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Common Transcriptional Mechanisms for Visual Photoreceptor Cell Differentiation among Pancrustaceans


Visual systems are populated by one of two fundamental types of photoreceptors, ciliary and rhabdomeric. Each photoreceptor type is defined by the opsin molecule expressed and the final morphological form adapted to house the phototransduction machinery. Here we address whether a common transcriptional mechanisms exists for the differentiation of rhabdomeric photoreceptors. We demonstrate that orthologs of two Drosophila (fruit fly) transcription factors, Pph13 and Orthodenticle, are expressed in photoreceptors of Pancrustaceans, Tribolium (red flour beetle) and Daphnia (water flea), and are capable of executing conserved functions of rhabdomeric photoreceptor differentiation. In particular, Tribolium and Daphnia orthologs are capable of substituting and rescuing the photoreceptor differentiation defects observed in their corresponding Drosophila mutants. Furthermore, loss of function analysis in Tribolium of both Pph13 and orthodenticle genes demonstrate they regulate opsin transcription and morphogenesis of the photoreceptor apical membrane. Our data illuminate a framework for rhabdomeric photoreceptor differentiation and provide the foundation for defining the ancestral regulatory modules for rhabdomeric differentiation and potential modifications that underlie the functional diversity observed in rhabdomeric photoreceptors.


Vyšlo v časopise: Common Transcriptional Mechanisms for Visual Photoreceptor Cell Differentiation among Pancrustaceans. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004484
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004484

Souhrn

Visual systems are populated by one of two fundamental types of photoreceptors, ciliary and rhabdomeric. Each photoreceptor type is defined by the opsin molecule expressed and the final morphological form adapted to house the phototransduction machinery. Here we address whether a common transcriptional mechanisms exists for the differentiation of rhabdomeric photoreceptors. We demonstrate that orthologs of two Drosophila (fruit fly) transcription factors, Pph13 and Orthodenticle, are expressed in photoreceptors of Pancrustaceans, Tribolium (red flour beetle) and Daphnia (water flea), and are capable of executing conserved functions of rhabdomeric photoreceptor differentiation. In particular, Tribolium and Daphnia orthologs are capable of substituting and rescuing the photoreceptor differentiation defects observed in their corresponding Drosophila mutants. Furthermore, loss of function analysis in Tribolium of both Pph13 and orthodenticle genes demonstrate they regulate opsin transcription and morphogenesis of the photoreceptor apical membrane. Our data illuminate a framework for rhabdomeric photoreceptor differentiation and provide the foundation for defining the ancestral regulatory modules for rhabdomeric differentiation and potential modifications that underlie the functional diversity observed in rhabdomeric photoreceptors.


Zdroje

1. EakinRM (1965) Evolution of photoreceptors. Cold Spring Harbor Symposia on Quantitative Biology 30: 363–370.

2. ArendtD, WittbrodtJ (2001) Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond B Biol Sci 356: 1545–1563.

3. ArendtD (2008) The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9: 868–882.

4. LambTD, ArendtD, CollinSP (2009) The evolution of phototransduction and eyes. Philosophical transactions of the Royal Society of London Series B, Biological Sciences 364: 2791–2793.

5. NilssonDE, ArendtD (2008) Eye evolution: the blurry beginning. Current Biology: CB 18: R1096–1098.

6. PlachetzkiDC, SerbJM, OakleyTH (2005) New insights into the evolutionary history of photoreceptor cells. Trends in Ecology and Evolution 20: 465–467.

7. MollereauB, DomingosPM (2005) Photoreceptor differentiation in Drosophila: from immature neurons to functional photoreceptors. Dev Dyn 232: 585–592.

8. TsachakiM, SprecherSG (2012) Genetic and developmental mechanisms underlying the formation of the Drosophila compound eye. Dev Dyn 241: 40–56.

9. FainGL, HardieR, LaughlinSB (2010) Phototransduction and the evolution of photoreceptors. Current Biology: CB 20: R114–124.

10. NilssonDE (2013) Eye evolution and its functional basis. Visual neuroscience 30: 5–20.

11. AcamporaD, AvantaggiatoV, TuortoF, BaroneP, ReichertH, et al. (1998) Murine Otx1 and Drosophila otd genes share conserved genetic functions required in invertebrate and vertebrate brain development. Development 125: 1691–1702.

12. SharmanAC, BrandM (1998) Evolution and homology of the nervous system: cross-phylum rescues of otd/Otx genes. Trends in Genetics 14: 211–214.

13. VandendriesER, JohnsonD, ReinkeR (1996) orthodenticle is required for photoreceptor cell development in the Drosophila eye. Dev Biol 173: 243–255.

14. JohnstonRJJr (2013) Lessons about terminal differentiation from the specification of color-detecting photoreceptors in the Drosophila retina. Ann N Y Acad Sci 1293: 33–44.

15. RanadeSS, Yang-ZhouD, KongSW, McDonaldEC, CookTA, et al. (2008) Analysis of the Otd-dependent transcriptome supports the evolutionary conservation of CRX/OTX/OTD functions in flies and vertebrates. Dev Biol 315: 521–534.

16. TahayatoA, SonnevilleR, PichaudF, WernetMF, PapatsenkoD, et al. (2003) Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev Cell 5: 391–402.

17. BaoR, FriedrichM (2009) Molecular evolution of the Drosophila retinome: exceptional gene gain in the higher Diptera. Molecular Biology and Evolution 26: 1273–1287.

18. GorielyA, MollereauB, CoffinierC, DesplanC (1999) Munster, a novel paired-class homeobox gene specifically expressed in the Drosophila larval eye. Mech Dev 88: 107–110.

19. ZelhofAC, KoundakjianE, ScullyAL, HardyRW, PoundsL (2003) Mutation of the photoreceptor specific homeodomain gene Pph13 results in defects in phototransduction and rhabdomere morphogenesis. Development 130: 4383–4392.

20. MishraM, OkeA, LebelC, McDonaldEC, PlummerZ, et al. (2010) Pph13 and orthodenticle define a dual regulatory pathway for photoreceptor cell morphogenesis and function. Development 137: 2895–2904.

21. JukamD, XieB, RisterJ, TerrellD, Charlton-PerkinsM, et al. (2013) Opposite Feedbacks in the Hippo Pathway for Growth Control and Neural Fate. Science 342: 1238016.

22. FortiniME, RubinGM (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev 4: 444–463.

23. MismerD, MichaelWM, LavertyTR, RubinGM (1988) Analysis of the promoter of the Rh2 opsin gene in Drosophila melanogaster. Genetics 120: 173–180.

24. PapatsenkoD, NazinaA, DesplanC (2001) A conserved regulatory element present in all Drosophila rhodopsin genes mediates Pax6 functions and participates in the fine-tuning of cell-specific expression. Mech Dev 101: 143–153.

25. BerghammerAJ, KlinglerM, WimmerEA (1999) A universal marker for transgenic insects. Nature 402: 370–371.

26. CaravasJ, FriedrichM (2010) Of mites and millipedes: recent progress in resolving the base of the arthropod tree. Bioessays 32: 488–495.

27. ShultzJW, RegierJC (2000) Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean+hexapod clade. Proc Biol Sci 267: 1011–1019.

28. RehmP, BornerJ, MeusemannK, von ReumontBM, SimonS, et al. (2011) Dating the arthropod tree based on large-scale transcriptome data. Mol Phylogenet Evol 61: 880–887.

29. RiegerD, StanewskyR, Helfrich-ForsterC (2003) Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms 18: 377–391.

30. ColbourneJK, PfrenderME, GilbertD, ThomasWK, TuckerA, et al. (2011) The ecoresponsive genome of Daphnia pulex. Science 331: 555–561.

31. Tribolium Genome SequencingC, RichardsS, GibbsRA, WeinstockGM, BrownSJ, et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949–955.

32. LiY, BrownSJ, HausdorfB, TautzD, DenellRE, et al. (1996) Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum. Development Genes and Evolution 206: 35–45.

33. BrowneWE, SchmidBG, WimmerEA, MartindaleMQ (2006) Expression of otd orthologs in the amphipod crustacean, Parhyale hawaiensis. Development Genes and Evolution 216: 581–595.

34. NoyesMB, ChristensenRG, WakabayashiA, StormoGD, BrodskyMH, et al. (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133: 1277–1289.

35. ZhongYF, HollandPW (2011) HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology. Evol Dev 13: 567–568.

36. RiveraAS, PankeyMS, PlachetzkiDC, VillacortaC, SymeAE, et al. (2010) Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach. BMC Evolutionary Biology 10: 123.

37. FriedrichM, RamboldI, MelzerRR (1996) The early stages of ommatidial development in the flour beetle Tribolium castaneum (Coleoptera, Tenebrionidae). Development Genes and Evolution 206: 136–146.

38. GuldnerFH, WolffJR (1970) [Ultrastructure of the compound eye of Daphnia pulex]. Zeitschrift fur Zellforschung und mikroskopische Anatomie 104: 259–274.

39. FlasterMS, MacagnoER (1984) Cellular interactions and pattern formation in the visual system of the branchiopod crustacean, Daphnia magna. III. The relationship between cell birthdates and cell fates in the optic lamina. The Journal of Neuroscience 4: 1486–1498.

40. LoprestiV, MacagnoER, LevinthalC (1973) Structure and development of neuronal connections in isogenic organisms: cellular interactions in the development of the optic lamina of Daphnia. Proc Natl Acad Sci USA 70: 433–437.

41. MacagnoER, LoprestiV, LevinthalC (1973) Structure and development of neuronal connections in isogenic organisms: variations and similarities in the optic system of Daphnia magna. Proc Natl Acad Sci USA 70: 57–61.

42. JackowskaM, BaoR, LiuZ, McDonaldEC, CookTA, et al. (2007) Genomic and gene regulatory signatures of cryptozoic adaptation: Loss of blue sensitive photoreceptors through expansion of long wavelength-opsin expression in the red flour beetle Tribolium castaneum. Front Zool 4: 24.

43. WilsonDS, ShengG, JunS, DesplanC (1996) Conservation and diversification in homeodomain-DNA interactions: a comparative genetic analysis. Proc Natl Acad Sci USA 93: 6886–6891.

44. CookT, PichaudF, SonnevilleR, PapatsenkoD, DesplanC (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4: 853–864.

45. BrandAH, PerrimonN (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.

46. McDonaldEC, XieB, WorkmanM, Charlton-PerkinsM, TerrellDA, et al. (2010) Separable transcriptional regulatory domains within Otd control photoreceptor terminal differentiation events. Dev Biol 347: 122–132.

47. TerrellD, XieB, WorkmanM, MahatoS, ZelhofA, et al. (2012) OTX2 and CRX rescue overlapping and photoreceptor-specific functions in the Drosophila eye. Dev Dyn 241: 215–228.

48. JohnstonRJJr, OtakeY, SoodP, VogtN, BehniaR, et al. (2011) Interlocked feedforward loops control cell-type-specific Rhodopsin expression in the Drosophila eye. Cell 145: 956–968.

49. PosnienN, SchinkoJ, GrossmannD, ShippyTD, KonopovaB, et al. (2009) RNAi in the red flour beetle (Tribolium). Cold Spring Harb Protoc 2009

50. ChenS, WangQL, NieZ, SunH, LennonG, et al. (1997) Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19: 1017–1030.

51. FurukawaT, MorrowEM, CepkoCL (1997) Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91: 531–541.

52. KoikeC, NishidaA, UenoS, SaitoH, SanukiR, et al. (2007) Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Molecular and Cellular Biology 27: 8318–8329.

53. NishidaA, FurukawaA, KoikeC, TanoY, AizawaS, et al. (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nature Neuroscience 6: 1255–1263.

54. BrittenRJ, DavidsonEH (1969) Gene regulation for higher cells: a theory. Science 165: 349–357.

55. HinmanVF, DavidsonEH (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 104: 19404–19409.

56. Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray. 502 p.

57. Salvini-PlawenL, MayerE (1977) On the evolution of photoreceptors and eyes. Evol Biol 10: 207–263.

58. GajT, GersbachCA, BarbasCF3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31: 397–405.

59. WeiC, LiuJ, YuZ, ZhangB, GaoG, et al. (2013) TALEN or Cas9 - rapid, efficient and specific choices for genome modifications. J Genet Genomics 40: 281–289.

60. GooleyJJ, LuJ, ChouTC, ScammellTE, SaperCB (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4: 1165.

61. ProvencioI, RodriguezIR, JiangG, HayesWP, MoreiraEF, et al. (2000) A novel human opsin in the inner retina. J Neurosci 20: 600–605.

62. FriocourtG, PoirierK, RakicS, ParnavelasJG, ChellyJ (2006) The role of ARX in cortical development. Eur J Neurosci 23: 869–876.

63. MarshE, FulpC, GomezE, NasrallahI, MinarcikJ, et al. (2009) Targeted loss of Arx results in a developmental epilepsy mouse model and recapitulates the human phenotype in heterozygous females. Brain 132: 1563–1576.

64. ShigaY, YasumotoR, YamagataH, HayashiS (2002) Evolving role of Antennapedia protein in arthropod limb patterning. Development 129: 3555–3561.

65. ReinkeR, KrantzDE, YenD, ZipurskySL (1988) Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52: 291–301.

66. Van VactorDJr, KrantzDE, ReinkeR, ZipurskySL (1988) Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52: 281–290.

67. ZelhofAC, YaoTP, ChenJD, EvansRM, McKeownM (1995) Seven-up inhibits ultraspiracle-based signaling pathways in vitro and in vivo. Mol Cell Biol 15: 6736–6745.

68. LorenzenMD, KimzeyT, ShippyTD, BrownSJ, DenellRE, et al. (2007) piggyBac-based insertional mutagenesis in Tribolium castaneum using donor/helper hybrids. Insect Molecular Biology 16: 265–275.

69. TomoyasuY, DenellRE (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 214: 575–578.

70. LohseM, BolgerAM, NagelA, FernieAR, LunnJE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research 40: W622–627.

71. KimD, PerteaG, TrapnellC, PimentelH, KelleyR, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14: R36.

72. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biology 11: R106.

73. GentlemanRC, CareyVJ, BatesDM, BolstadB, DettlingM, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5: R80.

74. ZelhofAC, HardyRW, BeckerA, ZukerCS (2006) Transforming the architecture of compound eyes. Nature 443: 696–699.

75. SagawaK, YamagataH, ShigaY (2005) Exploring embryonic germ line development in the water flea, Daphnia magna, by zinc-finger-containing VASA as a marker. Gene Expression Patterns 5: 669–678.

76. NieJ, MahatoS, MustillW, TippingC, BhattacharyaSS, et al. (2012) Cross species analysis of Prominin reveals a conserved cellular role in invertebrate and vertebrate photoreceptor cells. Dev Biol 371: 312–320.

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