Rapid evolution of coral proteins responsible for interaction with the environment

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Voolstra, Christian R ^a   Sunagawa, Shinichi ^b   Matz, Mikhail V ^c   Bayer, Till ^a   Aranda, Manuel ^a   Buschiazzo, Emmanuel ^d   DeSalvo, Michael K ^e   Lindquist, Erika ^f   Szmant, Alina M ^g   Coffroth, Mary Alice ^h   Medina, Mónica ^d  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f DOE JOINT GENOME INSTITUTE   (United States)

^g UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^h UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD63 ANTIGEN; GAMMA GLUTAMYL HYDROLASE; GAMMA INTERFERON; GLUTAREDOXIN; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; PROTEIN BAX; TOLL LIKE RECEPTOR 2; TRANSCRIPTOME; PROTEIN;

ARTICLE; CELL ADHESION; CELL LINEAGE; CNIDARIA; CONTROLLED STUDY; CORAL; DINOFLAGELLATE; ENDOSYMBIOSIS; EVOLUTIONARY ADAPTATION; EVOLUTIONARY RATE; EXPRESSED SEQUENCE TAG; INNATE IMMUNITY; ION TRANSPORT; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; OXIDATIVE STRESS; PHYLUM; PROTEIN ANALYSIS; REPRODUCTION; SENSORY SYSTEM; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; UNINDEXED SEQUENCE; ADAPTATION; ANIMAL; ANTHOZOA; CLASSIFICATION; CLUSTER ANALYSIS; ECOSYSTEM; ENVIRONMENT; EVOLUTION; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENETICS; GENOMICS; METABOLISM; METHODOLOGY; PROTEOMICS;

ACROPORA MILLEPORA; ACROPORA PALMATA; ANIMALIA; ANTHOZOA; AVES; DINOPHYCEAE; SYMBIODINIUM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; BIOLOGICAL EVOLUTION; CLUSTER ANALYSIS; ECOSYSTEM; ENVIRONMENT; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOMICS; PROTEINS; PROTEOMICS; SPECIES SPECIFICITY;

EID: 79957438702     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020392     Document Type: Article

References (80)

1. Hoegh-Guldberg O, (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50: 839-866.
2. Wilkinson C, (2004) Status of coral reefs of the world: 2004; Network GCRM, editor.
3. Weeks R, Russ GR, Alcala AC, White AT, (2009) Effectiveness of Marine Protected Areas in the Philippines for Biodiversity Conservation. Conserv Biol.
4. Game ET, Bode M, McDonald-Madden E, Grantham HS, Possingham HP, (2009) Dynamic marine protected areas can improve the resilience of coral reef systems. Ecol Lett.
5. Raymundo LJ, Halford AR, Maypa AP, Kerr AM, (2009) Functionally diverse reef-fish communities ameliorate coral disease. Proc Natl Acad Sci U S A 106: 17067-17070.
6. Bartlett CY, Manua C, Cinner J, Sutton S, Jimmy R, et al. (2009) Comparison of Outcomes of Permanently Closed and Periodically Harvested Coral Reef Reserves. Conserv Biol.
7. DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, et al. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952-3971.
8. Voolstra CR, Schnetzer J, Peshkin L, Randall CJ, Szmant AM, et al. (2009) Effects of temperature on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10: 627.
9. Portune KJ, Voolstra CR, Medina M, Szmant AM, (2010) Development and heat stress-induced transcriptomic changes during embryogenesis of the scleractinian coral Acropora palmata. Marine Genomics 3: 51-62.
10. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O, (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18: 5101-5114.
11. DeSalvo MK, Sunagawa S, Voolstra CR, Medina M, (2010) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Marine Ecology Progress Series 402: 97-113.
12. Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM, (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar Biotechnol (NY) 2: 533-544.
13. Meyer E, Davies S, Wang S, Willis B, Abrego D, et al. (2009) Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Marine Ecology Progress Series 392: 81-92.
14. Thompson DM, van Woesik R, (2009) Corals escape bleaching in regions that recently and historically experienced frequent thermal stress. Proc Biol Sci 276: 2893-2901.
15. Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, et al. (2008) Diversity and evolution of coral fluorescent proteins. PLoS One 3: e2680.
16. Field SF, Bulina MY, Kelmanson IV, Bielawski JP, Matz MV, (2006) Adaptive evolution of multicolored fluorescent proteins in reef-building corals. J Mol Evol 62: 332-339.
17. Schwarz JA, Brokstein PB, Voolstra C, Terry AY, Manohar CF, et al. (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9: 97.
18. Hayes ML, Eytan RI, Hellberg ME, (2010) High amino acid diversity and positive selection at a putative coral immunity gene (tachylectin-2). BMC Evol Biol 10: 150.
19. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
20. Hughes AL, Nei M, (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
21. Yang Z, Bielawski JP, (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15: 496-503.
22. Nielsen R, (2005) Molecular signatures of natural selection. Annu Rev Genet 39: 197-218.
23. Jensen JD, Wong A, Aquadro CF, (2007) Approaches for identifying targets of positive selection. Trends Genet 23: 568-577.
24. Fischer D, Eisenberg D, (1999) Finding families for genomic ORFans. Bioinformatics 15: 759-762.
25. Rubin GM, Yandell MD, Wortman JR, Gabor Miklos GL, Nelson CR, et al. (2000) Comparative Genomics of the Eukaryotes. Science 287: 2204-2215.
26. Wilson GA, Feil EJ, Lilley AK, Field D, (2007) Large-scale comparative genomic ranking of taxonomically restricted genes (TRGs) in bacterial and archaeal genomes. PLoS One 2: e324.
27. Wilson GA, Bertrand N, Patel Y, Hughes JB, Feil EJ, et al. (2005) Orphans as taxonomically restricted and ecologically important genes. Microbiology 151: 2499-2501.
28. Kunin V, Cases I, Enright AJ, de Lorenzo V, Ouzounis CA, (2003) Myriads of protein families, and still counting. Genome Biol 4: 401.
29. Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TC, (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends Genet 25: 404-413.
30. Tautz D, Schmid KJ, (1998) From genes to individuals: developmental genes and the generation of the phenotype. Philos Trans R Soc Lond B Biol Sci 353: 231-240.
31. Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M, (2009) Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS One 4: e4865.
32. Bosch TC, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, et al. (2009) Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev Comp Immunol 33: 559-569.
33. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
34. Suyama M, Torrents D, Bork P, (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34: W609-612.
35. Domazet-Loso T, Tautz D, (2003) An evolutionary analysis of orphan genes in Drosophila. Genome Res 13: 2213-2219.
36. Allocco D, Kohane I, Butte A, (2004) Quantifying the relationship between co-expression, co-regulation and gene function. BMC Bioinformatics 5: 18.
37. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, et al. (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18: 1823-1833.
38. Grasso LC, Maindonald J, Rudd S, Hayward DC, Saint R, et al. (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics 9: 540.
39. Reyes-Bermudez A, DeSalvo MK, Voolstra CR, Sunagawa S, Szmant AM, et al. (2009) Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata. Marine Genomics 2: 149-159.
40. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological) 57: 289-300.
41. Chen MC, Cheng YM, Sung PJ, Kuo CE, Fang LS, (2003) Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem Biophys Res Commun 308: 586-595.
42. Downs CA, Kramarsky-Winter E, Martinez J, Kushmaro A, Woodley CM, et al. (2009) Symbiophagy as a cellular mechanism for coral bleaching. Autophagy 5: 211-216.
43. Dunn SR, Schnitzler CE, Weis VM, (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc Biol Sci 274: 3079-3085.
44. Gates RD, Baghdasarian G, Muscatine L, (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182: 324-332.
45. Lesser M, Stochaj W, Tapley D, Shick J, (1990) Bleaching in coral reef anthozoans: Effects of irradiance, ultraviolet radiation and temperature, on the activities of protective enzymes against active oxygen. Coral Reefs 8: 225-232.
46. Merle PL, Sabourault C, Richier S, Allemand D, Furla P, (2007) Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic Biol Med 42: 236-246.
47. Sunagawa S, Choi J, Forman HJ, Medina M, (2008) Hyperthermic stress-induced increase in the expression of glutamate-cysteine ligase and glutathione levels in the symbiotic sea anemone Aiptasia pallida. Comp Biochem Physiol B: Biochem Mol Biol 151: 133-138.
48. van Oppen MJ, McDonald BJ, Willis B, Miller DJ, (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18: 1315-1329.
49. Hughes TP, Ayre D, Connell JH, (1992) The evolutionary ecology of corals. Trends in Ecology & Evolution 7: 292-295.
50. Babcock RC, (1991) Comparative Demography of Three Species of Scleractinian Corals Using Age- and Size-Dependent Classifications. Ecological Monographs 61: 225-244.
51. Baer CF, Miyamoto MM, Denver DR, (2007) Mutation rate variation in multicellular eukaryotes: causes and consequences. Nature Reviews Genetics 8: 619-631.
52. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
53. Voolstra CR, Sunagawa S, Schwarz JA, Coffroth MA, Yellowlees D, et al. (2008) Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium). Comp Biochem Physiol Part D Genomics Proteomics.
54. Frank SA, (1996) Host-symbiont conflict over the mixing of symbiotic lineages. Proceedings of the Royal Society of London Series B-Biological Sciences 263: 339-344.
55. DeSalvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, et al. (2010) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 19: 1174-1186.
56. Heinen TJ, Staubach F, Haming D, Tautz D, (2009) Emergence of a new gene from an intergenic region. Curr Biol 19: 1527-1531.
57. Foret S, Knack B, Houliston E, Momose T, Manuel M, et al. (2010) New tricks with old genes: the genetic bases of novel cnidarian traits. Trends Genet 26: 154-158.
58. Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, et al. (2008) Patterns of positive selection in six Mammalian genomes. PLoS genetics 4: e1000144.
59. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U, (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21: 1219.
60. Warner ME, Fitt WK, Schmidt GW, (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl Acad Sci U S A 96: 8007-8012.
61. Asada K, Takahashi M, (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ, editors. Amsterdam, Elsevier pp. 227-287 and Topics in photosynthesis, Vol 9: Photoinhibition.
62. Baird AH, Bhagooli R, Ralph PJ, Takahashi S, (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24: 16-20.
63. Dunn SR, Weis VM, (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environmental microbiology 11: 268-276.
64. Jimbo M, Yanohara T, Koike K, Sakai R, Muramoto K, et al. (2000) The D-galactose-binding lectin of the octocoral Sinularia lochmodes: characterization and possible relationship to the symbiotic dinoflagellates. Comparative biochemistry and physiology Part B, Biochemistry & molecular biology 125: 227-236.
65. Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM, (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8: 1985-1993.
66. Reynolds WS, Schwarz JA, Weis VM, (2000) Symbiosis-enhanced gene expression in cnidarian-algal associations: cloning and characterization of a cDNA, sym32, encoding a possible cell adhesion protein. Comparative biochemistry and physiology Part A, Molecular & integrative physiology 126: 33-44.
67. Rodriguez-Lanetty M, Phillips WS, Weis VM, (2006) Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7: 23.
68. Iwanaga S, Lee BL, (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38: 128-150.
69. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, et al. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10: 219.
70. Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, et al. (2009) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10: 258.
71. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
72. Tatusov RL, Koonin EV, Lipman DJ, (1997) A genomic perspective on protein families. Science 278: 631-637.
73. Telford MJ, (2007) Phylogenomics. Curr Biol 17: R945-946.
74. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
75. Goldman N, Yang Z, (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725-736.
76. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
77. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
78. Consortium UniProt (2011) Ongoing and future developments at the Universal Protein Resource. Nucleic acids research 39: D214-219.
79. Team RDC (2008) R: A language and environment for statistical computing: Vienna, Austria: R Foundation for Statistical Computing.
80. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, et al. (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS biology 3: e170.