Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians

Abstract

Coral reefs provide habitats for a disproportionate number of marine species relative to the small area of the oceans that they occupy. The mutualism between the cnidarian animal hosts and their intracellular dinoflagellate symbionts provides the nutritional foundation for coral growth and formation of reef structures, because algal photosynthesis can provide >90% of the total energy of the host. Disruption of this symbiosis (“coral bleaching”) is occurring on a large scale due primarily to anthropogenic factors and poses a major threat to the future of coral reefs. Despite the importance of this symbiosis, the cellular mechanisms involved in its establishment, maintenance, and breakdown remain largely unknown. We report our continued development of genomic tools to study these mechanisms in Aiptasia, a small sea anemone with great promise as a model system for studies of cnidarian–dinoflagellate symbiosis. Specifically, we have generated de novo assemblies of the transcriptomes of both a clonal line of symbiotic anemones and their endogenous dinoflagellate symbionts. We then compared transcript abundances in animals with and without dinoflagellates. This analysis identified >900 differentially expressed genes and allowed us to generate testable hypotheses about the cellular functions affected by symbiosis establishment. The differentially regulated transcripts include >60 encoding proteins that may play roles in transporting various nutrients between the symbiotic partners; many more encoding proteins functioning in several metabolic pathways, providing clues regarding how the transported nutrients may be used by the partners; and several encoding proteins that may be involved in host recognition and tolerance of the dinoflagellate.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 121

1. 1.

   Adams Y. Smith S. L. Schwartz-Albiez R. Andrews K. T., 2005 Carrageenans inhibit the in vitro growth of Plasmodium falciparum and cytoadhesion to CD36. Parasitol. Res. 97: 290–294

   Not in our library10.1007/s00436-005-1426-3

2. 2.

   Ainsworth T. D. Wasmund K. Ukani L. Seneca F. Yellowlees D., 2011 Defining the tipping point. A complex cellular life/death balance in corals in response to stress. Sci. Rep. 1: 160

   Not in our library10.1038/srep00160

3. 3.

   Altura M. A. Stabb E. Goldman W. Apicella M. McFall-Ngai M. J., 2011 Attenuation of host NO production by MAMPs potentiates development of the host in the squid-Vibrio symbiosis. Cell. Microbiol. 13: 527–537

   Not in our library10.1111/j.1462-5822.2010.01552.x

4. 4.
   Differential expression analysis for sequence count data · 2010

   No notice
5. 5.

   Areschoug T. Gordon S., 2009 Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell. Microbiol. 11: 1160–1169

   Not in our library10.1111/j.1462-5822.2009.01326.x

6. 6.

   Ashburner M. Ball C. A. Blake J. A. Botstein D. Butler H., 2000 Gene ontology: tool for the unification of biology. Nat. Genet. 25: 25–29

   Not in our library10.1038/75556

7. 7.

   Augustin R. Riley J. Moley K. H., 2005 GLUT8 contains a [DE]XXXL[LI] sorting motif and localizes to a late endosomal/lysosomal compartment. Traffic 6: 1196–1212

   Not in our library10.1111/j.1600-0854.2005.00354.x

8. 8.

   Baldauf S. L., 2003 The deep roots of eukaryotes. Science 300: 1703–1706

   Not in our library10.1126/science.1085544

9. 9.

   Bang M. L. Centner T. Fornoff F. Geach A. J. Gotthardt M., 2001 The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89: 1065–1072

   Not in our library10.1161/hh2301.100981

10. 10.

    Barneah O. Benayahu Y. Weis V. M., 2006 Comparative proteomics of symbiotic and aposymbiotic juvenile soft corals. Mar. Biotechnol. (NY) 8: 11–16

    Not in our library10.1007/s10126-004-5120-8

11. 11.

    Barshis D. J. Ladner J. T. Oliver T. A. Seneca F. O. Traylor-Knowles N., 2013 Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci. USA 110: 1387–1392

    Not in our library10.1073/pnas.1210224110

12. 12.
    Symbiodinium Transcriptomes: Genome Insights into the Dinoflagellate Symbionts of Reef-Building Corals · 2012

    No notice
13. 13.

    Bertucci A. Moya A. Tambutté S. Allemand D. Supuran C. T., 2013 Carbonic anhydrases in anthozoan corals—A review. Bioorg. Med. Chem. 21: 1437–1450

    Not in our library10.1016/j.bmc.2012.10.024

14. 14.

    Burkly L. C. Michaelson J. S. Hahm K. Jakubowski A. Zheng T. S., 2007 TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine 40: 1–16

    Not in our library10.1016/j.cyto.2007.09.007

15. 15.

    Burriesci, M. S., 2011 Developing Aiptasia pallida as a tractable model system for cnidarian-dinoflagellate symbiosis: transferred metabolites and designing tools for analysis of ultra-high-throughput-sequencing data. Ph.D. Dissertation, Stanford University, Stanford California.

    Not in our library

16. 16.

    Burriesci M. S. Raab T. K. Pringle J. R., 2012 Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J. Exp. Biol. 215: 3467–3477

    Not in our library10.1242/jeb.070946

17. 17.
    BLAST+: architecture and applications · 2009

    No notice
18. 18.

    Cates N. McLaughlin J. J. A., 1976 Differences of ammonia metabolism in symbiotic and aposymbiotic Condylactus and Cassiopea spp. J. Exp. Mar. Biol. Ecol. 21: 1–5

    Not in our library

19. 19.

    Chu H.-T. Hsiao W. W. L. Chen J.-C. Yeh T.-J. Tsai M.-H., 2013 EBARDenovo: Highly accurate de novo assembly of RNA-Seq with efficient chimera-detection. Bioinformatics 29: 1004–1010

    Not in our library10.1093/bioinformatics/btt092

20. 20.

    Conesa A. Götz S. García-Gómez J. Terol J. Talón M., 2005 Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674

    Not in our library10.1093/bioinformatics/bti610

21. 21.

    Crossland C. Barnes D. Borowitzka M., 1980 Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar. Biol. 60: 81–90

    Not in our library

22. 22.

    D’Aoust B. White R. Wells J. Olsen D., 1976 Coral-algal associations: capacity for producing and sustaining elevated oxygen tensions in situ. Undersea Biomed. Res. 3: 35–40

    Not in our library

23. 23.

    Davidson S. K. Koropatnick T. A. Kossmehl R. Sycuro L. McFall-Ngai M. J., 2004 NO means “yes” in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell. Microbiol. 6: 1139–1151

    Not in our library10.1111/j.1462-5822.2004.00429.x

24. 24.

    Davy S. K. Allemand D. Weis V. M., 2012 Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76: 229–261

    Not in our library10.1128/mmbr.05014-11

25. 25.

    De’ath G. Fabricius K. E. Sweatman H. Puotinen M., 2012 The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl. Acad. Sci. USA 109: 17995–17999

    Not in our library10.1073/pnas.1208909109

26. 26.

    Dennis G. Sherman B. T. Hosack D. A. Yang J. Gao W., 2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4: 3

    Not in our library

27. 27.

    Detournay O. Schnitzler C. E. Poole A. Weis V. M., 2012 Regulation of cnidarian–dinoflagellate mutualisms: evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont. Dev. Comp. Immunol. 38: 525–537

    Not in our library10.1016/j.dci.2012.08.008

28. 28.

    Downs C. A. Fauth J. E. Halas J. C. Dustan P. Bemiss J., 2002 Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 33: 533–543

    Not in our library10.1016/s0891-5849(02)00907-3

29. 29.

    Dudler N. Yellowlees D. Miller D. J., 1987 Localization of two L-glutamate dehydrogenases in the coral Acropora latistella. Arch. Biochem. Biophys. 254: 368–371

    Not in our library10.1016/0003-9861(87)90112-3

30. 30.

    Dunn S. R. Weis V. M., 2009 Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ. Microbiol. 11: 268–276

    Not in our library10.1111/j.1462-2920.2008.01774.x

31. 31.

    Dunn S. R. Bythell J. C. Le Tissier M. D. A. Burnett W. J. Thomason J. C., 2002 Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J. Exp. Mar. Biol. Ecol. 272: 29–53

    Not in our library

32. 32.

    Dunn S. R. Thomason J. C. Le Tissier M. D. A. Bythell J. C., 2004 Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ. 11: 1213–1222

    Not in our library10.1038/sj.cdd.4401484

33. 33.

    Dunn S. R. Phillips W. S. Green D. R. Weis V. M., 2007 Knockdown of actin and caspase gene expression by RNA interference in the symbiotic anemone Aiptasia pallida. Biol. Bull. 212: 250–258

    Not in our library10.2307/25066607

34. 34.

    Dykens J. A. Shick J. M., 1982 Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297: 579–580

    Not in our library

35. 35.

    Edgar R. C., 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797

    Not in our library10.1093/nar/gkh340

36. 36.

    Edgar R. C., 2010 Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461

    Not in our library10.1093/bioinformatics/btq461

37. 37.

    Fitt W. K., 2000 Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. Biol. Bull. 198: 110–120

    Not in our library10.2307/1542809

38. 38.

    Frolov A. Zielinski S. E. Crowley J. R. Dudley-Rucker N. Schaffer J. E., 2003 NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. J. Biol. Chem. 278: 25517–25525

    Not in our library10.1074/jbc.m302588200

39. 39.

    Furla P. Allemand D. Shick J. M. Ferrier-Pagès C. Richier S., 2005 The symbiotic anthozoan: a physiological chimera between alga and animal. Integr. Comp. Biol. 45: 595–604

    Not in our library10.1093/icb/45.4.595

40. 40.

    Ganot P. Moya A. Magnone V. Allemand D. Furla P., 2011 Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet. 7: e1002187

    Not in our library10.1371/journal.pgen.1002187

41. 41.

    Giner J.-L. Wikfors G. H., 2011 “Dinoflagellate sterols” in marine diatoms. Phytochemistry 72: 1896–1901

    Not in our library10.1016/j.phytochem.2011.05.002

42. 42.

    Guedes R. L. M. Prosdocimi F. Fernandes G. R. Moura L. K. Ribeiro H. A. L., 2011 Amino acids biosynthesis and nitrogen assimilation pathways: a great genomic deletion during eukaryotes evolution. BMC Genomics 12(Suppl 4): S2

    Not in our library10.1186/1471-2164-12-s4-s2

43. 43.

    Harland A. D. Bryan G. W. Brown B. E., 1990 Zinc and cadmium absorption in the symbiotic anemone Anemonia viridis and the non-symbiotic anemone Actinia equina. J. Mar. Biol. Assoc. U. K. 70: 789–802

    Not in our library

44. 44.

    Harland A. D. Navarro J. C. Spencer Davies P. Fixter L. M., 1993 Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar. Biol. 117: 113–117

    Not in our library

45. 45.

    Horton P. Park K.-J. Obayashi T. Fujita N. Harada H., 2007 WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35: W585–W587

    Not in our library10.1093/nar/gkm259

46. 46.

    Houten S. M. Wanders R. J. A., 2010 A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J. Inherit. Metab. Dis. 33: 469–477

    Not in our library10.1007/s10545-010-9061-2

47. 47.

    Huang S. Yuan S. Guo L. Yu Y. Li J., 2008 Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res. 18: 1112–1126

    Not in our library10.1101/gr.069674.107

48. 48.

    Huang X. Warren J. T. Buchanan J. Gilbert L. I. Scott M. P., 2007 Drosophila Niemann-Pick type C-2 genes control sterol homeostasis and steroid biosynthesis: a model of human neurodegenerative disease. Development 134: 3733–3742

    Not in our library10.1242/dev.004572

49. 49.

    Hughes T. P. Baird A. Bellwood D. R. Card M. Connolly S. R., 2003 Climate change, human impacts, and the resilience of coral reefs. Science 301: 929–933

    Not in our library10.1126/science.1085046

50. 50.

    Hutton D. M. C. Smith V. J., 1996 Antibacterial properties of isolated amoebocytes from the sea anemone Actinia equina. Biol. Bull. 191: 441–451

    Not in our library10.2307/1543017

51. 51.

    Infante R. E. Wang M. L. Radhakrishnan A. Kwon H. J. Brown M. S., 2008 NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc. Natl. Acad. Sci. USA 105: 15287–15292

    Not in our library10.1073/pnas.0807328105

52. 52.

    Jones R. J. Hoegh-Guldberg O. Larkum A. W. D. Schreiber U., 1998 Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21: 1219–1230

    Not in our library

53. 53.

    Kaldenhoff R., 2012 Mechanisms underlying CO2 diffusion in leaves. Curr. Opin. Plant Biol. 15: 276–281

    Not in our library10.1016/j.pbi.2012.01.011

54. 54.

    Ko D. C. Binkley J. Sidow A. Scott M. P., 2003 The integrity of a cholesterol-binding pocket in Niemann-Pick C2 protein is necessary to control lysosome cholesterol levels. Proc. Natl. Acad. Sci. USA 100: 2518–2525

    Not in our library10.1073/pnas.0530027100

55. 55.

    Kodzius R. Matsumura Y. Kasukawa T. Shimokawa K. Fukuda S., 2004 Absolute expression values for mouse transcripts: re-annotation of the READ expression database by the use of CAGE and EST sequence tags. FEBS Lett. 559: 22–26

    Not in our library10.1016/s0014-5793(04)00018-3

56. 56.
    Evolution of glyoxylate cycle enzymes in Metazoa: evidence of multiple horizontal transfer events and pseudogene formation. · 2006

    No notice
57. 57.

    Kuo J. Chen M.-C. Lin C.-H. Fang L.-S., 2004 Comparative gene expression in the symbiotic and aposymbiotic Aiptasia pulchella by expressed sequence tag analysis. Biochem. Biophys. Res. Commun. 318: 176–186

    Not in our library10.1016/j.bbrc.2004.03.191

58. 58.

    Kuo J. Liang Z. Lin C., 2010 Suppression subtractive hybridization identifies genes correlated to symbiotic and aposymbiotic sea anemone associated with dinoflagellate. J. Exp. Mar. Biol. Ecol. 388: 11–19

    Not in our library

59. 59.

    Kvitt H. Rosenfeld H. Zandbank K. Tchernov D., 2011 Regulation of apoptotic pathways by Stylophora pistillata (Anthozoa, Pocilloporidae) to survive thermal stress and bleaching. PLoS ONE 6: e28665

    Not in our library10.1371/journal.pone.0028665

60. 60.

    Labeit S. Kolmerer B., 1995 Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270: 293–296

    Not in our library10.1126/science.270.5234.293

61. 61.

    Lajeunesse T. Parkinson J. Reimer J., 2012 A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with Cnidaria. J. Phycol. 48: 1380–1391

    Not in our library10.1111/j.1529-8817.2012.01217.x

62. 62.

    Lehnert E. M. Burriesci M. S. Pringle J. R., 2012 Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida. BMC Genomics 13: 271

    Not in our library10.1186/1471-2164-13-271

63. 63.

    Lesser M. P., 1997 Oxidative stress causes coral bleaching during exposure to elevated temperatures. Planta 16: 187–192

    Not in our library

64. 64.

    Lesser M. P., 2006 Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68: 253–278

    Not in our library10.1146/annurev.physiol.68.040104.110001

65. 65.

    Lesser M. P., 2011 Coral bleaching: causes and mechanisms, pp. 405–419 in Coral reefs: an ecosystem in transition, edited by Z. Dubinsky Stambler N. Springer, Amsterdam

    Not in our library

66. 66.

    Li H. Durbin R., 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760

    Not in our library10.1093/bioinformatics/btp324

67. 67.

    Logan D. D. K. LaFlamme A. C. Weis V. M. Davy S. K., 2010 Flow-cytometric characterization of the cell-surface glycans of symbiotic dinoflagellates (Symbiodinium spp.). J. Phycol. 46: 525–533

    Not in our library

68. 68.

    Magoc T. Salzberg S. L., 2011 FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 1–8

    Not in our library10.1093/bioinformatics/btr507

69. 69.

    Martin, M., 2011 Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10–12.

    Not in our library

70. 70.

    Miflin B. J. Habash D. Z., 2002 The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J. Exp. Bot. 53: 979–987

    Not in our library10.1093/jexbot/53.370.979

71. 71.

    Muscatine L. Pool R. R., 1979 Regulation of numbers of intracellular algae. Proc. R. Soc. Lond. B Biol. Sci. 204: 131–139

    Not in our library10.1098/rspb.1979.0018

72. 72.

    Muscatine L. Falkowski P. G. Porter J. W. Dubinsky Z., 1984 Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. Lond. B Biol. Sci. 222: 181–202

    Not in our library

73. 73.
    Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. · 2008

    Not checked
74. 74.

    Nelson R. E. Fessler L. I. Takagi Y. Blumberg B. Keene D. R., 1994 Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 13: 3438–3447

    Not in our library10.1002/j.1460-2075.1994.tb06649.x

75. 75.

    Neumann, M., P. Scheurich, and O. Maier, 2013 Tumour necrosis factors. In: eLS. Chichester. John Wiley.

    Not in our library

76. 76.

    Olano C. T. Bigger C. H., 2000 Phagocytic activities of the gorgonian coral Swiftia exserta. J. Invertebr. Pathol. 76: 176–184

    Not in our library10.1006/jipa.2000.4974

77. 77.

    Palmer C. V. Mydlarz L. D. Willis B. L., 2008 Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc. Biol. Sci. 275: 2687–2693

    Not in our library10.1098/rspb.2008.0335

78. 78.

    Patterson M. J. Landolt M. L., 1979 Cellular reaction to injury in the anthozoan Anthopleura elegantissima. J. Invertebr. Pathol. 33: 189–196

    Not in our library

79. 79.

    Perez S. Weis V., 2006 Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J. Exp. Biol. 209: 2804–2810

    Not in our library10.1242/jeb.02309

80. 80.

    Pernice M. Dunn S. Miard T. Dufour S., 2011 Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PLoS ONE 6: e16095

    Not in our library10.1371/journal.pone.0016095

81. 81.

    Pernice M. Meibom A. Van Den Heuvel A. Kopp C. Domart-Coulon I., 2012 A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J. 6: 1314–1324

    Not in our library10.1038/ismej.2011.196

82. 82.

    Petes L. E. Harvell C. D. Peters E. C. Webb M. A. H. Mullen K. M., 2003 Pathogens compromise reproduction and induce melanization in Caribbean sea fans. Mar. Ecol. Prog. Ser. 264: 167–171

    Not in our library

83. 83.

    Randle P. J., 1998 Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab. Res. Rev. 14: 263–283

    Not in our library10.1002/(sici)1099-0895(199812)14:4<263::aid-dmr233>3.0.co;2-c

84. 84.

    Rees T. A. V., 1986 The green hydra symbiosis and ammonium. I. The role of the host in ammonium assimilation and its possible regulatory significance. Proc. R. Soc. Lond. B Biol. Sci. 229: 299–314

    Not in our library

85. 85.

    Rees T. A. V. Ellard F. M., 1989 Nitrogen conservation and the green hydra symbiosis. Proc. R. Soc. Lond. B Biol. Sci. 236: 203–212

    Not in our library

86. 86.

    Richier S. Sabourault C. Courtiade J. Zucchini N. Allemand D., 2006 Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J. 273: 4186–4198

    Not in our library10.1111/j.1742-4658.2006.05414.x

87. 87.

    Rodrigues C. D. Hannus M. Prudêncio M. Martin C. Gonçalves L. A., 2008 Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4: 271–282

    Not in our library10.1016/j.chom.2008.07.012

88. 88.

    Rodriguez-Lanetty M. Phillips W. S. Weis V. M., 2006 Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7: 23

    Not in our library10.1186/1471-2164-7-23

89. 89.

    Ronquist F. Huelsenbeck J. P., 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574

    Not in our library10.1093/bioinformatics/btg180

90. 90.

    Sabour Alaoui S. Dessirier V. De Araujo E. Alexaki V.-I. Pelekanou V., 2012 TWEAK affects keratinocyte G2/M growth arrest and induces apoptosis through the translocation of the AIF protein to the nucleus. PLoS ONE 7: e33609

    Not in our library10.1371/journal.pone.0033609

91. 91.

    Sabourault C. Ganot P. Deleury E. Allemand D. Furla P., 2009 Comprehensive EST analysis of the symbiotic sea anemone, Anemonia viridis. BMC Genomics 10: 333

    Not in our library10.1186/1471-2164-10-333

92. 92.

    Schoenberg D. A. Trench R. K., 1980 Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc. R. Soc. Lond. B Biol. Sci. 207: 445–460

    Not in our library

93. 93.

    Schulz M. H. Zerbino D. R. Vingron M. Birney E., 2012 Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28: 1086–1092

    Not in our library10.1093/bioinformatics/bts094

94. 94.

    Shinzato C. Shoguchi E. Kawashima T. Hamada M. Hisata K., 2011 Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476: 320–323

    Not in our library10.1038/nature10249

95. 95.

    Shoguchi E. Shinzato C. Kawashima T. Gyoja F. Mungpakdee S., 2013 Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23: 1399–1408

    Not in our library10.1016/j.cub.2013.05.062

96. 96.

    Sinha S. K. Chaudhary P. M., 2004 Induction of apoptosis by X-linked ectodermal dysplasia receptor via a caspase 8-dependent mechanism. J. Biol. Chem. 279: 41873–41881

    Not in our library10.1074/jbc.m407363200

97. 97.

    Sleat D. E. Wiseman J. A. El-Banna M. Price S. M. Verot L., 2004 Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl. Acad. Sci. USA 101: 5886–5891

    Not in our library10.1073/pnas.0308456101

98. 98.

    Sparks A. K., 1985 Synopsis of invertebrate pathology-exclusive of insects. Elsevier Science Publishers BV, Biomedical Division

    Not in our library

99. 99.
    Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont · 2009

    No notice
100. 100.

     Swanson R. Hoegh-Guldberg O., 1998 Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Mar. Biol. 131: 83–93

     Not in our library

101. 101.

     Szmant-Froelich A. Pilson M., 1977 Nitrogen excretion by colonies of the temperate coral Astrangia danae with and without zooxanthellae. Proc.- Int. Coral Reef Symp. 3: 417–424

     Not in our library

102. 102.

     Tchernov D. Kvitt H. Haramaty L. Bibby T. S. Gorbunov M. Y., 2011 Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc. Natl. Acad. Sci. USA 108: 9905–9909

     Not in our library10.1073/pnas.1106924108

103. 103.

     Tolleter D. Seneca F. O. DeNofrio J. C. Krediet C. J. Palumbi S. R., 2013 Coral bleaching independent of photosynthetic activity. Curr. Biol. 23: 1782–1786

     Not in our library10.1016/j.cub.2013.07.041

104. 104.

     Uehlein N. Sperling H. Heckwolf M. Kaldenhoff R., 2012 The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ. 35: 1077–1083

     Not in our library10.1111/j.1365-3040.2011.02473.x

105. 105.

     Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy et al., 2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: RESEARCH0034.

     Not in our library10.1186/gb-2002-3-7-research0034

106. 106.

     Venn A. A. Loram J. E. Douglas A. E., 2008 Photosynthetic symbioses in animals. J. Exp. Bot. 59: 1069–1080

     Not in our library10.1093/jxb/erm328

107. 107.

     Wang J.-T. Douglas A. E., 1998 Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J. Exp. Biol. 201: 2445–2453

     Not in our library10.1242/jeb.201.16.2445

108. 108.

     Wang J.-T. Douglas A. E., 1999 Essential amino acid synthesis and nitrogen recycling in an alga-invertebrate symbiosis. Mar. Biol. 135: 219–222

     Not in our library

109. 109.

     Wang M. L. Motamed M. Infante R. E. Abi-Mosleh L. Kwon H. J., 2010 Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab. 12: 166–173

     Not in our library10.1016/j.cmet.2010.05.016

110. 110.

     Weis V. M., 2008 Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211: 3059–3066

     Not in our library10.1242/jeb.009597

111. 111.

     Weis V. M. Levine R. P., 1996 Differential protein profiles reflect the different lifestyles of symbiotic and aposymbiotic Anthopleura elegantissima, a sea anemone from temperate waters. J. Exp. Biol. 199: 883–892

     Not in our library10.1242/jeb.199.4.883

112. 112.

     Weis V. M. Davy S. K. Hoegh-Guldberg O. Rodriguez-Lanetty M. Pringle J. R., 2008 Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23: 369–376

     Not in our library10.1016/j.tree.2008.03.004

113. 113.

     Whitehead L. F. Douglas A. E., 2003 Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J. Exp. Biol. 206: 3149–3157

     Not in our library10.1242/jeb.00539

114. 114.

     Wright P. A., 1995 Nitrogen excretion: three end products, many physiological roles. J. Exp. Biol. 281: 273–281

     Not in our library10.1242/jeb.198.2.273

115. 115.

     Xiang T. Hambleton E. A. DeNofrio J. C. Pringle J. R. Grossman A. R., 2013 Isolation of clonal, axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J. Phycol. 49: 447–458

     Not in our library10.1111/jpy.12055

116. 116.

     Yalaoui S. Huby T. Franetich J.-F. Gego A. Rametti A., 2008 Scavenger receptor BI boosts hepatocyte permissiveness to Plasmodium infection. Cell Host Microbe 4: 283–292

     Not in our library10.1016/j.chom.2008.07.013

117. 117.

     Yuyama I. Watanabe T. Takei Y., 2011 Profiling differential gene expression of symbiotic and aposymbiotic corals using a high coverage gene expression profiling (HiCEP) analysis. Mar. Biotechnol. (NY) 13: 32–40

     Not in our library10.1007/s10126-010-9265-3

118. 118.

     Zerbino D. R. Birney E., 2008 Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821–829

     Not in our library10.1101/gr.074492.107

119. 119.

     Zhang H. Hou Y. Miranda L. Campbell D. A. Sturm N. R., 2007 Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA 104: 4618–4623

     Not in our library10.1073/pnas.0700258104

120. 120.

     Zhang W. Bae I. Krishnaraju K. Azam N. Fan W., 1999 CR6: A third member in the MyD118 and Gadd45 gene family which functions in negative growth control. Oncogene 18: 4899–4907

     Not in our library10.1038/sj.onc.1202885

121. 121.

     Zhao S. Fernald R. D., 2005 Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12: 1047–1064

     Not in our library10.1089/cmb.2005.12.1047

Cited by papers we hold 3

• Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora · 2021
  Not checked
• Fungi in the Marine Environment: Open Questions and Unsolved Problems · 2019
  No notice
• Generation of clade- and symbiont-specific antibodies to characterize marker molecules during Cnidaria-Symbiodinium endosymbiosis · 2017
  Not checked

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.