#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genetic Analysis of Floral Symmetry in Van Gogh's Sunflowers Reveals Independent Recruitment of Genes in the Asteraceae


The genetic basis of floral symmetry is a topic of great interest because of its effect on pollinator behavior and, consequently, plant diversification. The Asteraceae, which is the largest family of flowering plants, is an ideal system in which to study this trait, as many species within the family exhibit a compound inflorescence containing both bilaterally symmetric (i.e., zygomorphic) and radially symmetric (i.e., actinomorphic) florets. In sunflower and related species, the inflorescence is composed of a single whorl of ray florets surrounding multiple whorls of disc florets. We show that in double-flowered (dbl) sunflower mutants (in which disc florets develop bilateral symmetry), such as those captured by Vincent van Gogh in his famous nineteenth-century sunflower paintings, an insertion into the promoter region of a CYCLOIDEA (CYC)-like gene (HaCYC2c) that is normally expressed specifically in WT rays is instead expressed throughout the inflorescence, presumably resulting in the observed loss of actinomorphy. This same gene is mutated in two independent tubular-rayed (tub) mutants, though these mutations involve apparently recent transposon insertions, resulting in little or no expression and radialization of the normally zygomorphic ray florets. Interestingly, a phylogenetic analysis of CYC-like genes from across the family suggests that different paralogs of this fascinating gene family have been independently recruited to specify zygomorphy in different species within the Asteraceae.


Vyšlo v časopise: Genetic Analysis of Floral Symmetry in Van Gogh's Sunflowers Reveals Independent Recruitment of Genes in the Asteraceae. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002628
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002628

Souhrn

The genetic basis of floral symmetry is a topic of great interest because of its effect on pollinator behavior and, consequently, plant diversification. The Asteraceae, which is the largest family of flowering plants, is an ideal system in which to study this trait, as many species within the family exhibit a compound inflorescence containing both bilaterally symmetric (i.e., zygomorphic) and radially symmetric (i.e., actinomorphic) florets. In sunflower and related species, the inflorescence is composed of a single whorl of ray florets surrounding multiple whorls of disc florets. We show that in double-flowered (dbl) sunflower mutants (in which disc florets develop bilateral symmetry), such as those captured by Vincent van Gogh in his famous nineteenth-century sunflower paintings, an insertion into the promoter region of a CYCLOIDEA (CYC)-like gene (HaCYC2c) that is normally expressed specifically in WT rays is instead expressed throughout the inflorescence, presumably resulting in the observed loss of actinomorphy. This same gene is mutated in two independent tubular-rayed (tub) mutants, though these mutations involve apparently recent transposon insertions, resulting in little or no expression and radialization of the normally zygomorphic ray florets. Interestingly, a phylogenetic analysis of CYC-like genes from across the family suggests that different paralogs of this fascinating gene family have been independently recruited to specify zygomorphy in different species within the Asteraceae.


Zdroje

1. DonoghueMJReeRHBaumDA 1998 Phylogeny and the evolution of flower symmetry in the Asteridae. Trends Plant Sci 3 311 317

2. EndressPK 2001 Evolution of floral symmetry. Curr Opin Plant Biol 4 86 91

3. PrestonJCHilemanLC 2009 Developmental genetics of floral symmetry evolution. Trends Plant Sci 14 147 154

4. SargentRD 2004 Floral symmetry affects speciation rates in angiosperms. Proc R Soc Lond B Biol Sci 271 603 608

5. TakhtajanA 1969 Flowering Plants: Origin and Dispersal. Oliver and Boyd, Edinburgh

6. DilcherD 2000 Toward a new synthesis: Major evolutionary trends in the angiosperm fossil record. Proc Nat Acad Sci USA 97 7030 7036

7. WesterkampCClaßen-BockhoffR 2007 Bilabiate flowers: The ultimate response to bees? Ann Bot 100 361 374

8. CubasP 2004 Floral zygomorphy, the recurring evolution of a successful trait. Bioessays 26 1175 1184

9. FunkVABayerRJKeeleySChanRWatsonL 2005 Everywhere but Antarctica: Using a supertree to understand the diversity and distribution of the Compositae. Biol Skr 55 343 373

10. StevensPF 2001 onwards Angiosperm Phylogeny Website. Version 8, June 2007. http://www.mobot.org/MOBOT/research/APweb/

11. PaneroJLFunkVA 2008 The value of sampling anomalous taxa in phylogenetic studies: Major clades of the Asteraceae revealed. Mol Phylogenet Evol 47 757 782

12. FunkVASusannaAStuessyTFBayerRJ 2009 Systematics, Evolution, and Biogeography of Compositae. International Association for Plant Taxonomy (Vienna)

13. AnderssonS 2008 Pollinator and nonpollinator selection on ray morphology in Leucanthemum vulgare (oxeye daisy, Asteraceae). Am J Bot 95 1072 1078

14. NielsenLRPhilippMSiegismundHR 2002 Selective advantage of ray florets in Scalesia affinis and S. pedunculata (Asteraceae), two endemic species from the Galapagos. Evol Ecol 16 139 153

15. StuessyTFSpoonerDMEvansKA 1986 Adaptive significance of ray corollas in Helianthus grosseserratus (Compositae). Am Midl Nat 115 191 197

16. FengXZZhaoZTianZXuSLuoY 2006 Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Nat Acad Sci USA 103 4970 4975

17. LuoDCarpenterRVincentCCopseyLCoenE 1996 Origin of floral asymmetry in Antirrhinum. Nature 383 794 799

18. CorleySBCarpenterRCopseyLCoenE 2005 Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Nat Acad Sci USA 102 5068 50734

19. BroholmSKTähtiharjuSLaitinenRAEAlbertVATeeriTH 2008 A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Nat Acad Sci USA 105 9117 9122

20. KimMCuiM-LCubasPGilliesALeeK 2008 Regulatory genes control a key morphological and ecological trait transferred between species. Science 322 1116 1119

21. CarlsonSEHowarthDGDonoghueMJ 2011 Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evolutionary Biology, 11 325

22. ChapmanMALeebens-MackJBurkeJM 2008 Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Mol Biol Evol 25 1260 1273

23. CockerellTDA 1915 Specific and varietal characters in annual sunflowers. Am Nat 49 609 622

24. FambriniMBertiniDPugliesiC 2003 The genetic basis of a mutation that alters the floral symmetry in sunflower. Ann Appl Biol 143 341 347

25. FambriniMMichelottiVPugliesiC 2007 The unstable tubular ray flower allele of sunflower: inheritance of the reversion to wild-type. Plant Breeding 126 548 550

26. FickGN 1976 Genetics of floral color and morphology in sunflowers. J Hered 67 227 230

27. WitteC-PLeQHBureauTKiumarA 2001 Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Nat Acad Sci USA 98 13778 13783

28. NealPRDafniAGiurfaM 1998 Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu Rev Ecol Syst 29 345 373

29. BartlettMESpechtCD 2011 Changes in expression pattern of the teosinte branched1-like genes in the Zingiberales provide a mechanism for evolutionary shifts in symmetry across the order. Am J Bot 98 227 243

30. CiterneHLPenningtonRTCronkQCB 2006 An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proc Nat Acad Sci USA 103 12017 12020

31. HilemanLCKramerEMBaumDA 2003 Differential regulation of symmetry genes and the evolution of floral morphologies. Proc Nat Acad Sci USA 100 12814 12819

32. ZhangWKramerEMDavisCC 2010 Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proc Nat Acad Sci USA 100 6388 6393

33. ZhouXRWangYZSmithJFChenRJ 2008 Altered expression patterns of TCP and MYB genes relating to the floral developmental transition from initial zygomorphy to actinomorphy in Bournea (Gesneriaceae). New Phytol 178 532 543

34. HowarthDGDonoghueMJ 2005 Duplications in CYC-like genes from Dipsacales correlate with floral form. Int J Plant Sci 166 357 370

35. PrestonJCMartinezCCHilemanLC 2011 Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome. Proc Nat Acad Sci USA 108 2343 2348

36. HughesTA 2006 Regulation of gene expression by alternative untranslated regions. Trends Genet 22 119 122

37. PesoleGMignoneFGissiCGrilloGLicciulliF 2001 Structural and functional features of eukaryotic mRNA untranslated regions. Gene 276 73 81

38. BarkerMSKaneNCMatvienkoMKozikAMichelmoreRW 2008 Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25 2445 2555

39. TankDCDonoghueMJ 2010 Phylogeny and phylogenetic nomenclature of the Campanulidae based on an expanded sample of genes and taxa. Syst Bot 35 425 441

40. WoodTBurkeJMRiesebergLH 2005 Parallel genotypic adaptation: when evolution repeats itself. Genetica 123 157 170

41. ColosimoPFHosemannKEBalabhadraSVillarealGDicksonM 2005 Widespread parallel evolution in sticklebacks by repeated fixation ofectodysplasin alleles. Science 307 1928 1933

42. McCrackenKGBargerCPBulgarellaMJohnsonKPSonsthagenSA 2009 Parallel evolution in the major haemoglobin genes of eight species of Andean waterfowl. Mol Ecol 18 3992 4005

43. GanforninaMDSanchezD 1999 Generation of evolutionary novelty by functional shift. Bioessays 21 432 439

44. TrueJRCarrollSB 2002 Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol 18 53 80

45. ChenLBDeVriesALChengCHC 1997 Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Nat Acad Sci USA 94 3817 3822

46. SutherlandTDYoungJHWeismanSHayashiCYMerrittDJ 2010 Insect Silk: One Name, Many Materials. Annu Rev Entomol 55 171 188

47. HoffmannFGOpazoJCStorzJF 2010 Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates. Proc Nat Acad Sci USA 107 14274

48. RosinFMKramerEM 2010 Old dogs, new tricks: Regulatory evolution in conserved genetic modules leads to novel morphologies in plants. Dev Biol 332 25 35

49. TangSKishoreVKKnappSJ 2003 PCR-multiplexes for a genome-wide framework of simple sequence repeat marker loci in cultivated sunflower. Theor Appl Genet 107 6 19

50. ChapmanMAPashleyCHWenzlerJHvalaJTangS 2008 A genomic scan for selection reveals candidates for genes involved in the evolution of cultivated sunflower (Helianthus annuus). Plant Cell 20 2931 2945

51. MandelJDechaineJMarekLBurkeJ 2011 Genetic diversity and population structure in cultivated sunflower and a comparison to its wild progenitor, Helianthus annuus L. Theor Appl Genet 123 693 704

52. PfafflMW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 2002 2007

53. ThompsonJDHigginsDGGibsonTJ 1994 Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673 4680

54. GuindonSGascuelO 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704

55. RonquistFHuelsenbeckJP 2003 MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

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#