Genetics of gene expression responses to temperature stress in a sea urchin gene network

Molecular Ecology

Volumn 21, Issue 18, 2012, Pages 4547-4562

  Runcie, Daniel E ^a   Garfield, David A ^a   Babbitt, Courtney C ^a   Wygoda, Jennifer A ^a   Mukherjee, Sayan ^a,b   Wray, Gregory A ^a  

^a DUKE UNIVERSITY   (United States)

^b Duke University   (United States)

Author keywords

gene expression; gene network; gene environment interaction; stress response; Strongylocentrotus purpuratus

Indexed keywords

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLIMATE CHANGE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; SEQUENCE ANALYSIS; STRONGYLOCENTROTUS; SYSTEMS BIOLOGY; TEMPERATURE;

ANIMALS; BAYES THEOREM; CLIMATE CHANGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENE-ENVIRONMENT INTERACTION; MODELS, GENETIC; SEQUENCE ANALYSIS, RNA; STRONGYLOCENTROTUS PURPURATUS; SYSTEMS BIOLOGY; TEMPERATURE;

ECHINOIDEA; STRONGYLOCENTROTUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 84866262328     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05717.x     Document Type: Article

References (82)

1. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image processing with ImageJ. Biophotonics international, 11, 36-42.
2. Andronikov V, (1975) Heat resistance of gametes of marine invertebrates in relation to temperature conditions under which the species exist. Marine Biology, 30, 1-11.
3. Angerer LM, Angerer RC, (2003) Patterning the Sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Current Topics in Developmental Biology, 53, 159-198.
4. Azad AK, Pearce CM, McKinley RS, (2011) Influence of stocking density and temperature on early development and survival of the purple sea urchin, Strongylocentrotus purpuratus (Stimpson, 1857). Aquaculture Research, 1-15. DOI: 10.1111/j.1365-2109.2011.02960.x.
5. Barry JP, Baxter CH, Sagarin RD, Gilman SE, (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science, 267, 672-675.
6. Basch L, Tegner M, (2007) Reproductive responses of purple sea urchin (Strongylocentrotus purpuratus) populations to environmental conditions across a coastal depth gradient. Bulletin of Marine Science, 81, 255-282.
7. Bédard PA, Brandhorst BP, (1986) Translational activation of maternal mRNA encoding the heat-shock protein hsp90 during sea urchin embryogenesis. Developmental Biology, 117, 286-293.
8. 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.
9. Bertram D, Strathmann R, (1998) Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology, 79, 315-327.
10. Bolouri H, Davidson EH, (2003) Transcriptional regulatory cascades in development: initial rates, not steady state, determine network kinetics. Proceedings of the National Academy of Sciences of the United States of America, 100, 9371-9376.
11. Bürger R, Lynch M, (1997) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution, 49, 151-163.
12. Byrne M, Selvakumaraswamy P, Ho MA, Woolsey E, Nguyen HD, (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Research Part II: Topical Studies in Oceanography, 58, 712-719.
13. Chen C, Chen B, (1992) Effects of high temperature on larval development and metamorphosis of Arachnoides placenta (Echinodermata: Echinoidea). Marine Biology, 122, 445-449.
14. Cochran RC, Engelmann F, (1975) Environmental regulation of the annual reproductive season of Strongylocentrotus purpuratus (Stimpson). Biological Bulletin, 148, 393-401.
15. Comstock R, Robinson H, (1948) The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics, 4, 254-266.
16. Davidson EH, Rast JP, Oliveri P, et al., (2002) A genomic regulatory network for development. Science, 295, 1669-1678.
17. Delworth TL, Broccoli AJ, Rosati A, et al., (2006) GFDL's CM2 global coupled climate models. Part I: formulation and simulation characteristics. Journal of Climate, 19, 643-674.
18. Edmands S, Moberg P, Burton R, (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Marine Biology, 126, 443-450.
19. Farmanfarmaian A, Giese A, (1963) Thermal tolerance and acclimation in the western Purple Sea urchin, Strongylocentrotus purpuratus. Physiological Zoology, 36, 237-243.
20. Feder ME, Hofmann GE, (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology, 61, 243-282.
21. Fujisawa H, (1989) Differences in temperature dependence of early development of sea urchins with different growing seasons. Biological Bulletin, 176, 96.
22. Fujisawa H, (1993) Temperature sensitivity of a hybrid between two species of sea urchin differing in thermotolerance. Development Growth and Differentiation, 35, 395-401.
23. Fujisawa H, Shigei M, (1990) Correlation of embryonic temperature sensitivity of sea-urchins with spawning season. Journal of Experimental Marine Biology and Ecology, 136, 123-139.
24. Gasch AP, Spellman PT, Kao CM, et al., (2000) Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell, 11, 4241-4257.
25. George SB, (1999) Egg quality, larval growth and phenotypic plasticity in a forcipulate seastar. Journal of Experimental Marine Biology and Ecology, 237, 203-224.
26. Gibson G, Dworkin I, (2004) Uncovering cryptic genetic variation. Nature Reviews Genetics, 5, 681-690.
27. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J, (2008) Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology, 17, 167-178.
28. Giese A, Farmanfarmaian A, (1963) Resistance of the purple sea urchin to osmotic stress. Biological Bulletin, 124, 182.
29. Hammond LM, Hofmann GE, (2010) Thermal tolerance of Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns. Marine Biology, 157, 2677-2687.
30. Hellemans J, Mortier G, Paepe AD, Speleman F, Vandesompele J, (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology, 8, R19.
31. Hinman VF, Davidson EH, (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proceedings of the National Academy of Sciences, 104, 19404-19409.
32. Hochachka PW, Somero GN, (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution, 1st edn. Oxford University Press, New York, NY, USA.
33. Hoffmann AA, Hercus M, (2000) Environmental stress as an evolutionary force. BioScience, 50, 217-226.
34. Huey RB, (1974) Behavioral thermoregulation in lizards-importance of associated costs. Science, 184, 1001-1003.
35. Huey RB, et al. (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society. B, Biological Sciences, 276, 1939-1948.
36. IPCC (2007) Climate Change 2007: Synthesis Report. IPCC, Cambridge University Press, Cambridge, UK.
37. Kellermann V, Heerwaarden BV, Sgro C, Hoffmann AA, (2009) Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science, 325, 1244-1246.
38. Kenner MC, (1992) Population dynamics of the sea urchin Strongylocentrotus purpuratus in a Central California kelp forest: recruitment, mortality, growth, and diet. Marine Biology, 112, 107-118.
39. Koehn RK, Bayne BL, (1989) Towards a physiological and genetical understanding of the energetics of the stress response. Biological Journal of the Linean Society, 37, 157-171.
40. Kuhn K, Baker S, Chudin E, et al., (2004) A novel, high-performance random array platform for quantitative gene expression profiling. Genome Research, 14, 2347-2356.
41. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
42. Lindquist S, (1986) The heat-shock response. Annual Reviews Biochemistry, 55, 1151-1191.
43. Lindsley DE, Poodry CA, (1977) A reversible temperature-induced developmental arrest in Drosophila. Developmental Biology, 56, 213-218.
44. Loeb J, (1916) The Organism as a Whole, From a Physicochemical Viewpoint. Putnam's Sons, New York, NY.
45. Longabaugh WJR, Davidson EH, Bolouri H, (2005) Computational representation of developmental genetic regulatory networks. Developmental Biology, 283, 1-16.
46. Lynch M, Walsh B, (1998) Genetics and Analysis of Quantitative Traits, 1st edn. Sinauer Associates Inc, Sunderland, MA.
47. Masel J, (2006) Cryptic genetic variation is enriched for potential adaptations. Genetics, 172, 1985-1991.
48. McCarthy DJ, Chen Y, Smyth GK, (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research, 40, 4288-4297.
49. Meiklejohn C, Hartl D, (2002) A single mode of canalization. Trends in Ecology & Evolution, 17, 468-473.
50. Oleksiak MF, Roach JL, Crawford DL, (2005) Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nature Genetics, 37, 67-72.
51. Oliver TA, Garfield DA, Manier MK, Haygood R, Wray GA, Palumbi SR, (2010) Whole-genome positive selection and habitat-driven evolution in a shallow and a deep-sea urchin. Genome Biology and Evolution, 2, 800-814.
52. Oliveri P, Tu Q, Davidson E, (2008) Global regulatory logic for specification of an embryonic cell lineage. Proceedings of the National Academy of Sciences of the United States of America, 105, 5955-5962.
53. Osovitz C, Hofmann GE, (2005) Thermal history-dependent expression of the hsp70 gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. Journal of Experimental Marine Biology and Ecology, 327, 134-143.
54. Palumbi SR, Wilson AC, (1990) Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and S. droebachiensis. Evolution, 44, 403-415.
55. Parmesan C, Yohe G, (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
56. Pearse JS, (2006) Ecological role of purple sea urchins. Science, 314, 940-941.
57. Pearse JS, Pearse VB, Davis KK, (1986) Photoperiodic regulation of gametogenesis and growth in the sea urchin Strongylocentrotus purpuratus. Journal of Experimental Zoology, 237, 107-118.
58. Pespeni MH, Garfield DA, Manier MK, Palumbi SR, (2011) Genome-wide polymorphisms show unexpected targets of natural selection. Proceedings of the Royal Society. B, Biological Sciences, 279, 1412-1420.
59. Peter IS, Davidson EH, (2010) The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Developmental Biology, 340, 188-199.
60. Pfaffl M, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
61. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP, (2010) Phenotypic plasticity's impacts on diversification and speciation. Trends in Ecology & Evolution, 25, 459-467.
62. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
63. Rice SH, (2000) The evolution of developmental interactions: epistasis, canalization, and integration. In: Epistasis and the Evolutionary Process (eds, Wolf JBW, Brodie ED, and, Wade MJ,), pp. 1-17. Oxford University Press, New York, NY USA.
64. Richter K, Haslbeck M, Buchner J, (2010) The heat shock response: life on the verge of death. Molecular Cell, 40, 253-266.
65. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
66. Roepke TA, Snyder MJ, Cherr GN, (2005) Estradiol and endocrine disrupting compounds adversely affect development of sea urchin embryos at environmentally relevant concentrations. Aquatic Toxicology, 71, 155-173.
67. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA, (2003) Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60.
68. Sanders B, Martin L, (1994) Copper inhibits the induction of stress protein synthesis by elevated temperatures in embryos of the sea urchin Strongylocentrus purpuratus. Comparative Biochemistry and Physiology. Part C, Pharmacology, Toxicology & Endocrinology, 109C (3), 295-307.
69. Schlichting CD, (2008) Hidden reaction norms, cryptic genetic variation, and evolvability. Annals of the New York Academy of Sciences, 1133, 187-203.
70. Schlichting CD, Pigliucci M, (1993) Control of phenotypic plasticity via regulatory genes. The American Naturalist, 142 (2), 366-370.
71. Sewell M, Young C, (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. Journal of Experimental Marine Biology and Ecology, 236, 291-305.
72. Sodergren E, Weinstock G, Davidson E, et al., (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science, 314, 941-952.
73. Somero GN, (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and "losers". Journal of Experimental Biology, 213, 912-920.
74. Strathmann MF, (1987) Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast, data and methods for the study of eggs, embryos, and larvae. Univ of Washington Pr, Seattle, WA, USA.
75. Todgham AE, Hofmann GE, (2009) Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. Journal of Experimental Biology, 212, 2579-2594.
76. Tomanek L, (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs. Journal of Experimental Biology, 213, 971-979.
77. Tu Q, Brown CT, Davidson EH, Oliveri P, (2006) Sea urchin Forkhead gene family: phylogeny and embryonic expression. Developmental Biology, 300, 49-62.
78. Via S, Lande R, (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 505-522.
79. Visser J, Hermisson J, Wagner G, (2003) Perspective: evolution and detection of genetic robustness. Evolution, 57, 1959-1972.
80. Wagner G, Booth G, Bagheri H, (1997) A population genetic theory of canalization. Evolution, 51, 329-347.
81. Wray G, Kitazawa C, Miner B, (2004) Culture of echinoderm larvae through metamorphosis. Methods in Cell Biology, 74, 75-86.
82. Yuh C-H, Dorman ER, Davidson EH, (2005) Brn1/2/4, the predicted midgut regulator of the endo16 gene of the sea urchin embryo. Developmental Biology, 281, 286-298.