The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges

Molecular Biology and Evolution

Volumn 31, Issue 5, 2014, Pages 1102-1120

  Riesgo, Ana ^a,c   Farrar, Nathan ^b   Windsor, Pamela J ^b   Giribet, Gonzalo ^a   Leys, Sally P ^b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Adhesion; Coordination; Epithelia; Innate immunity; RNAseq; Sex determination; Signaling

Indexed keywords

TRANSCRIPTOME;

AMPHIMEDON QUEENSLANDICA; ANTIGEN RECOGNITION; AQUIFER; ARTICLE; CALCAREA; CELL COMMUNICATION; CELL LINEAGE; CELL TYPE; DEMOSPONGIAE; GENETIC COMPLEMENTATION; GENOME ANALYSIS; HEXACTINELLIDA; HOMOSCLEROMORPHA; MOLECULAR EVOLUTION; MORPHOLOGY; NONHUMAN; OPISTHOKONTA; OSCARELLA CARMELA; SPONGE (PORIFERA);

ADHESION; COORDINATION; EPITHELIA; INNATE IMMUNITY; RNASEQ; SEX-DETERMINATION; SIGNALING;

ANIMALS; CELL ADHESION; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENOME; IMMUNITY, INNATE; PHYLOGENY; PORIFERA; REPRODUCTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTOME;

EID: 84898714170     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu057     Document Type: Article

References (102)

1. Adams EDM, Goss GG, Leys SP. 2010. Freshwater sponges have functional, sealing epithelia with high transepithelial resistance and negative transepithelial potential. PLoS One 5:e15040.
2. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM. 2007. Wnt and TGF-b expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2:e1031.
3. Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM. 2010. Structure and expression of conserved Wnt pathway components of the demosponge Amphimedon queenslandica. Evol Dev. 12:494-518.
4. Adamska M, Matus DQ, Adamski M, Green K, Rokhsar DS, Martindale MQ, Degnan BM. 2007. The evolutionary origin of hedgehog proteins. Curr Biol. 17:R836-R837.
5. Adell T, Nefkens I, Müller WEG. 2003. Polarity factor "Frizzled" in the demosponge Suberites domuncula: identification, expression and localization of the receptor in the epithelium/pinacoderm. FEBS Lett. 554:363-368.
6. Adell T, Thakur AN,Müller WEG. 2007. Isolation and characterization of Wnt pathway-related genes from Porifera. Cell Biol Int. 31:939-949.
7. Alié A, Manuel M. 2010. The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol Biol. 10:34.
8. Altschul SF, Madden TL, Schäffer 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.
9. Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Bamber R, Barber A, Bartsch I, Berta A, et al. 2012. The magnitude of global marine species diversity. Curr Biol. 22:2189-2202.
10. Armstrong PB, Quigley JP. 1999. a2-macroglobulin: an evolutionarily conserved arm of the innate immune system. Dev Comp Immunol. 23:375-390.
11. Bownes M. 1986. Expression of the genes coding for vitellogenin (yolk protein). Ann Rev Entomol. 31:507-531.
12. Buss LW. 1988. Diversification and germ-line determination. Paleobiology 14:313-321.
13. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+ : architecture and applications. BMC Bioinformatics 10:421.
14. Conaco C, Neveu P, Xhou H, ArcilaML, Degnan SM, Degnan BM, Kosik KS. 2012. Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions. BMC Genomics 13:209.
15. Conesa A, Götz S, Garc?́a-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
16. Conway Morris S. 1993. The fossil record and the early evolution of the Metazoa. Nature 361:219-225.
17. Counihan RT, McNamara DC, Souter DC, Jebreen EJ, Preston NP, Johnson CR, Degnan BM. 2001. Pattern, synchrony and predictability of spawning of the tropical abalone Haliotis asinina form Heron Reef, Australia. Mar Ecol Prog Ser. 213:193-202.
18. Dickinson DJ, Nelson WJ, Weis WI. 2011. A polarized epithelium organized by b-and a-catenin predates cadherin and metazoan origins. Science 331:1336-1339.
19. Dickinson DJ, Nelson WJ, Wiens M. 2012. An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity. BioEssays 34:833-840.
20. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, et al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749.
21. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res. 32:1792-1797.
22. Elliott GRD, Leys SP. 2010. Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae). J Exp Biol. 213:2310-2321.
23. Ellwanger K, Nickel M. 2006. Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoan Tethya wilhelma (Demospongiae, Porifera). Front Zool. 3:7.
24. Emson RH. 1966. The reactions of the sponge Cliona celata to applied stimuli. Comp Biochem Physiol. 18:805-827.
25. Ewen-Campen B, Schwager EE, Extavour CGM. 2010. The molecular machinery of germ line specification. Mol Reprod Dev. 77:3-18.
26. Extavour CGM, Akam M. 2003. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869-5884.
27. Fahey B, Degnan BM. 2010. Origin of animal epithelia: insights from the sponge genome. Evol Dev. 12:601-617.
28. Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, et al. 2013. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 15:R15.
29. Funayama N, NakatsukasaM,Mohri K, Agata K. 2010. Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol Dev. 12:275-287.
30. Gazave E, Lapébie P, Richards GS, Brunet F, Ereskovsky AV, Degnan BM, Borchiellini C, Vervoort M, Renard E. 2009. Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol. 9:249.
31. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 27:221-224.
32. Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW. 2006. The Wnt code: cnidarians signal the way. Oncogene 25: 7450-7460.
33. Harcet M, Roller M, Cetkovic H, Perina D, Wiens M, Müller WEG, Vlahovicek K. 2010. Demosponge EST sequencing reveals a complex genetic toolkit of the simplest metazoans. Mol Biol Evol. 27: 2747-2756.
34. Hardege JD, Bentley MG. 1997. Spawning synchrony in Arenicola marina: evidence for sex pheromonal control. Proc Biol Sci. 264: 1041-1047.
35. Harwood AJ. 2008. Dictyostelium development: a prototypic Wnt pathway?. In: Vincan E, editor. Wnt signalling. Vol. II: Pathway models. New York: Springer/Business Media. p. 21-32.
36. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, et al. 2009. Assessing the root of bilaterian animals with scalable phylogenomicmethods. Proc Biol Sci. 276:4261-4270.
37. Hibino T, Loza-Coll M,Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, et al. 2006. The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol. 300:349-365.
38. Hoppe WF, Reichert MJM. 1987. Predictable annual mass release of gametes by the coral reef sponge Neofibularia nolitangere (Porifera: Demospongiae). Mar Biol. 94:277-285.
39. Hughes AL. 1997. Rapid evolution of immunoglobulin superfamily C2 domains expressed in immune system cells. Mol Biol Evol. 14: 1-5.
40. Ingham PW, Nakano Y, Seger C. 2011. Mechanisms and functions of Hedgehog signalling across the Metazoa. Nat Rev Genet. 12: 393-406.
41. Iwaki D, Kanno K, Takahashi M, Endo Y, Matsushita M, Fujita T. 2011. The role of Mannose-binding-lectin-associated Serine protease-3 in activation of the alternative complement pathway. J Immunol. 187: 3751-3758.
42. Jackson DJ, Macis L, Reitner J, Degnan BM, Wörheide G. 2007. Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science 316:1893-1895.
43. Juliano C, Wessel G. 2010. Versatile germline genes: when are germline cells segregated during animal development? Science 329: 640-641.
44. Katoh K, Kuma K-I, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33:511-518.
45. Kelley LA, Sternberg MJE. 2009. Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc. 4:363-371.
46. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788.
47. Kopp A. 2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 28:175-184.
48. Labouesse M, Georges-Labouesse E. 2003. Cell adhesion: parallels between vertebrate and invertebrate focal adhesions. Curr Biol. 13: R528-R530.
49. Lapébie P, Gazave E, Ereskovsky A, Derelle R, Bézac C, Renard E, Houliston E, Borchiellini C TL. 2009. WNT/b-catenin signalling and epithelial patterning in the homoscleromorph sponge. Oscarella. PLoS One 4:e5823.
50. Lentz TL. 1966. Histochemical localization of neurohumors in a sponges. J Exp Zool. 162:171-179.
51. Leys SP, Riesgo A. 2012. Epithelia, an evolutionary novelty of metazoans. J Exp Zool B Mol Dev Evol. 318:438-447.
52. Li J, Wang S, Huang S, Cheng D, Shen S, Xiong C. 2009. Attractin gene deficiency contributes to testis vacuolization and sperm dysfunction in male mice. J Huazhong Univ Sci Technol. 29:750-754.
53. Lin H. 1997. The tao of stem cells in the germline. Ann Rev Genet. 31: 455-491.
54. Matus DQ, Magie CR, Pang K, Martindale MQ, Thomsen GH. 2008. The Hedgehog gene family of the cnidarian Nematostella vectensis and implications for understanding metazoan Hedgehog pathway evolution. Dev Biol. 313:501-518.
55. Medina M, Collins AG, Silberman JD, Sogin ML. 2001. Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Nat Acad Sci U S A. 98: 9707-9712.
56. MckeownM,Madigan SJ. 1992. Sex determination and differentiation in invertebrates: Drosophila and Caenorhabditis elegans. Curr Opin Cell Biol. 4:948-954.
57. McShea DW. 1996. Perspective: Metazoan complexity and evolution: is there a trend? Evolution 50:477-492.
58. Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TCG. 2007. The innate immune repertoire in Cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8:R59.
59. Miller SW, Hayward DC, Bunch TA, Miller DJ, Ball EE, Bardwell VJ, Zarkower D, Brower DL. 2003. A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol Dev. 5:251-258.
60. Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T. 2001. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev Genes Evol. 211: 299-308.
61. Mochizuki K, Sano H, Kobayashi S, Nishimiya-Fujisawa C, Fujisawa T. 2000. Expression and evolutionary conservation of nanos-related genes in Hydra. Dev Genes Evol. 210:591-602.
62. Nichols SA, Dirks W, Pearse JS, King N. 2006. Early evolution of animal cell signalling and adhesion genes. Proc Nat Acad Sci U S A. 103: 12451-12456.
63. Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N. 2012. Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/b-catenin complex. Proc Nat Acad Sci U S A. 109: 13046-13051.
64. Nielsen C. 2012. Animal evolution: interrelationships of the living phyla. Oxford: Oxford University Press.
65. Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, MaldonadoM,MüllerWE, Nickel M, Schierwater B, et al. 2013. Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol. 67:223-233.
66. Notredame C, Higgins DG, Heringa H. 2000. T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol. 302: 205-217.
67. Novo M, Riesgo A, Fernández-Guerra A, Giribet G. 2013. Pheromone evolution, reproductive genes, and comparative transcriptomics in Mediterranean earthworms (Annelida, Oligochaeta, Hormogastridae). Mol Biol Evol. 30:1614-1629.
68. Painter SD, Clough B, Garden RW, Sweedler JV, Nagle GT. 1998. Characterization of Aplysia Attractin, the first water-borne peptide pheromone in invertebrates. Biol Bull. 194:120-131.
69. Pérez-Porro AR, Navarro-Gómez D, Uriz MJ, Giribet G. 2013. A NGS approach to the encrusting Mediterranean sponge Crella elegans (Porifera, Demospongiae, Poecilosclerida): transcriptome sequencing, characterization and overview of the gene expression along three life cycle stages. Mol Ecol Res. 13:494-509.
70. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D. 2011. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 9: e1000602.
71. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alié A, Morgenstern B, Manuel M, et al. 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol. 27:1983-1987.
72. Raz E. 2000. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1:1017.1011-1017.1016.
73. Richards GS, Degnan BM. 2009. The dawn of developmental signalling in the Metazoa. Cold Spring Harbor Symp Quant Biol. 74:81-90.
74. Richards GS, Degnan BM. 2012. The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signalling in metazoan development. Evo Devo. 3:15.
75. Richards GS, Simionato E, Peron M, Adamska M, Vervoort M, Degnan BM. 2008. Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol. 18:1156-1161.
76. Riesgo A, Andrade SCS, Sharma PP, Novo M, Pérez-Porro AR, Vahtera V, González VL, Kawauchi GY, Giribet G. 2012. Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Frontiers Zool. 9:33.
77. Riesgo A, Maldonado M. 2008. Differences in reproductive timing among sponges sharing habitat and thermal regime. Invertebr Biol. 127:357-367.
78. Riesgo A, Maldonado M. 2009. Sexual reproduction of demosponges. Berlin: Verlag.
79. Riesgo A, Maldonado M, Durfort M. 2007. Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Mar Freshw Res. 58:398-417.
80. Riesgo A, Pérez-Porro AR, Carmona S, Leys SP, Giribet G. 2012. Optimization of preservation and storage time of sponge tissues to obtain quality mRNA for next-generation sequencing. Mol Ecol Res. 12:312-322.
81. Ryan JF, Pang K, Program NCS, Mullikin JC, Martindale MQ, Baxevanis AD. 2010. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to ParaHoxozoa. Evo Devo. 1:9.
82. Ryan JF, Pang K, Schnitzler CE, Nguyen A-D, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Comparative Sequencing Program NISC, et al. 2013. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342: 1242592.
83. Ryan TJ, Grant SGN. 2009. The origin and evolution of synapses. Nat Rev Neurosci. 10:701-712.
84. Saffman EE, Lasko P. 1999. Germline development in vertebrates and invertebrates. Cell Mol Life Sci. 55:1141-1163.
85. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang I-F, Tidor B, Degnan BM, Kosik KS. 2007. A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2:e506.
86. Salmoun M, Devijer C, Daloze D, Braekman J-C, van Soest RWM. 2002. 5-Hydroxytryptamine-derived alkaloids from two marine sponges of the genus Hyrtiois. J Nat Prod. 65:1173-1176.
87. Sebé-Pedrós A, Roger AJ, Lang FB, King N, Ruiz-Trillo I. 2010. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc Nat Acad Sci U S A. 107:10142-10147.
88. Simpson TL. 1984. The cell biology of sponges. Berlin: Springer Verlag.
89. Song X, Ping J, Sheng Q, Liming C, Fei M. 2012. The evolution and origin of animal Toll-like receptor signaling pathway revealed by network-level molecular evolutionary analyses. PLoS One 7: e51657.
90. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, et al. 2008. The Trichoplax genome and the nature of placozoans. Nature 454: 955-960.
91. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720-726.
92. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
93. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 57:758-771.
94. Tucker RP. 2013. Horizontal gene transfer in choanoflagellates. J Exp Zool B Mol Dev Evol. 320:1-9.
95. Turner CE. 2000. Paxillin and focal adhesion signalling. Nat Cell Biol. 2: E231-E236.
96. Vacalet J, Boury-Esnault N. 1995. Carnivorous sponges. Nature 373: 26.
97. Weyrer S, Rützler K, Rieger R. 1999. Serotonin in Porifera? From developing Tedania ignis, the Caribbean fire sponge (Demospongiae). Mem Queensland Mus. 44:659-665.
98. Wiley HS, Wallace RA. 1981. The structure of Vitellogenin. J Biol Chem. 256:8626-8634.
99. Windsor PJ, Leys SP. 2010. Wnt signalling and induction in the sponges aquiferous system: evidence for an ancient origin of the organizer. Evol Dev. 12:484-493.
100. Wyatt TD. 2003. Pheromones and animal behaviour: communication by smell and taste. Cambridge: Cambridge University Press.
101. Wylie C. 1999. Germ cells. Cell 96:165-174.
102. Zrzavý J, Mihulka S, Kepka P, Bezde?k A, Tietz D. 1998. Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249-285.