Coral Reefs

, 26:475 | Cite as

Genomic and microarray approaches to coral reef conservation biology

  • S. Forêt
  • K. S. Kassahn
  • L. C. Grasso
  • D. C. Hayward
  • A. Iguchi
  • E. E. Ball
  • D. J. Miller


New technologies based on DNA microarrays and comparative genomics hold great promise for providing the background biological information necessary for effective coral reef conservation and management. Microarray analysis has been used in a wide range of applications across the biological sciences, most frequently to examine simultaneous changes in the expression of large numbers of genes in response to experimental manipulation or environmental variation. Other applications of microarray methods include the assessment of divergence in gene sequences between species and the identification of fast-evolving genes. Arrays are presently available for only a limited range of species, but with appropriate controls they can be used for related species, thus avoiding the considerable costs associated with development of a system de novo. Arrays are in use or preparation to study stress responses, early development, and symbiosis in Acropora and Montastraea. Ongoing projects on several corals are making available large numbers of expressed gene sequences, enabling the identification of candidate genes for studies on gamete specificity, allorecognition and symbiont interactions. Over the next few years, microarray and comparative genomic approaches are likely to assume increasingly important and widespread use to study many aspects of the biology of coral reef organisms. Application of these genomic approaches to enhance our understanding of genetic and physiological correlates during stress, environmental disturbance and disease bears direct relevance to the conservation of coral reef ecosystems.


Microarray Genomics EST WGS Acropora Fast evolving genes 



We gratefully acknowledge the contributions of various members of our laboratories and external collaborators, and the support of the Australian Research Council (ARC) both directly to DJM and EEB (Grants A00105431, DP0209460 and DP0344483) and via the Centre for the Molecular Genetics of Development and the Centre of Excellence for Coral Reef Studies.


  1. Adjaye J, Herwig R, Herrmann D, Wruck W, BenKahla A, Brink T, Nowak M, Carnwath J, Hultschig C, Niemann H, Lehrach H (2004) Cross-species hybridisation of human and bovine orthologous genes on high density cDNA microarrays. BMC Genomics 5:83CrossRefGoogle Scholar
  2. Allison DB, Cui X, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet 7:55–65CrossRefGoogle Scholar
  3. 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 25:3389–3402CrossRefGoogle Scholar
  4. Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, Saint R, Harrison P L, Miller DJ (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46:671–678Google Scholar
  5. Bielawski JP, Yang Z (2004) A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol 59:121–132CrossRefGoogle Scholar
  6. Bowtell D, Sambrook J (2003) DNA microarrays: a molecular cloning manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  7. Brunelle B, Nicholson T, Stephens R (2004) Microarray-based genomic surveying of gene polymorphisms in Chlamydia trachomatis. Genome Biol 5:R42CrossRefGoogle Scholar
  8. Castillo-Davis CI, Kondrashov FA, Hartl DL, Kulathinal RJ (2004) The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res 14:802–811CrossRefGoogle Scholar
  9. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, Wolfsberg TG, Gabrielian AE, Landsman D, Lockhart DJ, Davis RW (1998) A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2:65–73CrossRefGoogle Scholar
  10. Churchill GA (2002) Fundamentals of experimental design for cDNA microarrays. Nat Genet Supp 32:490–495CrossRefGoogle Scholar
  11. Cohen S (2002) Strong positive selection and habitat-specific amino acid substitution patterns in MHC from an estuarine fish under intense pollution stress. Mol Biol Evol 19:1870–1880Google Scholar
  12. Douglas AE (2003) Coral bleaching-how and why? Mar Pollut Bull 46:385–392CrossRefGoogle Scholar
  13. Edge SE, Morgan MB, Gleason DF, Snell TW (2005) Development of a coral cDNA array to examine gene expression profiles in Montastraea faveolata exposed to environmental stress. Mar Pollut Bull 51:507–523CrossRefGoogle Scholar
  14. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868CrossRefGoogle Scholar
  15. Fairhead C, Dujon B (2006) Structure of Kluyveromyces lactis subtelomeres: duplications and gene content. FEMS Yeast Res 6:428–441CrossRefGoogle Scholar
  16. Feder ME, Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nature Rev Genet 4:651–657CrossRefGoogle Scholar
  17. Galindo BE, Vacquier VD, Swanson WJ (2003) Positive selection in the egg receptor for abalone sperm lysin. Proc Natl Acad Sci USA 100:4639–4643CrossRefGoogle Scholar
  18. Gao B, Klein LE, Britten RJ, Davidson EH (1986) Sequence of mRNA coding for bindin, a species-specific sea urchin sperm protein required for fertilization. Proc Natl Acad Sci USA 83:8634–8638CrossRefGoogle Scholar
  19. Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S (2005) (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, HeidelbergGoogle Scholar
  20. Gilad Y, Rifkin SA, Bertone P, Gerstein M, White KP (2005) Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. Genome Res 15:674–680CrossRefGoogle Scholar
  21. Gilad Y, Oshlack A, Rifkin SA (2006) Natural selection on gene expression. Trends Genet 22:456–461CrossRefGoogle Scholar
  22. Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98:1993–1998CrossRefGoogle Scholar
  23. Gracey AY, Fraser EJ, Li W, Fang Y, Taylor RR, Rogers J, Brass A, Cossins AR (2004) Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101:16970–16975CrossRefGoogle Scholar
  24. Harr B (2006) Genomic islands of differentiation between house mouse subspecies. Genome Res 16:730–737CrossRefGoogle Scholar
  25. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279CrossRefGoogle Scholar
  26. Hinchliffe SJ, Isherwood KE, Stabler RA, Prentice MB, Rakin A, Nichols RA, Oyston PCF, Hinds J, Titball RW, Wren BW (2003) Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res 13:2018–2029CrossRefGoogle Scholar
  27. Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129Google Scholar
  28. Iyer VR, Eisen MB, Ross DT, Schuler G, Moore T, Lee JC, Trent JM, Staudt LM, Hudson J Jr, Boguski MS, Lashkari D, Shalon D, Botstein D, Brown PO (1999) The transcriptional program in the response of human fibroblasts to serum. Science 283:83–87CrossRefGoogle Scholar
  29. Ji W, Zhou W, Gregg K, Yu N, Davis S, Davis S (2004) A method for cross-species gene expression analysis with high-density oligonucleotide arrays. Nucleic Acids Res 32:e93CrossRefGoogle Scholar
  30. Kane M, Jatkoe T, Stumpf C, Lu J, Thomas J, Madore S (2000) Assessment of the sensitivity and specificity of oligonucleotide (50mer) microarrays. Nucleic Acids Res 28:4552–4557CrossRefGoogle Scholar
  31. Kassahn KS, Caley MJ, Ward AC, Connolly AR, Stone G, Crozier RH (in press) Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish. Mol EcolGoogle Scholar
  32. Kim C, Joyce E, Chan K, Falkow S (2002) Improved analytical methods for microarray-based genome-composition analysis. Genome Biol 3: research0065Google Scholar
  33. Kimmel AR, Oliver B (2006a) DNA Microarrays Part A: Array Platforms and Wet-Bench Protocols. Methods Enzymol, vol 410Google Scholar
  34. Kimmel AR, Oliver B (2006b) DNA Microarrays Part B: Databases and Statistics. Methods Enzymol, vol 411Google Scholar
  35. Kortschak RD, Samuel G, Saint R, Miller DJ (2003) EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol 13:2190–2195CrossRefGoogle Scholar
  36. Krasnov A, Koskinen H, Pehkonen P, Rexroad CE, Afanasyev S, Molsa H (2005) Gene expression in the brain and kidney of rainbow trout in response to handling stress. BMC Genomics 6:3. doi:10.1186/1471-2164-6-3Google Scholar
  37. Kresge N, Vacquier VD, Stout CD (2001) Abalone lysin: the dissolving and evolving sperm protein. Bioessays 23:95–103CrossRefGoogle Scholar
  38. Le Quere A, Eriksen KA, Rajashekar B, Schutzenbubel A, Canback B, Johansson T, Tunlid A (2006) Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Mol Ecol 15:535–550CrossRefGoogle Scholar
  39. Lecompte O, Ripp R, Puzos-Barbe V, Duprat S, Heilig R, Dietrich J, Thierry JC, Poch O (2001) Genome evolution at the genus level: Comparison of three complete genomes of hyperthermophilic Archaea. Genome Res 11:981–993CrossRefGoogle Scholar
  40. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654CrossRefGoogle Scholar
  41. Makalowski W, Zhang JH, Boguski MS (1996) Comparative analysis of 1196 orthologous mouse and human full-length mRNA and protein sequences. Genome Res 6:846–857CrossRefGoogle Scholar
  42. Mardis ER (2006) Anticipating the $1,000 genome. Genome Biol 7:112. doi:10.1186/gb-2006-7-7-112Google Scholar
  43. Massingham T, Goldman N (2005) Detecting amino acid sites under positive selection and purifying selection. Genetics 169:1753–1762CrossRefGoogle Scholar
  44. Matzkin LM (2005) Activity variation in alcohol dehydrogenase paralogs is associated with adaptation to cactus host use in cactophilic Drosophila. Mol Ecol 14:2223–2231CrossRefGoogle Scholar
  45. Medhora M, Bousamra M, Zhu DL, Somberg L, Jacobs ER (2002) Upregulation of collagens detected by gene array in a model of flow-induced pulmonary vascular remodeling. Am J Physiol Heart Circ Physiol 282:H414–H422Google Scholar
  46. Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217CrossRefGoogle Scholar
  47. Mueller WA, Leitz T (2002) Metamorphosis in the Cnidaria. Can J Zool 80:1755–1771CrossRefGoogle Scholar
  48. Murray AE, Lies D, Li G, Nealson K, Zhou J, Tiedje JM (2001) DNA/DNA hybridization to microarrays reveals gene-specific differences between closely related microbial genomes. Proc Natl Acad Sci USA 98:9853–9858CrossRefGoogle Scholar
  49. Nei M (2005) Selectionism and neutralism in molecular evolution. Mol Biol Evol 22:2318–2342CrossRefGoogle Scholar
  50. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218CrossRefGoogle Scholar
  51. Nunney L, Schuenzel EL (2006) Detecting natural selection at the molecular level: a reexamination of some “classic” examples of adaptive evolution. J Mol Evol 62:176–195CrossRefGoogle Scholar
  52. Podrabsky JE, Somero GN (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol 207:2237–2254CrossRefGoogle Scholar
  53. Pollack JR, Perou CM, Alizadeh AA, Eisen MB, Pergamenschikov A, Williams CF, Jeffrey SS, Botstein D, Brown PO (1999) Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet 23:41–46CrossRefGoogle Scholar
  54. Popesco MC, Maclaren EJ, Hopkins J, Dumas L, Cox M, Meltesen L, McGavran L, Wyckoff GJ, Sikela JM (2006) Human lineage-specific amplification, selection, and neuronal expression of DUF1220 domains. Science 313:1304–1307CrossRefGoogle Scholar
  55. Powers DA, Schulte PM (1998) Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment: a multi-disciplinary approach to address the million-year saga of a small fish. J Exp Zool 282:71–94CrossRefGoogle Scholar
  56. Renn SC, Aubin-Horth N, Hofmann HA (2004) Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5:42. doi:10.1186/1471-2164-5-42Google Scholar
  57. Rudd S (2003) Expressed sequence tags: alternative or complement to whole genome sequences? Trends Plant Sci 8:321–329CrossRefGoogle Scholar
  58. Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470CrossRefGoogle Scholar
  59. Schwarz J, Brokstein P, Manohar C, Coffroth MA, Szmant A, Medina M (2006) Coral Reef Genomics: Developing tools for the functional genomics of coral symbiosis. Proc 10th Int Coral Reef Symp 274–281Google Scholar
  60. Shi P, Zhang J (2006) Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23:292–300CrossRefGoogle Scholar
  61. Spady TC, Seehausen O, Loew ER, Jordan RC, Kocher TD, Carleton KL (2005) Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Mol Biol Evol 22:1412–1422CrossRefGoogle Scholar
  62. Stoyanova R, Upson JJ, Patriotis C, Ross EA, Henske EP, Datta K, Boman B, Clapper ML, Knudson AG, Bellacosa A (2004) Use of RNA amplification in the optimal characterization of global gene expression using cDNA microarrays. J Cell Physiol 201:359–365CrossRefGoogle Scholar
  63. Suzuki Y, Gojobori T (2003) Analysis of coding sequence. In: Salemi M, Vandamme A-M (eds) The phylogenetic handbook. Cambridge University Press, Cambridge, pp 283–311Google Scholar
  64. Suzuki Y, Gojobori T, Nei M (2001) ADAPTSITE: detecting natural selection at single amino acid sites. Bioinformatics 17:660–661CrossRefGoogle Scholar
  65. Swanson WJ, Aquadro CF (2002) Positive darwinian selection promotes heterogeneity among members of the antifreeze protein multigene family. J Mol Evol 54:403–410Google Scholar
  66. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–14CrossRefGoogle Scholar
  67. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF (2001) Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA 98:7375–7379CrossRefGoogle Scholar
  68. Tautz D, Schmid KJ (1998) From genes to individuals: developmental genes and the generation of the phenotype. Philos Trans R Soc Lond B 353:231–240CrossRefGoogle Scholar
  69. Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639CrossRefGoogle Scholar
  70. Tennessen JA (2005) Molecular evolution of animal antimicrobial peptides: widespread moderate positive selection. J Evol Biol 18:1387–1394CrossRefGoogle Scholar
  71. Thomas JH, Kelley JL, Robertson HM, Ly K, Swanson WJ (2005) Adaptive evolution in the SRZ chemoreceptor families of Caenorhabditis elegans and Caenorhabditis briggsae. Proc Natl Acad Sci USA 102:4476–4481CrossRefGoogle Scholar
  72. Tsoi SCM, Cale JM, Bird IM, Ewart V, Brown LL, Douglas S (2003) Use of human cDNA microarrays for identification of differentially expressed genes in Atlantic salmon liver during Aeromonas salmonicida infection. Mar Biotechnol 5:545–554CrossRefGoogle Scholar
  73. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biology 3:1572–1578CrossRefGoogle Scholar
  74. Williams TD, Gensberg K, Minchin SD, Chipman JK (2003) A DNA expression array to detect toxic stress response in European flounder (Platichthys flesus). Aquatic Toxicol 65:141–157CrossRefGoogle Scholar
  75. Wu LY, Thompson DK, Li GS, Hurt RA, Tiedje JM, Zhou JZ (2001) Development and evaluation of functional gene arrays for detection of selected genes in the environment. Appl Env Microbiol 67:5780–5790CrossRefGoogle Scholar
  76. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503CrossRefGoogle Scholar
  77. Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917Google Scholar
  78. Yang YH, Speed T (2002) Design issues for cDNA microarray experiments. Nat Rev Genet 3:579–588Google Scholar
  79. Yang YH, Speed T (2003) Design of microarray expression experiments. In: Bowtell D, Sambrook J (eds) DNA microarrays: a molecular cloning manual. Cold Spring Harbor Laboratory Press, New York, pp 513–525Google Scholar
  80. Yu X-J, Zheng H-K, Wang J, Wang W, Su B (in press) Detecting lineage-specific adaptive evolution of brain-expressed genes in human using rhesus macaque as outgroup. Genomics. doi:10.1016/j.ygeno.2006.05.008Google Scholar
  81. Zakon HH, Lu Y, Zwickl DJ, Hillis DM (2006) Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc Natl Acad Sci USA 103:3675–3680CrossRefGoogle Scholar
  82. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479CrossRefGoogle Scholar
  83. Zhu B, Xu F, Baba Y (2006) An evaluation of linear RNA amplification in cDNA microarray gene expression analysis. Mol Genet Metab 87:71–79CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • S. Forêt
    • 1
  • K. S. Kassahn
    • 2
    • 5
  • L. C. Grasso
    • 3
  • D. C. Hayward
    • 3
  • A. Iguchi
    • 4
  • E. E. Ball
    • 3
  • D. J. Miller
    • 4
  1. 1.Mathematical Science InstituteAustralian National UniversityCanberraAustralia
  2. 2.School of Tropical Biology, James Cook UniversityTownsvilleAustralia
  3. 3.ARC Centre for the Molecular Genetics of Development, Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  4. 4.ARC Centre of Excellence in Coral Reef Biology and Comparative Genomics CentreJames Cook UniversityTownsvilleAustralia
  5. 5.Institute for Molecular BiosciencesUniversity of QueenslandBrisbaneAustralia

Personalised recommendations