, WismanE, SaedlerH, et al. (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21: 351–360.

51. NordborgM, HuTT, IshinoY, JhaveriJ, ToomajianC, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3: e196 doi:10.1371/journal.pbio.0030196.

52. SmaczniakC, ImminkRG, AngenentGC, KaufmannK (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139: 3081–3098.

53. LiD, LiuC, ShenL, WuY, ChenH, et al. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15: 110–120.

54. JangS, TortiS, CouplandG (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60: 614–625.

55. LeeJH, YooSJ, ParkSH, HwangI, LeeJS, et al. (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21: 397–402.

56. FujiwaraS, OdaA, YoshidaR, NiinumaK, MiyataK, et al. (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20: 2960–2971.

57. de FolterS, ImminkRG, KiefferM, ParenicovaL, HenzSR, et al. (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17: 1424–1433.

58. GregisV, SessaA, ColomboL, KaterMM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18: 1373–1382.

59. KaufmannK, WellmerF, MuinoJM, FerrierT, WuestSE, et al. (2010) Orchestration of floral initiation by APETALA1. Science 328: 85–89.

60. TaoZ, ShenL, LiuC, LiuL, YanY, et al. (2012) Genome-wide identification of SOC1 and SVP targets during the floral transition in Arabidopsis. Plant J 70: 549–561.

61. HuangK, LouisJM, DonaldsonL, LimFL, SharrocksAD, et al. (2000) Solution structure of the MEF2A-DNA complex: structural basis for the modulation of DNA bending and specificity by MADS-box transcription factors. Embo J 19: 2615–2628.

62. WernerJD, BorevitzJO, WarthmannN, TrainerGT, EckerJR, et al. (2005) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc Natl Acad Sci U S A 102: 2460–2465.

63. CaicedoAL, RichardsC, EhrenreichIM, PuruggananMD (2009) Complex rearrangements lead to novel chimeric gene fusion polymorphisms at the Arabidopsis thaliana MAF2-5 flowering time gene cluster. Mol Biol Evol 26: 699–711.

64. HuangX, EffgenS, MeyerRC, TheresK, KoornneefM (2012) Epistatic natural allelic variation reveals a function of AGAMOUS-LIKE6 in axillary bud formation in Arabidopsis. Plant Cell 24: 2364–2379.

65. YanL, LoukoianovA, TranquilliG, HelgueraM, FahimaT, et al. (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci U S A 100: 6263–6268.

66. MasieroS, LiMA, WillI, HartmannU, SaedlerH, et al. (2004) INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum. Development 131: 5981–5990.

67. CiannameaS, KaufmannK, FrauM, TonacoIA, PetersenK, et al. (2006) Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne. J Exp Bot 57: 3419–3431.

68. TrevaskisB, TadegeM, HemmingMN, PeacockWJ, DennisES, et al. (2007) Short vegetative phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiol 143: 225–235.

69. LiZM, ZhangJZ, MeiL, DengXX, HuCG, et al. (2010) PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants. Plant Mol Biol 74: 129–142.

70. LeeJH, ParkSH, AhnJH (2012) Functional conservation and diversification between rice OsMADS22/OsMADS55 and Arabidopsis SVP proteins. Plant Sci 185–186: 97–104.

71. CohenO, BorovskyY, David-SchwartzR, ParanI (2012) CaJOINTLESS is a MADS-box gene involved in suppression of vegetative growth in all shoot meristems in pepper. J Exp Bot 63: 4947–4957.

72. BielenbergDG, WangY, LiZ, ZhebentyayevaT, FanS, et al. (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4: 495–507.

73. RockmanMV (2012) The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66: 1–17.

74. OrrHA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6: 119–127.

75. KempinSA, SavidgeB, YanofskyMF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267: 522–525.

76. FerrandizC, GuQ, MartienssenR, YanofskyMF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127: 725–734.

77. PelazS, DittaGS, BaumannE, WismanE, YanofskyMF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200–203.

78. ScortecciK, MichaelsSD, AmasinoRM (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol Biol 52: 915–922.

79. Alonso-BlancoC, PeetersAJ, KoornneefM, ListerC, DeanC, et al. (1998) Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J 14: 259–271.

80. BellCJ, EckerJR (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19: 137–144.

81. PicoFX, Mendez-VigoB, Martinez-ZapaterJM, Alonso-BlancoC (2008) Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian peninsula. Genetics 180: 1009–1021.

82. NicholasKB, NicholasHBJ, DeerfieldDW (1997) GeneDoc: Analysis and Visualization of Genetic Variation. EMBNEW NEWS 4.

83. LibradoP, RozasJ (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

84. HepworthSR, ValverdeF, RavenscroftD, MouradovA, CouplandG (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. Embo J 21: 4327–4337.

85. LazoGR, SteinPA, LudwigRA (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology 9: 963–967.

86. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.

87. GomaaNH, Montesinos-NavarroA, Alonso-BlancoC, PicoFX (2011) Temporal variation in genetic diversity and effective population size of Mediterranean and subalpine Arabidopsis thaliana populations. Mol Ecol 20: 3540–3554.

88. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#