Differential selection on carotenoid biosynthesis genes as a function of gene position in the metabolic pathway: A study on the carrot and dicots

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Clotault, Jérémy ^a,b,c   Peltier, Didier ^a,b,c   Soufflet Freslon, Vanessa ^a,b,c   Briad, Mathilde ^a,b,c   Geoffriau, Emmanuel ^a,b,c  

^a UNIVERSITÉ D'ANGERS   (France)

^b AGROCAMPUS OUEST   (France)

^c Universite d'Angers   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENE HYDROXYLASE; CAROTENOID; CAROTENOID ISOMERASE; ISOMERASE; ISOPENTENYL DIPHOSPHATE; LYASE; LYCOPENE BETA CYCLASE; LYCOPENE EPSILON CYCLASE; OXIDOREDUCTASE; OXYGENASE; PHYTOENE SYNTHASE; UNCLASSIFIED DRUG; ZEAXANTHIN EPOXIDASE;

ARTICLE; CARROT; CHXE GENE; CRTISO GENE; EUDICOT; GENE FREQUENCY; GENE LOCATION; GENE TARGETING; GENETIC CONSERVATION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; IPI GENE; LYCB GENE; LYCE GENE; NONHUMAN; PDS GENE; PHYLOGENY; PLANT BREEDING; PLANT GENE; PLANT METABOLISM; PLANT ROOT; POPULATION GENETICS; SPECIES CULTIVATION; TAXONOMY; ZEP GENE;

ARABIDOPSIS PROTEINS; BAYES THEOREM; CAROTENOIDS; CIS-TRANS-ISOMERASES; DAUCUS CAROTA; EVOLUTION, MOLECULAR; GENES, PLANT; GENETICS, POPULATION; GEOGRAPHY; MODELS, BIOLOGICAL; MODELS, GENETIC; NUCLEOTIDES; PHYLOGENY; PLANT PHYSIOLOGICAL PHENOMENA; PLANT ROOTS; POLYMORPHISM, GENETIC; PRINCIPAL COMPONENT ANALYSIS;

EID: 84862496070     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038724     Document Type: Article

References (65)

1. Cork JM, Purugganan MD, (2004) The evolution of molecular genetic pathways and networks. BioEssays 26: 479-484.
2. Wright KM, Rausher MD, (2010) The evolution of control and distribution of adaptive mutations in a metabolic pathway. Genetics 184: 483-502.
3. Flowers JM, Sezgin E, Kumagai S, Duvernell DD, Matzkin LM, et al. (2007) Adaptive evolution of metabolic pathways in Drosophila. Mol Biol Evol 24: 1347-1354.
4. Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES, (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci U S A 99: 12959-12962.
5. Ramsay H, Rieseberg LH, Ritland K, (2009) The correlation of evolutionary rate with pathway position in plant terpenoid biosynthesis. Mol Biol Evol 26: 1045-1053.
6. Rausher MD, Miller RE, Tiffin P, (1999) Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. Mol Biol Evol 16: 266-274.
7. Lu Y, Rausher MD, (2003) Evolutionary rate variation in anthocyanin pathway genes. Mol Biol Evol 20: 1844-1853.
8. Rausher MD, Lu Y, Meyer K, (2008) Variation in constraint versus positive selection as an explanation for evolutionary rate variation among anthocyanin genes. J Mol Evol 67: 137-144.
9. Ramos-Onsins SE, Puerma E, Balana-Alcaide D, Salguero D, Aguade M, (2008) Multilocus analysis of variation using a large empirical data set: phenylpropanoid pathway genes in Arabidopsis thaliana. Mol Ecol 17: 1211-1223.
10. Yang Y-hua, Zhang F-min, Ge S, (2009) Evolutionary rate patterns of the gibberellin pathway genes. BMC Evol Biol 9: 206.
11. Yu G, Olsen KM, Schaal BA, (2011) Molecular evolution of the endosperm starch synthesis pathway genes in rice (Oryza sativa L.) and its wild ancestor, O. rufipogon L. Mol Biol Evol 28: 659-671.
12. Bouvier F, Rahier A, Camara B, (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog Lipid Res 44: 357-429.
13. Bartley GE, Scolnik PA, (1995) Plant Carotenoids: Pigments for Photoprotection, Visual Attraction, and Human Health. Plant Cell 7: 1027-1038.
14. Livingstone K, Anderson S, (2009) Patterns of variation in the evolution of carotenoid biosynthetic pathway enzymes of higher plants. J Hered 100: 754-761.
15. Fu Z, Yan J, Zheng Y, Warburton M, Crouch J, et al. (2010) Nucleotide diversity and molecular evolution of the PSY1 gene in Zea mays compared to some other grass species. Theor Appl Genet 120: 709-720.
16. Palaisa KA, Morgante M, Williams M, Rafalski A, (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15: 1795-1806.
17. Nicolle C, Simon G, Rock E, Amouroux P, Remesy C, (2004) Genetic variability influences carotenoid, vitamin, phenolic, and mineral content in white, yellow, purple, orange, and dark-orange carrot cultivars. J Am Soc Hortic Sci 129: 523-529.
18. Surles RL, Weng N, Simon PW, Tanumihardjo SA, (2004) Carotenoid profiles and consumer sensory evaluation of specialty carrots (Daucus carota, L.) of various colors. J Agric Food Chem 52: 3417-3421.
19. Banga O, (1957) Origin of the European cultivated carrot. Euphytica 6: 54-63.
20. Banga O, (1963) Main types of the western carotene carrot and their origin. Zwolle: W.E.J. Tjeenk Willink. 153 p.
21. Mackevic VI, (1929) The carrot of Afghanistan. Bulletin of Applied Botany, Genetics and Plant Breeding 20: 517-562.
22. Laufer B, (1919) The carrot. In: Sino-Iranica: Chinese contributions to the History of civilization in Ancient Iran with special reference to the History of cultivated plants and products. Chicago: Field Museum of Natural History, Vol. 15: 451-454.
23. Shinohara S, (1984) Introduction and variety development in Japan. In: Vegetable seed production technology of Japan elucidated with respective variety development histories, particulars. Tokyo: Shinohara's Authorized Agricultural Consulting Engineer Office 4-7-7, Vol. 1: 273-282.
24. Just BJ, Santos CAF, Fonseca MEN, Boiteux LS, Oloizia BB, et al. (2007) Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping. Theor Appl Genet 114: 693-704.
25. Wright SI, Charlesworth B, (2004) The HKA test revisited a maximum-likelihood-ratio test of the standard neutral model. Genetics 168: 1071-1076.
26. Kreitman M, (2000) Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet 1: 539-559.
27. Barreiro LB, Laval G, Quach H, Patin E, Quintana-Murci L, (2008) Natural selection has driven population differentiation in modern humans. Nat Genet 40: 340-345.
28. Yu H-S, Shen Y-H, Yuan G-X, Hu Y-G, Xu H-E, et al. (2011) Evidence of selection at melanin synthesis pathway loci during silkworm domestication. Mol Biol Evol 28: 1785-1799.
29. Howitt CA, Pogson BJ, (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant, Cell & Environment 29: 435-445.
30. Ma Y-Z, Holt NE, Li X-P, Niyogi KK, Fleming GR, (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci U S A 100: 4377-4382.
31. Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J, (2006) A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18: 1947-1960.
32. Maass D, Arango J, Wust F, Beyer P, Welsch R, (2009) Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS ONE 4: e6373.
33. Just BJ, Santos CAF, Yandell BS, Simon PW, (2009) Major QTL for carrot color are positionally associated with carotenoid biosynthetic genes and interact epistatically in a domesticated × wild carrot cross. Theor Appl Genet 119: 1155-1169.
34. Clotault J, Geoffriau E, Lionneton E, Briard M, Peltier D, (2010) Carotenoid biosynthesis genes provide evidence of geographical subdivision and extensive linkage disequilibrium in the carrot. Theor Appl Genet 121: 659-667.
35. Charlesworth D, (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2: e64.
36. Lu S, Li L, (2008) Carotenoid metabolism: Biosynthesis, regulation, and beyond. J Integr Plant Biol 50: 778-785.
37. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, et al. (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333.
38. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389.
39. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R, (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
40. Watterson GA, (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7: 256-276.
41. Nei M, (1987) Molecular Evolutionary Genetics. New York: Columbia University Press. 512 p.
42. Nordborg M, Innan H, (2003) The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163: 1201-1213.
43. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, et al. (2005) The effects of artificial selection on the maize genome. Science 308: 1310-1314.
44. De Mita S, Ronfort J, McKhann HI, Poncet C, El Malki R, et al. (2007) Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in Nod factor signaling in Medicago truncatula. Genetics 177: 2123-2133.
45. Beaumont MA, Zhang W, Balding DJ, (2002) Approximate Bayesian Computation in population genetics. Genetics 162: 2025-2035.
46. Jukes TH, Cantor CR, (1969) Evolution of protein molecules. In: Munro HN, editors. 3: 21-132 editor. Mammalian protein metabolism. New York: Academic Press, Vol.
47. Cornuet J-M, Ravignie V, Estoup A, (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11: 401.
48. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution pp. 1358-1370.
49. Chakraborty R, Jin L, (1993) A unified approach to study hypervariable polymorphisms: statistical considerations of determining relatedness and population distances. In: Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ, editors. 67: 153-175 editors. DNA fingerprinting: state of the science. Basel: Birkhäuser Verlag, Vol.
50. Hudson RR, Slatkin M, Maddison WP, (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
51. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
52. Zeng K, Fu Y-X, Shi S, Wu C-I, (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439.
53. Clotault J, Thuillet A-C, Buiron M, De Mita S, Couderc M, et al. (2012) Evolutionary history of pearl millet (Pennisetum glaucum [L.] R. Br.) and selection on flowering genes since its domestication. Mol Biol Evol 29: 1199-1212.
54. Pavlidis P, Laurent S, Stephan W, (2010) msABC: a modification of Hudson's ms to facilitate multi-locus ABC analysis. Mol Ecol Resour 10: 723-727.
55. Baudry E, Depaulis F, (2003) Effect of misoriented sites on neutrality tests with outgroup. Genetics 165: 1619-1622.
56. Kronholm I, Loudet O, de Meaux J, (2010) Influence of mutation rate on estimators of genetic differentiation- lessons from Arabidopsis thaliana. BMC Genet 11: 33.
57. R Development Core Team (2009) R: A language and environment for statistical computing.
58. Hudson RR, Kreitman M, Aguade M, (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
59. Li WH, Wu CI, Luo CC, (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2: 150-174.
60. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
61. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
62. Thompson JD, Higgins DG, Gibson TJ, (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.
63. Emanuelsson O, Nielsen H, Von Heijne G, (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984.
64. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731-2739.
65. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.