Genetic basis of stage-specific melanism: A putative role for a cysteine sulfinic acid decarboxylase in insect pigmentation

Heredity

Volumn 108, Issue 6, 2012, Pages 594-601

  Saenko, S V ^a,c   Jeronimo M A ^b   Beldade, P ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

black; evo devo; lepidoptera; melanogenesis; pigmentation; PLP dependent enzyme

Indexed keywords

CARBOXYLYASE; MELANIN; SULFOALANINE DECARBOXYLASE;

ADAPTATION; BIOLOGICAL DEVELOPMENT; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; HERITABILITY; MELANISM; MORPHOLOGY; MOTH; MUTATION; NATURAL SELECTION;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BUTTERFLY; ENZYMOLOGY; EVOLUTION; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PIGMENTATION;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; BUTTERFLIES; CARBOXY-LYASES; MELANINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; PIGMENTATION; SELECTION, GENETIC;

ANIMALIA; BICYCLUS ANYNANA; BISTON BETULARIA; HEXAPODA; LEPIDOPTERA; PAPILIONOIDEA; THEOBROMA CACAO;

EID: 84861340556     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2011.127     Document Type: Article

References (57)

1. Allen CE, Beldade P, Zwaan BJ, Brakefield PM (2008). Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution. BMC Evol Biol 8: 94.
2. Arakane Y, Lomakin J, Beeman RW, Muthukrishnan S, Gehrke SH, Kanost MR et al. (2009). Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum. J Biol Chem 284: 16584-16594.
3. Bear A, Simons A, Westerman E, Monteiro A (2010). The genetic, morphological, and physiological characterization of a dark larval cuticle mutation in the butterfly, Bicyclus anynana. PLoS One 5: E11563.
4. Beldade P, Brakefield PM (2002). The genetics and evo-devo of butterfly wing patterns. Nat Rev Genet 3: 442-452.
5. Beldade P, Brakefield PM, Long AD (2005). Generating phenotypic variation: Prospects from ''evo-devo'' research on Bicyclus anynana wing patterns. Evol Dev 7: 101-107.
6. Beldade P, French V, Brakefield PM (2008). Developmental and genetic mechanisms for evolutionary diversification of serial repeats: Eyespot size in Bicyclus anynana butterflies. J Exp Zool B Mol Dev Evol 310: 191-201.
7. Beldade P, Koops K, Brakefield PM (2002). Developmental constraints versus flexibility in morphological evolution. Nature 416: 844-847.
8. Beldade P, Mateus ARA, Keller RA (2011). Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20: 1347-1363.
9. Beldade P, Rudd S, Gruber JD, Long AD (2006). A wing expressed sequence tag resource for Bicyclus anynana butterflies, an evo-devo model. BMC Genomics 7: 130.
10. Beldade P, Saenko SV, Pul N, Long AD (2009). A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome. PLoS Genet 5: E1000366.
11. Brakefield P, Beldade P, Zwaan BJ (2009). The African butterfly Bicyclus anynana: A model for evolutionary genetics and evolutionary developmental biology. In: Behringer RR, Johnson AD, Krumlauf RE (eds). Emerging Model Organisms: A Laboratory Manual. Cold Spring Harbor Laboratory Press Vol.1, Chapter 12.
12. Caro T (2005). The adaptive significance of coloration in mammals. BioScience 55: 125-136.
13. Christen P, Mehta PK (2001). From cofactor to enzymes. The molecular evolution of pyridoxal-5¢ a-phosphate-dependent enzymes. Chem Rec 1: 436-447.
14. Conceiç aã ao IC, Long AD, Gruber JD, Beldade P (2011). Genomic sequence around butterfly wing development genes: Annotation and comparative analysis. PLoS One 6: E23778.
15. Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O'Brien SJ (2003). Molecular genetics and evolution of melanism in the cat family. Curr Biol 13: 448-453.
16. Freeman AM, Mole BM, Silversmith RE, Bourret RB (2011). Action at a distance: Amino acid substitutions that affect binding of the phosphorylated CheY response regulator and catalysis of dephosphorylation can be far from the CheZ phosphatase active site. J Bacteriol 193: 4709-4718.
17. Futahashi R, Banno Y, Fujiwara H (2010). Caterpillar color patterns are determined by a two-phase melanin gene prepatterning process: New evidence from tan and laccase2. Evol Dev 12: 157-167.
18. Futahashi R, Fujiwara H (2005). Melanin-synthesis enzymes coregulate stage-specific larval cuticular markings in the swallowtail butterfly, Papilio xuthus. Dev Genes Evol 215: 519-529.
19. Futahashi R, Sato J, Meng Y, Okamoto S, Daimon T, Yamamoto K et al. (2008). yellow and ebony are the responsible genes for the larval color mutants of the silkworm Bombyx mori. Genetics 180: 1995-2005.
20. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005). Change caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
21. Goulson D (1994). Determination of larval melanization in the moth, Mamestra brassicae, and the role of melanin in thermoregulation. Heredity 73: 471-479.
22. Gross JB, Borowsky R, Tabin CJ (2009). A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5: E1000326.
23. Guion-Rain MC, Portemer C, Chatagner F (1975). Rat liver cysteine sulfinate decarboxylase: Purification, new appraisal of the molecular weight and determination of catalytic properties. Biochim Biophys Acta 384: 265-276.
24. Haag ES, True JR (2001). From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology. Evolution 55: 1077-1084.
25. Hazel WN (2002). The environmental and genetic control of seasonal polyphenism in larval color and its adaptive significance in a swallowtail butterfly. Evolution 56: 342-348.
26. John RA (1995). Pyridoxal phosphate-dependent enzymes. Biochim Biophys Acta 1248: 81-96.
27. Jones M, Rakes L, Yochum M, Dunn G, Wurster S, Kinney K et al. (2007). The proximate control of pupal color in swallowtail butterflies: Implications for the evolution of environmentally cued pupal color in butterflies (Lepidoptera: Papilionidae). J Insect Physiol 53: 40-46.
28. Koch PB, Behnecke B, Weigmann-Lenz M, Ffrench-Constant RH (2000). Insect pigmentation: Activities of beta-alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus. Pigment Cell Res (Suppl)8: 54-58.
29. Kramer KJ, Morgan TD, Hopkins TL, Roseland CR, Aso Y, Beeman RW et al. (1984). Cateholamines and b-alanine in the red flour beetle, Tribolium castaneum - roles in cuticle sclerotization and melanization. Insect Biochem 14: 293-298.
30. Manceau M, Domingues VS, Mallarino R, Hoekstra HE (2011). The developmental role of Agouti in color pattern evolution. Science 331: 1062-1065.
31. Mills MG, Nuckels RJ, Parichy DM (2007). Deconstructing evolution of adult phenotypes: Genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes. Development 134: 1081-1090.
32. Mills MG, Patterson LB (2009). Not just black and white: Pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol 20: 72-81.
33. Mozzarelli A, Bettati S (2006). Exploring the pyridoxal 5¢ a-phosphate-dependent enzymes. Chem Rec 6: 275-287.
34. Nachman MW, Hoekstra HE, D'Agostino SL (2003). The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100: 5268-5273.
35. Noor MA, Parnell RS, Grant BS (2008). A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars. PLoS One 3: E3142.
36. Oliver JC, Robertson KA, Monteiro A (2009). Accommodating natural and sexual selection in butterfly wing pattern evolution. Proc Biol Sci 276: 2369-2375.
37. Percudani R, Peracchi A (2003). A genomic overview of pyridoxal-phosphate-dependent enzymes. EMBO reports 4: 850-854.
38. Phillips AM, Smart R, Strauss R, Brembs B, Kelly LE (2005). The Drosophila black enigma: The molecular and behavioural characterization of the black1 mutant allele. Gene 351: 131-142.
39. Pijpe J, Pul N, van Duijn S, Brakefield PM, Zwaan BJ (2011). Changed gene expression for candidate ageing genes in long-lived Bicyclus anynana butterflies. Exp Gerontol 46: 426-434.
40. Protas ME, Patel NH (2008). Evolution of coloration patterns. Annu Rev Cell Dev Biol 24: 425-446.
41. Protas ME, Trontelj P, Patel NH (2011). Genetic basis of eye and pigment loss in the cave crustacean, Asellus aquaticus. Proc Natl Acad Sci USA 108: 5702-5707.
42. Reed RD, Chen PH, Frederik Nijhout H (2007). Cryptic variation in butterfly eyespot development: The importance of sample size in gene expression studies. Evol Dev 9: 2-9.
43. Richardson G, Ding H, Rocheleau T, Mayhew G, Reddy E, Han Q et al. (2010). An examination of aspartate decarboxylase and glutamate decarboxylase activity in mosquitoes. Mol Biol Rep 37: 3199-3205.
44. Rosenblum EB, Rö ampler H, Schö aneberg T, Hoekstra HE (2010). Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci USA 107: 2113-2117.
45. Saenko SV, Brakefield PM, Beldade P (2010). Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty. BMC Biol 8: 111.
46. Saenko SV, French V, Brakefield PM, Beldade P (2008). Conserved developmental processes and the formation of evolutionary novelties: Examples from butterfly wings. Philos Trans R Soc Lond B Biol Sci 363: 1549-1555.
47. Saenko SV, Marialva MS, Beldade P (2011). Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2: 9.
48. Sato K, Matsunaga TM, Futahashi R, Kojima T, Mita K, Banno Y et al. (2008). Positional cloning of a Bombyx wingless locus flugellos (fl) reveals a crucial role for fringe that is specific for wing morphogenesis. Genetics 179: 875-885.
49. True JR (2003). Insect melanism: The molecules matter. Trends Ecol Evol 18: 640-647.
50. True JR, Yeh SD, Hovemann BT, Kemme T, Meinertzhagen IA, Edwards TN et al. (2005). Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet 1: E63.
51. van't Hof AE, Edmonds N, Dalí aková aM, Marec F, Saccheri IJ (2011). Industrial melanism in british peppered moths has a singular and recent mutational origin. Science 332: 958-960.
52. van't Hof AE, Saccheri I.J. 2010) Industrial melanism in the peppered moth is not associated with genetic variation in canonical melanisation gene candidates. PLoS One 5 e10889.
53. Weatherbee SD, Nijhout HF, Grunert LW, Halder G, Galant R, Selegue J et al. (1999). Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr Biol 9: 109-115.
54. Wittkopp PJ, Beldade P (2009). Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 20: 65-71.
55. Wittkopp PJ, Carroll SB, Kopp A (2003). Evolution in black and white: Genetic control of pigment patterns in Drosophila. Trends Genet 19: 495-504.
56. Wittkopp PJ, Vaccaro K, Carroll SB (2002). Evolution of yellow gene regulation and pigmentation in Drosophila. Curr Biol 12: 1547-1556.
57. Zhan S, Guo Q, Li M, Li M, Li J, Miao X et al. (2010). Disruption of an N-acetyltransferase gene in the silkworm reveals a novel role in pigmentation. Development 137: 4083-4090.