Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize

English version České info

We compared the genetic architecture of thirteen maize morphological traits in a large population of recombinant inbred lines. Four traits from the male inflorescence (tassel) and three traits from the female inflorescence (ear) were measured and studied using linkage and genome-wide association analyses and compared to three flowering and three leaf traits previously studied in the same population. Inflorescence loci have larger effects than flowering and leaf loci, and ear effects are larger than tassel effects. Ear trait models also have lower predictive ability than tassel, flowering, or leaf trait models. Pleiotropic loci were identified that control elongation of ear and tassel, consistent with their common developmental origin. For these pleiotropic loci, the ear effects are larger than tassel effects even though the same causal polymorphisms are likely involved. This implies that the observed differences in genetic architecture are not due to distinct features of the underlying polymorphisms. Our results support the hypothesis that genetic architecture is a function of trait stability over evolutionary time, since the traits that changed most during the relatively recent domestication of maize have the largest effects.

Vyšlo v časopise: Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002383
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002383

Souhrn

Zdroje

1. FlintJMackayTFC 2009 Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research 19 723 733 doi:10.1101/gr.086660.108

2. ValdarWSolbergLCGauguierDBurnettSKlenermanP 2006 Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat Genet 38 879 887 doi:10.1038/ng1840

3. BucklerESHollandJBBradburyPJAcharyaCBBrownPJ 2009 The genetic architecture of maize flowering time. Science 325 714 718 doi:10.1126/science.1174276

4. TianFBradburyPJBrownPJHungHSunQ 2011 Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43 159 162 doi:10.1038/ng.746

5. KumpKLBradburyPJWisserRJBucklerESBelcherAR 2011 Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43 163 168 doi:10.1038/ng.747

6. GudbjartssonDFWaltersGBThorleifssonGStefanssonHHalldorssonBV 2008 Many sequence variants affecting diversity of adult human height. Nat Genet 40 609 615 doi:10.1038/ng.122

7. LettreGJacksonAUGiegerCSchumacherFRBerndtSI 2008 Identification of ten loci associated with height highlights new biological pathways in human growth. Nat Genet 40 584 591 doi:10.1038/ng.125

8. WeedonMNLangoHLindgrenCMWallaceCEvansDM 2008 Genome-wide association analysis identifies 20 loci that influence adult height. Nat Genet 40 575 583 doi:10.1038/ng.121

9. AllenHLEstradaKLettreGBerndtSIWeedonMN 2010 Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature

10. FisherRA 1930 The genetical theory of natural selection Oxford University Press, Oxford, UK p

11. OrrHA 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52 935 949

12. BoykoARQuignonPLiLSchoenebeckJJDegenhardtJD 2010 A Simple Genetic Architecture Underlies Morphological Variation in Dogs. PLoS Biol 8 e1000451 doi:10.1371/journal.pbio.1000451

13. Van LaereASNguyenMBraunschweigMNezerCColletteC 1998 A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Hippocampus 8 244 261

14. CarlborgÖJacobssonLÅhgrenPSiegelPAnderssonL 2006 Epistasis and the release of genetic variation during long-term selection. Nat Genet 38 418 420 doi:10.1038/ng1761

15. ColosimoPFPeichelCLNerengKBlackmanBKShapiroMD 2004 The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol 2 E109 doi:10.1371/journal.pbio.0020109

16. SalomePABombliesKLaitinenRAEYantLMottR 2011 Genetic Architecture of Flowering Time Variation in Arabidopsis thaliana. Genetics. Available: http://www.genetics.org/cgi/doi/10.1534/genetics.111.126607. Accessed 30 Mar 2011

17. Ross-IbarraJMorrellPLGautBS 2007 Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc Natl Acad Sci U S A 104 Suppl 1 8641 8648 doi:10.1073/pnas.0700643104

18. GoddardMEHayesBJ 2009 Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet 10 381 391 doi:10.1038/nrg2575

19. MatsuokaYVigourouxYGoodmanMMSanchez GJBucklerE 2002 A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci U S A 99 6080 6084 doi:10.1073/pnas.052125199

20. BeadleGW 1978 Teosinte and the origin of maize. Maize breeding and genetics. Section 2. Evolution.. Available: http://apps.isiknowledge.com/full_record.do?product=CABI&search_mode=GeneralSearch&qid=1&SID=3A47lK9MCanJdApDb&page=1&doc=4. Accessed 15 Mar 2011

21. DoebleyJStecAHubbardL 1997 The evolution of apical dominance in maize. Nature 386 485 488 doi:10.1038/386485a0

22. WangHNussbaum-WaglerTLiBZhaoQVigourouxY 2005 The origin of the naked grains of maize. Nature 436 714 719 doi:10.1038/nature03863

23. BeadleGW 1980 The ancestry of corn. Sci Amer 242 112 119

24. MangelsdorfPC 1986 The origin of corn. Sci Amer 254 80 86

25. VollbrechtESchmidtRJ 2009 Development of the Inflorescences. Handbook of Maize: Its Biology New York, NY Springer New York 13 40 Available: http://www.springerlink.com/content/v14444r6930r16v8/. Accessed 21 Mar 2011

26. ParkinsonSEGrossSMHollickJB 2007 Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states. Dev Biol 308 462 473 doi:10.1016/j.ydbio.2007.06.004

27. YuJHollandJBMcMullenMDBucklerES 2008 Genetic design and statistical power of nested association mapping in maize. Genetics 178 539 551 doi:10.1534/genetics.107.074245

28. McMullenMDKresovichSVilledaHSBradburyPLiH 2009 Genetic Properties of the Maize Nested Association Mapping Population. Science 325 737 740 doi:10.1126/science.1174320

29. GoreMAChiaJ-MElshireRJSunQErsozES 2009 A First-Generation Haplotype Map of Maize. Science 326 1115 1117 doi:10.1126/science.1177837

30. ValdarWHolmesCCMottRFlintJ 2009 Mapping in Structured Populations by Resample Model Averaging. Genetics 182 1263 1277 doi:10.1534/genetics.109.100727

31. BortiriEChuckGVollbrechtERochefordTMartienssenR 2006 ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18 574 585 doi:10.1105/tpc.105.039032

32. MorenoMAHarperLCKruegerRWDellaportaSLFreelingM 1997 liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev 11 616 628

33. JiaoYWangYXueDWangJYanM 2010 Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42 541 544 doi:10.1038/ng.591

34. MiuraKIkedaMMatsubaraASongX-JItoM 2010 OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42 545 549 doi:10.1038/ng.592

35. SternD 2010 Evolution, Development, and the Predictable Genome. Roberts & Company, USA. p. Available: http://www.publish.csiro.au/nid/223/pid/6186.htm. Accessed 21 Mar 2011

36. DoebleyJ 2004 The genetics of maize evolution. Annu Rev Genet 38 37 59 doi:10.1146/annurev.genet.38.072902.092425

37. LauterNDoebleyJ 2002 Genetic variation for phenotypically invariant traits detected in teosinte: implications for the evolution of novel forms. Genetics 160 333

38. GillespieJH 2004 Population genetics: a concise guide Johns Hopkins Univ Pr p

39. GibsonG 2009 Decanalization and the origin of complex disease. Nature Reviews Genetics 10 134 140

40. IltisHH 1983 From Teosinte to Maize: The Catastrophic Sexual Transmutation. Science 222 886 894 doi:10.1126/science.222.4626.886

41. DudleyJWLambertRJ 2004 100 Generations of Selection for Oil and Protein in Corn. Plant Breeding Rev 24 79 110 doi:10.1002/9780470650240.ch5

42. DeLongACalderon-UrreaADellaportaSL 1993 Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74 757 768

43. McSteenPMalcomberSSkirpanALundeCWuX 2007 barren inflorescence2 Encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiol 144 1000 1011 doi:10.1104/pp.107.098558

44. BensenRJJohalGSCraneVCTossbergJTSchnablePS 1995 Cloning and characterization of the maize An1 gene. Plant Cell 7 75 84 doi:10.1105/tpc.7.1.75

45. PengJRichardsDEHartleyNMMurphyGPDevosKM 1999 Green revolution genes encode mutant gibberellin response modulators. Nature 400 256 261 doi:10.1038/22307

46. VollbrechtEVeitBSinhaNHakeS 1991 The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350 241 243 doi:10.1038/350241a0

47. ChuckGMeeleyRBHakeS 1998 The control of maize spikelet meristem fate by theAPETALA2-like gene indeterminate spikelet1. Genes & Development 12 1145 1154

48. BombliesKWangR-LAmbroseBASchmidtRJMeeleyRB 2003 Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130 2385 2395

49. AcostaIFLaparraHRomeroSPSchmelzEHambergM 2009 tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323 262 265 doi:10.1126/science.1164645

50. ChuckGCiganAMSaeteurnKHakeS 2007 The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39 544 549 doi:10.1038/ng2001

51. ChuckGMeeleyRIrishESakaiHHakeS 2007 The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39 1517 1521 doi:10.1038/ng.2007.20

52. VeitBBriggsSPSchmidtRJYanofskyMFHakeS 1998 Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature 393 166 168 doi:10.1038/30239

53. WalshJWatersCAFreelingM 1998 The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary. Genes & Development 12 208 218 doi:10.1101/gad.12.2.208

54. GallavottiAZhaoQKyozukaJMeeleyRBRitterMK 2004 The role of barren stalk1 in the architecture of maize. Nature 432 630 635 doi:10.1038/nature03148

55. GallavottiABarazeshSMalcomberSHallDJacksonD 2008 sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. Proceedings of the National Academy of Sciences 105 15196

56. Taguchi-ShiobaraF 2001 The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes & Development 15 2755 2766 doi:10.1101/gad.208501

57. BommertPLundeCNardmannJVollbrechtERunningM 2005 thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132 1235

58. WhippleCJHallDHDeBlasioSTaguchi-ShiobaraFSchmidtRJ 2010 A conserved mechanism of bract suppression in the grass family. The Plant Cell Online 22 565

59. VollbrechtESpringerPSGohLBucklerESIVMartienssenR 2005 Architecture of floral branch systems in maize and related grasses. Nature 436 1119 1126 doi:10.1038/nature03892

60. ChuckGWhippleCJacksonDHakeS 2010 The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137 1585 1585 doi:10.1242/dev.052373

61. Satoh-NagasawaNNagasawaNMalcomberSSakaiHJacksonD 2006 A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441 227 230 doi:10.1038/nature04725

62. ChuckG 2002 The Control of Spikelet Meristem Identity by the branched silkless1 Gene in Maize. Science 298 1238 1241 doi:10.1126/science.1076920

63. MuszynskiMGDamTLiBShirbrounDMHouZ 2006 delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant physiology 142 1523