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From Many, One: Genetic Control of Prolificacy during Maize Domestication


A reduction in number and an increase in size of inflorescences is a common aspect of plant domestication. When maize was domesticated from teosinte, the number and arrangement of ears changed dramatically. Teosinte has long lateral branches that bear multiple small ears at their nodes and tassels at their tips. Maize has much shorter lateral branches that are tipped by a single large ear with no additional ears at the branch nodes. To investigate the genetic basis of this difference in prolificacy (the number of ears on a plant), we performed a genome-wide QTL scan. A large effect QTL for prolificacy (prol1.1) was detected on the short arm of chromosome 1 in a location that has previously been shown to influence multiple domestication traits. We fine-mapped prol1.1 to a 2.7 kb “causative region” upstream of the grassy tillers1 (gt1) gene, which encodes a homeodomain leucine zipper transcription factor. Tissue in situ hybridizations reveal that the maize allele of prol1.1 is associated with up-regulation of gt1 expression in the nodal plexus. Given that maize does not initiate secondary ear buds, the expression of gt1 in the nodal plexus in maize may suppress their initiation. Population genetic analyses indicate positive selection on the maize allele of prol1.1, causing a partial sweep that fixed the maize allele throughout most of domesticated maize. This work shows how a subtle cis-regulatory change in tissue specific gene expression altered plant architecture in a way that improved the harvestability of maize.


Vyšlo v časopise: From Many, One: Genetic Control of Prolificacy during Maize Domestication. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003604
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003604

Souhrn

A reduction in number and an increase in size of inflorescences is a common aspect of plant domestication. When maize was domesticated from teosinte, the number and arrangement of ears changed dramatically. Teosinte has long lateral branches that bear multiple small ears at their nodes and tassels at their tips. Maize has much shorter lateral branches that are tipped by a single large ear with no additional ears at the branch nodes. To investigate the genetic basis of this difference in prolificacy (the number of ears on a plant), we performed a genome-wide QTL scan. A large effect QTL for prolificacy (prol1.1) was detected on the short arm of chromosome 1 in a location that has previously been shown to influence multiple domestication traits. We fine-mapped prol1.1 to a 2.7 kb “causative region” upstream of the grassy tillers1 (gt1) gene, which encodes a homeodomain leucine zipper transcription factor. Tissue in situ hybridizations reveal that the maize allele of prol1.1 is associated with up-regulation of gt1 expression in the nodal plexus. Given that maize does not initiate secondary ear buds, the expression of gt1 in the nodal plexus in maize may suppress their initiation. Population genetic analyses indicate positive selection on the maize allele of prol1.1, causing a partial sweep that fixed the maize allele throughout most of domesticated maize. This work shows how a subtle cis-regulatory change in tissue specific gene expression altered plant architecture in a way that improved the harvestability of maize.


Zdroje

1. HammerK (1984) Das domestikationssyndrom. Kulturpflanze 32: 11–34.

2. Harlan JR (1992) Crops and man. Madison, Wisconsin: American Society of Agronomy. 284 p.

3. GeptsP (2002) A Comparison between crop domestication, classical plant breeding, and genetic engineering. Crop Sci 42: 1780–1790.

4. MatsuokaY, VigourouxY, GoodmanMM, SanchezJ, BucklerES, et al. (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci U S A 99: 8060–8064.

5. PipernoDR, RanereAJ, HolstI, IriarteJ, DickauR (2009) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci U S A 106: 5019–5024.

6. IltisHH (1983) From teosinte to maize: The catastrophic sexual transmutation. Science 222: 886–94.

7. DoebleyJF, StecA, HubbardL (1997) The evolution of apical dominance in maize. Nature 386: 485–488.

8. ShannonLM (2012) The genetic architecture of maize domestication and range expansion. [PhD Dissertation] The University of Wisconsin-Madison

9. WhippleCJ, KebromTH, WeberAL, YangF, HallDH, et al. (2011) grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. Proc Natl Acad Sci U S A 108: e506–e512.

10. ClarkR, Nussbaum-WaglerT, QuijadaP, DoebleyJ (2006) A distant upstream enhancer at the maize domestication gene, tb1, has pleiotropic effects on plant and inflorescence architecture. Nat Genet 38: 594–597.

11. ArborA (1930) Studies in the Gramineae IX. 1. The nodal plexus. 2. Amphivasal bundles. Annals of Botany 44: 593–620.

12. WrightSI, BiIV, SchroederSG, YamasakiM, DoebleyJF, et al. (2005) The effects of artificial selection on the maize genome. Science 308: 1310–1314.

13. Eyre-WalkerA, GautRL, HiltonH, FeldmanDL, GautBS (1998) Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci U S A 95: 4441–4446.

14. HudsonRR (2007) The variance of coalescent time estimates from DNA sequences. J Mol Evol 64: 702–705.

15. ThomsonR, PritchardJK, ShenPD, OefnerPJ, FeldmanMW (2000) Recent common ancestry of human Y chromosomes: Evidence from DNA sequence data. Proc Natl Acad Sci U S A 97: 7360–7365.

16. Paterniani E, Goodman MM (1977) Races of maize in Brazil and adjacent areas. Mexico City: CIMMYT.

17. DoebleyJF, WendelJF, SmithJSC, StuberCW, GoodmanMM (1988) The origin of cornbelt maize: the isozyme evidence. Econ Bot 42: 120–131.

18. TanksleySD (2004) The genetic, developmental and molecular bases of fruit size an shape variation in tomato. Plant Cell 16: S181–S189.

19. DoebleyJ, StecA (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129: 285–295.

20. DoebleyJF, StecA (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134: 559–570.

21. BriggsWH, McMullenMD, GautBS, DoebleyJ (2007) Linkage mapping of domestication loci in a large maize teosinte backcross resource. Genetics 177: 1915–1928.

22. GrandilloS, TanksleySD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92: 935–952.

23. DoganlarS, FraryA, KuHM, TanksleySD (2002) Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpenellifolium (LA1589). Genome 45: 1189–1202.

24. KoinangeEMK, SinghSP, GeptsP (1996) Genetic control of the domestication syndrome in common bean. Crop Sci 36: 1037–1045.

25. PoncetV, LamyF, DevosK, GaleM, SarrA, et al. (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poacae). Theor Appl Genet 100: 147–159.

26. WillsDM, BurkeJM (2007) Quantitative trait locus analysis of the early domestication of sunflower. Genetics 176: 2589–2599.

27. TangS, LeonA, BridgesWC, KnappSJ (2006) Quantitative trait loci for genetically correlated seed traits are tightly linked to branching and pericarp pigment loci in sunflower. Crop Sci 46: 721–734.

28. LesterRN (1989) Evolution under domestication involving disturbance of genic balance. Euphytica 44: 125–132.

29. StuderA, ZhaoQ, Ross-IbarraJ, DoebleyJF (2011) A transposon insertion was the causative mutation in the maize domestication gene tb1. Nat Genet 43: 1160–1163.

30. WangH, Nussbaum-WaglerT, LiB, ZhaoQ, VigourouxY, et al. (2005) The origin of the naked grains of maize. Nature 436: 714–719.

31. BeadleGW (1939) Teosinte and the origin of maize. J Hered 30: 245–247.

32. DoebleyJF (2004) The genetics of maize evolution. Ann Rev Genet 38: 37–59.

33. StuderA, DoebleyJF (2011) Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1. Genetics 188: 673–681.

34. GrossBL, OlsenKM (2010) Genetic perspectives on crop domestication. Trends Plant Sci 15: 529–537.

35. LinZ, LiX, ShannonLM, YehCT, WangML, et al. (2012) Parallel domestication of the Shattering1 genes in cereals. Nat Genet 44: 720–724.

36. LiC, ZhouA, SangT (2006) Rice domestication by reducing shattering. Science 311: 1936–1939.

37. KonishiS, IzawaT, LinSY, EbanaK, FukutaY, et al. (2006) An SNP caused loss of seed shattering during rice domestication. Science 312: 1392–1396.

38. CongB, BarreroLS, TanksleySD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40: 800–804.

39. FraryA, NesbittTC, FraryA, GrandilloS, van der KnaapE, et al. (2000) fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 289: 85–88.

40. JinJ, HuangW, GaoJP, YangJ, ShiM, et al. (2008) Genetic control of rice plant architecture under domestication. Nat Genet 40: 1365–1369.

41. TanL, LiX, LiuF, SunX, LiC, et al. (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40: 1360–1364.

42. HungHY, ShannonLM, TianF, BradburyPJ, ChenC, et al. (2012) ZmCCT and the genetic basis of day-length adaptation underlying the post-domestication spread of maize. Proc Natl Acad Sci U S A 109: E1913–E1921.

43. KomatsudaT, PourkheirandishM, HeC, AzhaguvelP, KanamoriH, et al. (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci U S A 104: 1424–1429.

44. DussertY, RemigereauMS, FontaineMC, SnircA, LakisG, et al. (2013) Polymorphism pattern at a miniature inverted-repeat transposable element locus downstream of the domestication gene Teosinte-branched1 in wild and domesticated pearl millet. Mol Ecol 22: 327–340.

45. XiaoH, JiangN, SchaffnerE, StockingerEJ, van der KnaapE (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527–1530.

46. GallavottiA, ZhaoQ, KyozukaJ, MeeleyRB, RitterMK, et al. (2004) The role of barren stalk1 in the architecture of maize. Nature 432: 630–635.

47. RalphP, CoopG (2010) Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186: 647–668.

48. HuffordMB, XuX, van HeerwaardenJ, PyhäjärviT, ChiaJM, et al. (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44: 808–811.

49. InnanH, KimY (2004) Pattern of polymorphism after strong artificial selection in a domestication event. Proc Natl Acad Sci U S A 101: 10667–10672.

50. HermissonJ, PenningsPS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352.

51. SmithH, WhitelamGC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant, Cell and Environment 20: 840–844.

52. ElshireRJ, GlaubitzJC, SunQ, PolandJA, KawamotoK, et al. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6: e19379.

53. BromanKW, WuH, SenS, ChurchillGA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889–890.

54. JacksonD, VeitB, HakeS (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413.

55. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

56. 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.

57. PritchardJK, StephensM, DonnellyP (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

58. TeshimaKM, InnanH (2009) mbs: modifying Hudson's ms software to generate samples of DNA sequences with a biallelic site under selection. BMC Bioinformatics 10: 166.

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


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