Molecular evolution of the Drosophila retinome: Exceptional gene gain in the higher diptera

Molecular Biology and Evolution

Volumn 26, Issue 6, 2009, Pages 1273-1287

  Bao, Riyue ^a   Friedrich, Markus ^a,b  

^a WAYNE STATE UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Eye development; Gene duplication; InaC; InaF; Intracellular subfunctionalization; Lazaro; Opsin; Phototransduction; Redundancy; Wunen

Indexed keywords

OPSIN;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENE CLUSTER; GENE DUPLICATION; GENE FUNCTION; GENE SEQUENCE; GENETIC DATABASE; GENETIC LINKAGE; MOLECULAR EVOLUTION; NONHUMAN; ORTHOLOGY; PHOTOTRANSDUCTION; PHYLOGENY; RETINA DEVELOPMENT; VISION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; COMPOUND EYE, ARTHROPOD; DATABASES, GENETIC; DIPTERA; DROSOPHILA; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; EYE PROTEINS; GENE DUPLICATION; GENE EXPRESSION; GENES, INSECT; GENOMICS; MODELS, STATISTICAL; MULTIGENE FAMILY; PHOTORECEPTOR CELLS, INVERTEBRATE; PHYLOGENY; ROD OPSINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; VISION, OCULAR;

ACTINIARIA; APIS MELLIFERA; DIPTERA; HEXAPODA; TRIBOLIUM CASTANEUM;

EID: 66249135996     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp039     Document Type: Article

References (117)

1. Adams MD, Celniker SE, Holt RA, et al. 2000. The genome sequence of Drosophila melanogaster. Science. 287:2185-2195.
2. Adamski FM, Zhu MY, Bahiraei F, Shieh BH. 1998. Interaction of eye protein kinase C and INAD in Drosophila. Localization of binding domains and electrophysiological characterization of a loss of association in transgenic flies. J Biol Chem. 273:17713-17719.
3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Ashburner M. 2007. The genomes of Diptera. In: Wiegmann BM, Yeates DK, editors. The evolutionary biology of flies. New York: Columbia University Press. p. 65-125.
5. Benzer S. 1967. Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci USA. 58:1112-1119.
6. Bessa J, Carmona L, Casares F. 2009. Zinc-finger paralogues tsh and tio are functionally equivalent during imaginal development in Drosophila and maintain their expression levels through auto-and cross-negative feedback loops. Dev Dyn. 238:19-28.
7. Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annu Rev Entomol. 46:471-510.
8. Brown S, Fellers J, Shippy T, Denell R, Stauber M, Schmidt-Ott U. 2001. A strategy for mapping bicoid on the phylogenetic tree. Curr Biol. 11:R43-R44.
9. Brown SJ, Denell RE, Beeman RW. 2003. Beetling around the genome. Genet Res. 82:155-161.
10. Byun-McKay SA, Geeta R. 2007. Protein subcellular relocalization: a new perspective on the origin of novel genes. Trends Ecol Evol. 22:338-344.
11. Cantera R, Luer K, Rusten TE, Barrio R, Kafatos FC, Technau GM. 2002. Mutations in spalt cause a severe but reversible neurodegenerative phenotype in the embryonic central nervous system of Drosophila melanogaster. Development. 129:5577-5586.
12. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552.
13. Chain FJ, Evans BJ. 2006. Multiple mechanisms promote the retained expression of gene duplicates in the tetraploid frog Xenopus laevis. PLoS Genet. 2:e56.
14. Cheng Y, Nash HA. 2007. Drosophila TRP channels require a protein with a distinctive motif encoded by the inaF locus. Proc Natl Acad Sci USA. 104:17730-17734.
15. Clark AG, Eisen MB, Smith DR, et al. (415 co-authors). 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 450:203-218.
16. Conant GC, Wolfe KH. 2008. Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet. 9:938-950.
17. Curtiss J, Burnett M, Mlodzik M. 2007. distal antenna and distal antenna-related function in the retinal determination network during eye development in Drosophila. Dev Biol. 306:685-702.
18. Dean EJ, Davis JC, Davis RW, Petrov DA. 2008. Pervasive and persistent redundancy among duplicated genes in yeast. PLoS Genet. 4:e1000113.
19. Dearden PK, Wilson MJ, Sablan L, et al. (16 co-authors). 2006. Patterns of conservation and change in honey bee developmental genes. Genome Res. 16:1376-1384.
20. Des Marais DL, Rausher MD. 2008. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature. 454:762-765.
21. Domingos PM, Brown S, Barrio R, Ratnakumar K, Frankfort BJ, Mardon G, Steller H, Mollereau B. 2004. Regulation of R7 and R8 differentiation by the spalt genes. Dev Biol. 273:121-133.
22. Domingos PM, Mlodzik M, Mendes CS, Brown S, Steller H, Mollereau B. 2004. Spalt transcription factors are required for R3/R4 specification and establishment of planar cell polarity in the Drosophila eye. Development. 131:5695-5702.
23. Dong PD, Todi SV, Eberl DF, Boekhoff-Falk G. 2003. Drosophila spalt/spalt-related mutants exhibit Townes-Brocks' syndrome phenotypes. Proc Natl Acad Sci USA. 100:10293-10298.
24. Donner AL, Maas RL. 2004. Conservation and non-conservation of genetic pathways in eye specification. Int J Dev Biol. 48:743-753.
25. Drysdale RA, Crosby MA. 2005. FlyBase: genes and gene models. Nucleic Acids Res. 33:D390-D395.
26. Elstob PR, Brodu V, Gould AP. 2001. spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development. 128:723-732.
27. Emerald BS, Curtiss J, Mlodzik M, Cohen SM. 2003. Distal antenna and distal antenna related encode nuclear proteins containing pipsqueak motifs involved in antenna development in Drosophila. Development. 130:1171-1180.
28. Fares MA, Byrne KP, Wolfe KH. 2006. Rate asymmetry after genome duplication causes substantial long-branch attraction artifacts in the phylogeny of Saccharomyces species. Mol Biol Evol. 23:245-253.
29. Felsenstein J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool. 19:401-410.
30. Felsenstein J. 1986. Jackknife, bootstrap and other resampling methods in regression-analysis - discussion. Ann Stat. 14:1304-1305.
31. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 151:1531-1545.
32. Friedrich M. 2008. Opsins and cell fate in the Drosophila Bolwig organ: tricky lessons in homology inference. Bioessays. 30:980-993.
33. Garcia-Murillas I, Pettitt T, Macdonald E, Okkenhaug H, Georgiev P, Trivedi D, Hassan B, Wakelam M, Raghu P. 2006. lazaro encodes a lipid phosphate phosphohydrolase that regulates phosphatidylinositol turnover during Drosophila phototransduction. Neuron. 49:533-546.
34. Gehring WJ, Ikeo K. 1999. Pax6: mastering eye morphogenesis and eye evolution. Trends Genet. 15:371-377.
35. Goodman M, Czelusniak J, Moore G, Romero-Herrera A, Matsuda G. 1979. Fitting the gene lineage into its species lineage, a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool. 28:132-163.
36. Gu Y, Oberwinkler J, Postma M, Hardie RC. 2005. Mechanisms of light adaptation in Drosophila photoreceptors. Curr Biol. 15:1228-1234.
37. Gu ZL, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH. 2003. Role of duplicate genes in genetic robustness against null mutations. Nature. 421:63-66.
38. Hahn MW. 2007. Bias in phylogenetic tree reconciliation methods: implications for vertebrate genome evolution. Genome Biol. 8:R141.
39. Hahn MW, Han MV, Han SG. 2007. Gene family evolution across 12 Drosophila genomes. PLoS Genet. 3:e197.
40. Hanyu-Nakamura K, Kobayashi S, Nakamura A. 2004. Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development. 131:4545-4553.
41. Hardie RC, Raghu P. 2001. Visual transduction in Drosophila. Nature. 413:186-193.
42. Heger A, Ponting CP. 2008. OPTIC: orthologous and paralogous transcripts in clades. Nucleic Acids Res. 36:D267-270.
43. Heger A, Ponting CP. 2007. Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. Genome Res. 17:1837-1849.
44. Hendy MD, Penny D. 1989. A framework for the quantitative study of phylogenetic trees. Syst Zool. 38:297-309.
45. Higashijima S, Kojima T, Michiue T, Ishimaru S, Emori Y, Saigo K. 1992. Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev. 6:50-60.
46. Holt RA, Subramanian GM, Halpern A, et al. (123 co-authors). 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 298:129-149.
47. Honeybee Genome Sequencing Consortium et al. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 443:931-949.
48. Hotta Y, Benzer S. 1970. Genetic dissection of the Drosophila nervous system by means of mosaics. Proc Natl Acad Sci USA. 67:1156-1163.
49. Hughes AL. 2005. Gene duplication and the origin of novel proteins. Proc Natl Acad Sci USA. 102:8791-8792.
50. Jackowska M, Bao R, Liu Z, McDonald EC, Cook TA, Friedrich M. 2007. Genomic and gene regulatory signatures of cryptozoic adaptation: loss of blue sensitive photoreceptors through expansion of long wavelengthopsin expression in the red flour beetle Tribolium castaneum. Front Zool. 4:24.
51. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
52. Kafri R, Levy M, Pilpel Y. 2006. The regulatory utilization of genetic redundancy through responsive backup circuits. Proc Natl Acad Sci USA. 103:11653-11658.
53. Kaminker JS, Singh R, Lebestky T, Yan H, Banerjee U. 2001. Redundant function of Runt Domain binding partners, Big brother and Brother, during Drosophila development. Development. 128:2639-2648.
54. Karolchik D, Kuhn RM, Baertsch R, et al. (25 co-authors). 2008. The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res. 36:D773-779.
55. Kenyon KL, Li DJ, Clouser C, Tran S, Pignoni F. 2005. Fly SIX-type homeodomain proteins Sine oculis and Optix partner with different cofactors during eye development. Dev Dyn. 234:497-504.
56. Kojima T, Sato M, Saigo K. 2000. Formation and specification of distal leg segments in Drosophila by dual Bar homeobox genes, BarH1 and BarH2. Development. 127:769-778.
57. Kumar R, Shieh BH. 2001. The second PDZ domain of INAD is a type I domain involved in binding to eye protein kinase C. Mutational analysis and naturally occurring variants. J Biol Chem. 276:24971-24977.
58. Kumar S. 1996. PHYLTEST: phylogenetic hypothesis testing software. Version 2.0. University Park, Pennsylvania: Pennsylvania State University.
59. Kumar SK, Tamura K, Nei M. 1993. MEGA: Molecular Evolutionary Genetics Analysis. University Park, Pennsylvania: Pennsylvania State University.
60. Kwon Y, Montell C. 2006. Dependence on the Lazaro phosphatidic acid phosphatase for the maximum light response. Curr Biol. 16:723-729.
61. Laughlin SB, Weckstrom M. 1993. Fast and slow photo-receptors - a comparative-study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol A. 172:593-609.
62. Laugier E, Yang Z, Fasano L, Kerridge S, Vola C. 2005. A critical role of teashirt for patterning the ventral epidermis is masked by ectopic expression of tiptop, a paralog of teashirt in Drosophila. Dev Biol. 283:446-458.
63. Li C, Geng C, Leung HT, Hong YS, Strong LL, Schneuwly S, Pak WL. 1999. INAF, a protein required for transient receptor potential Ca(2+) channel function. Proc Natl Acad Sci USA. 96:13474-13479.
64. Lynch M. 2007. The origins of genome architecture. Sunderland (MA): Sinauer.
65. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science. 290:1151-1155.
66. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics. 154:459-473.
67. Maslov S, Sneppen K, Eriksen KA, Yan KK. 2004. Upstream plasticity and downstream robustness in evolution of molecular networks. BMC Evol Biol. 4:9.
68. Matsumoto H, Kurien BT, Takagi Y, et al. (12 co-authors). 1994. Phosrestin-i undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein-kinase in Drosophila photoreceptors. Neuron. 12:997-1010.
69. Mishra P, Socolich M, Wall MA, Graves J, Wang Z, Ranganathan R. 2007. Dynamic scaffolding in a G protein-coupled signaling system. Cell. 131:80-92.
70. Mita K, Kasahara M, Sasaki S, et al. (21 co-authors). 2004. The genome sequence of silkworm, Bombyx mori. DNA Res. 11:27-35.
71. Mollereau B, Dominguez M, Webel R, Colley NJ, Keung B, de Celis JF, Desplan C. 2001. Two-step process for photoreceptor formation in Drosophila. Nature. 412:911-913.
72. Morante J, Desplan C, Celik A. 2007. Generating patterned arrays of photoreceptors. Curr Opin Genet Dev. 17:314-319.
73. Moses K. 2002. Drosophila visual system development. Berlin (Germany): Springer Verlag.
74. Musso G, Costanzo M, Huangfu M, et al. (11 co-authors). 2008. The extensive and condition-dependent nature of epistasis among whole-genome duplicates in yeast. Genome Res. 18:1092-1099.
75. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol. 302:205-217.
76. Pak WL, Grossfield J, White NV. 1969. Nonphototactic mutants in a study of vision of Drosophila. Nature. 222:351-354.
77. Pappu KS, Mardon G. 2004. Genetic control of retinal specification and determination in Drosophila. Int J Dev Biol. 48:913-924.
78. Pasek S, Risler JL, Brezellec P. 2006. The role of domain redundancy in genetic robustness against null mutations. J Mol Biol. 362:184-191.
79. Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL. 2000. Evidence for DNA loss as a determinant of genome size. Science. 287:1060-1062.
80. Popescu DC, Ham AJ, Shieh BH. 2006. Scaffolding protein INAD regulates deactivation of vision by promoting phosphorylation of transient receptor potential by eye protein kinase C in Drosophila. J Neurosci. 26:8570-8577.
81. Pyne S, Kong KC, Darroch PI. 2004. Lysophosphatidic acid and sphingosine 1-phosphate biology: the role of lipid phosphate phosphatases. Semin Cell Dev Biol. 15:491-501.
82. Quiring R, Walldorf U, Kloter U, Gehring WJ. 1994. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science. 265:785-789.
83. Rambaut A, Grassly N. 1997. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci. 13:235-238.
84. Ready DF. 2002. Drosophila compound eye morphogenesis: blind mechanical engineers? In: Moses K, editor. Results and problems in cell differentiation. Berlin (Germany): Springer Verlag.
85. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
86. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406-425.
87. Sano H, Renault AD, Lehmann R. 2005. Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J Cell Biol. 171:675-683.
88. Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ. 2006. Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res. 16:1334-1338.
89. Schaeffer E, Smith D, Mardon G, Quinn W, Zuker C. 1989. Isolation and characterization of two new Drosophila protein kinase C genes, including one specifically expressed in photoreceptor cells. Cell. 57:403-412.
90. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics. 18:502-504.
91. Seimiya M, Gehring WJ. 2000. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless- independent mechanism. Development. 127:1879-1886.
92. Sheng G, Thouvenot E, Schmucker D, Wilson DS, Desplan C. 1997. Direct regulation of rhodopsin 1 by Pax-6/ eyeless in Drosophila: evidence for a conserved function in photoreceptors. Genes Dev. 11:1122-1131.
93. Shieh BH, Parker L, Popescu D. 2002. Protein kinase C (PKC) isoforms in Drosophila. J Biochem. 132:523-527.
94. Silver SJ, Rebay I. 2005. Signaling circuitries in development: insights from the retinal determination gene network. Development. 132:3-13.
95. Smith DP, Ranganathan R, Hardy RW, Marx J, Tsuchida T, Zuker CS. 1991. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science. 254:1478-1484.
96. Stauber M, Jackle H, Schmidt-Ott U. 1999. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA. 96:3786-3789.
97. Stauber M, Prell A, Schmidt-Ott U. 2002. A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA. 99:274-279.
98. Stavenga DG. 1995. Insect retinal pigments: spectral characteristics and physiological functions. Prog Retin Eye Res. 15:231-259.
99. Stavenga DG. 2004. Visual acuity of fly photoreceptors in natural conditions - dependence on UV sensitizing pigment and light-controlling pupil. J Exp Biol. 207:1703-1713.
100. Suzanne M, Estella C, Calleja M, Sanchez-Herrero E. 2003. The hernandez and fernandez genes of Drosophila specify eye and antenna. Dev Biol. 260:465-483.
101. Taylor JS, Raes J. 2004. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet. 38:615-643.
102. Tribolium Genome Sequencing Consortium. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature. 452:949-955.
103. Van Emden B, Ramos H, Panchanathan S, Newfeld S, Kumar S. 2006. FlyExpress: an image-matching web-tool for finding genes with overlapping patterns of expression in Drosophila embryos. Tempe (AZ): Arizona State University.[Internet]. Available from: www.flyexpress.net.
104. Velarde RA, Sauer CD, Walden KK, Fahrbach SE, Robertson HM. 2005. Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem Mol Biol. 35:1367-1377.
105. Wagner A. 2008. Gene duplications, robustness and evolutionary innovations. Bioessays. 30:367-373.
106. Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K. 2005. Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften. 92:464-467.
107. Wang T, Montell C. 2007. Phototransduction and retinal degeneration in Drosophila. Pflugers Archiv-European Journal of Physiology. 454:821-847.
108. White RH, Xu H, Munch TA, Bennett RR, Grable EA. 2003. The retina of Manduca sexta: rhodopsin expression, the mosaic of green-, blue- and UV-sensitive photoreceptors, and regional specialization. J Exp Biol. 206:3337-3348.
109. Wiegmann BM, Yeates DK, Thorne JL, Kishino H. 2003. Time flies, a new molecular time-scale for brachyceran fly evolution without a clock. Syst Biol. 52:745-756.
110. Wolfsberg TG. 2007. Using the NCBI Map Viewer to browse genomic sequence data. Curr Protoc Bioinformatics. Chapter 1: Unit 1.5
111. Xia Q, Zhou Z, Lu C, et al. (83 co-authors). 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science. 306:1937-1940.
112. Yan H, Canon J, Banerjee U. 2003. A transcriptional chain linking eye specification to terminal determination of cone cells in the Drosophila eye. Dev Biol. 263:323-329.
113. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
114. Yao JG, Weasner BM, Wang LH, et al. (11 co-authors). 2008. Differential requirements for the Pax6(5a) genes eyegone and twin of eyegone during eye development in Drosophila. Dev Biol.
115. Yeates DK, Wiegmann BM. 2007. Phylogeny and evolution of Diptera: recent insights and new perspectives. In: Yeates DK, Wiegmann BM, editors. The evolutionary biology of flies. New York: Columbia Press University. p. 2-14.
116. Zdobnov EM, Bork P. 2007. Quantification of insect genome divergence. Trends Genet. 23:16-20.
117. Zhang T, Ranade S, Cai CQ, Clouser C, Pignoni F. 2006. Direct control of neurogenesis by selector factors in the fly eye: regulation of atonal by Ey and So. Development. 133:4881-4889.