Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family

Molecular Biology and Evolution

Volumn 25, Issue 7, 2008, Pages 1260-1273

  Chapman, Mark A ^a   Leebens Mack, James H ^a   Burke, John M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

CYCLOIDEA; Floral development; Helianthus; Sunflower; TEOSINTE BRANCHED1; Transcription factors

Indexed keywords

ARTICLE; CONTROLLED STUDY; CYC LIKE GENE; GENE; GENE AMPLIFICATION; GENE DUPLICATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYPLOIDY; QUANTITATIVE TRAIT LOCUS; SUNFLOWER;

AMINO ACID SEQUENCE; CHROMOSOME MAPPING; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENES, PLANT; HELIANTHUS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PLANT PROTEINS; SELECTION (GENETICS); SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; VARIATION (GENETICS);

ANTIRRHINUM; ASTERACEAE; HELIANTHUS; HELIANTHUS ANNUUS; ZEA MAYS;

EID: 45849117530     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn001     Document Type: Article

References (88)

1. Abbott RJ, James JK, Milne RI, Gillies ACM. 2003. Plant introductions, hybridization and gene flow. Philos Trans R Soc Lond B Biol Sci. 358:1123-1132.
2. Aguilar-Martinez JA, Poza-Carrión C, Cubas P. 2007. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell. 19:458-472.
3. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Andersson S. 2001. The genetic basis of floral variation in Senecio jacobaea (Asteraceae). J Hered. 92:409-414.
5. Baldwin BG, Wessa BL, Panero JL. 2002. Nuclear rDNA evidence for major lineages of helenioid Heliantheae (Compositae). Syst Bot. 27:161-198.
6. Barkman TJ, Martins TR, Sutton E, Stout JT. 2007. Positive selection for single amino acid change promotes substrate discrimination of a plant volatile-producing enzyme. Mol Biol Evol. 24:1320-1329.
7. Burke JM, Lai Z, Salmaso M, Nakazato T, Tang S, Heesacker A, Knapp SJ, Rieseberg LH. 2004. Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics. 167:449-457.
8. Burke JM, Tang S, Knapp SJ, Rieseberg LH. 2002. Genetic analysis of sunflower domestication. Genetics. 161:1257-1267.
9. Carroll SB. 2000. Endless forms: the evolution of gene regulation and morphological diversity. Cell. 101:577-580.
10. Chapman MA. 2004. The taxonomy of Senecio sect. Senecio: hybridisation and speciation. St Andrews (UK): University of St Andrews.
11. Chung BYW, Simons C, Firth AE, Brown CM, Hellens RP. 2006. Effect of 5′ UTR introns on gene expression in Arabidopsis thaliana. BMC Genomics. 7:120.
12. Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB. 2003. A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae. Plant Physiol. 131:1042-1053.
13. Citerne HL, Möller M, Cronk QCB. 2000. Diversity of cycloidea-like genes in Gesneriaceae in relation to floral symmetry. Ann Bot (Lond). 86:167-176.
14. Cubas P. 2002. Role of TCP genes in the evolution of key morphological characters in Angiosperms. In: Cronk QCB, Bateman RM, Hawkins JA, editors. Developmental genetics and plant evolution. London: Taylor and Francis Ltd. p. 247-266.
15. Cubas P, Lauter N, Doebley J, Coen ES. 1999. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18:215-222.
16. Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 401:157-161.
17. Damerval C, Le Guilloux M, Jager M, Charon C. 2007. Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. Plant Physiol. 143: 759-772.
18. Doebley J. 1993. Genetics, development and plant evolution. Curr Opin Genet Dev. 3:865-872.
19. Doebley J, Lukens L. 1998. Transcriptional regulators and the evolution of plant form. Plant Cell. 10:1075-1082.
20. Doebley J, Stec A, Hubbard L. 1997. The evolution of apical dominance in maize. Nature. 386:485-488.
21. Donoghue MJ, Ree RH, Baum DA. 1998. Phylogeny and evolution of flower symmetry in the Asteridae. Trends Plant Sci. 3:311-317.
22. Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA. 2004. Genetic control of branching in foxtail millet. Proc Natl Acad Sci USA. 101:9045-9050.
23. Duarte JM, Cui LY, Wall PK, Zhang Q, Zhang XH, Leebens-Mack J, Ma H, Altman N, dePamphilis CW. 2006. Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol. 23:469-478.
24. Feng XZ, Zhao Z, Tian ZX, et al. 2006. Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA. 103:4970-4975.
25. Ford VS, Gottlieb LD. 1990. Genetic studies of floral evolution in Layia. Heredity. 64:29-44.
26. Fukuda T, Yokoyama J, Maki M. 2003. Molecular evolution of cycloidea-like genes in Fabaceae. J Mol Evol. 57:588-597.
27. Funk VA, Bayer RJ, Keeley S, et al. 2005. Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biol Skr. 55:343-374.
28. Gentzbittel L, Mestries E, Mouzeyar S, Mazeryat F, Badaoui S, Vear F, Tourvieille de la Brouhe D, Nicolas P. 1999. A composite map of expressed sequences and phenotypic traits of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet. 99:218-234.
29. Gillies ACM, Cubas P, Coen ES, Abbott RJ. 2002. Making rays in the Asteraceae: genetics and evolution of variation for radiate versus discoid flower heads. In: Cronk QCB, Bateman RM, Hawkins JA, editors. Developmental genetics and plant evolution. London: Taylor & Francis. p. 237-246.
30. Giurfa M, Dafni A, Neal PR. 1999. Floral symmetry and its role in plant-pollinator systems. Int J Plant Sci. 160:S41-S50.
31. Guillet-Claude C, Isabel N, Pelgas B, Bousquet J. 2004. The evolutionary implications of knox-I gene duplications in conifers: correlated evidence from phylogeny, gene mapping, and analysis of functional divergence. Mol Biol Evol. 21:2232-2245.
32. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
33. Guindon S, Rodrigo AG, Dyer KA, Huelsenbeck JP. 2004. Modeling the site-specific variation of selection patterns along lineages. Proc Natl Acad Sci USA. 101:12957-12962.
34. Hasegawa M, Kishino H, Yano T. 1985. Dating of the humanape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22:160-174.
35. He LM, Du CG, Covaleda L, Xu ZY, Robinson AF, Yu JZ, Kohel RJ, Zhang HB. 2004. Cloning, characterization, and evolution of the NBS-LRR-encoding resistance gene analogue family in polyploid cotton (Gossypium hirsutum L.). Mol Plant Microbe. 17:1234-1241.
36. Hileman LC, Baum DA. 2003. Why do paralogs persist? Molecular evolution of CYCLOIDEA and related floral symmetry genes in Antirrhineae (Veronicaceae). Mol Biol Evol. 20:591-600.
37. Hileman LC, Kramer EM, Baum DA. 2003. Differential regulation of symmetry genes and the evolution of floral morphologies. Proc Natl Acad Sci USA. 100:12814-12819.
38. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP. 2000. A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol. 123:1313-1323.
39. Hong X, Scofield DG, Lynch M. 2006. Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol. 23:2392-2404.
40. Howarth DG, Donoghue MJ. 2005. Duplications in CYC-like genes from dipsacales correlate with floral form. Int J Plant Sci. 166:357-370.
41. Howarth DG, Donoghue MJ. 2006. Phylogenetic analysis of the "ECE" (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA. 103:9101-9106.
42. Hughes TA. 2006. Regulation of gene expression by alternative untranslated regions. Trends Genet. 22:119-122.
43. Kanazin V, Marek LF, Shoemaker RC. 1996. Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA. 93:11746-11750.
44. Kim KJ, Choi KS, Jansen RK. 2005. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol. 22:1783-1792.
45. Kim MJ, Kim H, Shin JS, Chung CH, Ohlrogge JB, Suh MC. 2006. Seed-specific expression of sesame microsomal oleic acid desaturase is controlled by combinatorial properties between negative cis-regulatory elements in the SeFAD2 promoter and enhancers in the 5′-UTR intron. Mol Genet Genomics. 276:351-368.
46. Kolsch A, Gleissberg S. 2006. Diversification of CYCLOIDEA-like TCP genes in the basal eudicot families Fumariaceae and Papaveraceae s.str. Plant Biol. 8:680-687.
47. Kosambi DD. 1944. The estimation of map distances from recombination values. Ann Eugen. 12:172-175.
48. Kosugi S, Ohashi Y. 1997. PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell. 9:1607-1619.
49. Kosugi S, Ohashi Y. 2002. DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J. 30:337-348.
50. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1:174-181.
51. Lawton-Rauh AL, Alvarez-Buylla ER, Purugganan MD. 2000. Molecular evolution of flower development. Trends Ecol Evol. 15:144-149.
52. Lincoln S, Daly M, Lander E. 1992. Constructing genetic maps with MAPMAKER/EXP 3.0. 3rd ed. Cambridge (MA): Whitehead Institute.
53. Linhart C, Shamir R. 2005. The degenerate primer design problem: theory and applications. J Comput Biol. 12:431-456.
54. Lukens L, Doebley J. 2001. Molecular evolution of the teosinte branched gene among maize and related grasses. Mol Biol Evol. 18:627-638.
55. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen ES. 1999. Control of organ asymmetry in flowers of Antirrhinum. Cell. 99:367-376.
56. Luo D, Carpenter R, Vincent C, Copsey L, Coen E. 1996. Origin of floral asymmetry in Antirrhinum. Nature. 383:794-799.
57. Lynch M, Force AG. 2000. The origin of interspecific genomic incompatibility via gene duplication. Am Nat. 156:590-605.
58. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y. 2005. Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA. 102:5454-5459.
59. Menossi M, Rabaneda F, Puigdomenech P, Martinez-Izquierdo JA. 2003. Analysis of regulatory elements of the promoter and the 3′ untranslated region of the maize Hrgp gene coding for a cell wall protein. Plant Cell Rep. 21:916-923.
60. Michelmore RW, Meyers BC. 1998. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:1113-1130.
61. Moore RC, Purugganan MD. 2005. The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol. 8:122-128.
62. Morello L, Bardini M, Cricri M, Sala F, Breviario D. 2006. Functional analysis of DNA sequences controlling the expression of the rice OsCDPK2 gene. Planta. 223:479-491.
63. Morello L, Bardini M, Sala F, Breviario D. 2002. A long leader intron of the Ostub16 rice beta-tubulin gene is required for high-level gene expression and can autonomously promote transcription both in vivo and in vitro. Plant J. 29:33-44.
64. Ohno S. 1970. Evolution by gene duplication. New York: Springer.
65. Purugganan MD. 1998. The molecular evolution of development. Bioessays. 20:700-711.
66. Putt ED. 1964. Recessive branching in sunflowers. Crop Sci. 4:444-445.
67. Ree RH, Citerne HL, Lavin M, Cronk QCB. 2004. Heterogeneous selection on LEGCYC paralogs in relation to flower morphology and the phylogeny of Lupinus (Leguminosae). Mol Biol Evol. 21:321-331.
68. Reeves PA, Olmstead RG. 2003. Evolution of the TCP gene family in Asteridae: cladistic and network approaches to understanding regulatory gene family diversification and its impact on morphological evolution. Mol Biol Evol. 20:1997-2009.
69. Sanderson MJ. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol. 19:101-109.
70. Sanderson MJ. 2003. R8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 19:301-302.
71. Scott MP, Weiner AJ. 1984. Structural relationships among genes that control development-sequence homology between the Antennapedia, Ultrabithorax, and Fushi Tarazu loci of Drosophila. Proc Natl Acad Sci USA. 81:4115-4119.
72. Self SG, Liang KY. 1987. Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under non-standard conditions. J Am Stat Assoc. 82:605-610.
73. Smith JF, Hileman LC, Powell MP, Baum DA. 2004. Evolution of GCYC, a Gesneriaceae homolog of CYCLOIDEA, within Gesnerioideae (Gesneriaceae). Mol Phylogenet Evol. 31:765-779.
74. Soranzo N, Gorla MS, Mizzi L, De Toma G, Frova C. 2004. Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics. 271:511-521.
75. Sossey-Alaoui K, Serieys H, Tersac M, Lambert P, Schilling E, Griveau Y, Kaan F, Berville A. 1998. Evidence for several genomes in Helianthus. Theor Appl Genet. 97:422-430.
76. Stebbins GL. 1974. Flowering plants: evolution above the species level. Cambridge: Harvard University Press.
77. Stevens PF. 2006. Angiosperm Phylogeny Website, Version 7 [Internet]. [cited 2006 May] http://www.mobot.org/MOBOT/research/APweb
78. Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C. 2003. The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 33:513-520.
79. Tang S, Yu JK, Slabaugh MB, Shintani DK, Knapp SJ. 2002. Simple sequence repeat map of the sunflower genome. Theor Appl Genet. 105:1124-1136.
80. Tang SX, Leon A, Bridges WC, Knapp SJ. 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.
81. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H. 2000. A short history of MADS-box genes in plants. Plant Mol Biol. 42:115-149.
82. Trow AH. 1912. On the inheritance of certain characters in the common groundsel-Senecio vulgaris-and its segregates. J Genet. 2:239-276.
83. Wikström N, Savolainen V, Chase MW. 2001. Evolution of the angiosperms: calibrating the family tree. Proc R Soc Lond B Biol Sci. 268:2211-2220.
84. Wilkie GS, Dickson KS, Gray NK. 2003. Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci. 28:182-188.
85. Wills DM, Burke JM. 2007. QTL analysis of the early domestication of sunflower. Genetics. doi: 10.1534/genetics.107.075333.
86. Wong WSW, Yang ZH, Goldman N, Nielsen R. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics. 168:1041-1051.
87. Yang Z. 2000. Phylogenetic analysis by maximum likelihood (PAML). London: University College.
88. Yanofsky MF. 1995. Floral meristems to floral organs - genes controlling early events in Arabidopsis flower development. Annu Rev Plant Physiol. 46:167-188.