Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types

Marine Genomics

Volumn 15, Issue , 2014, Pages 65-73

  Franssen, Susanne U ^a   Gu, Jenny ^a   Winters, Gidon ^a   Huylmans, Ann Kathrin ^a   Wienpahl, Isabell ^a   Sparwel, Maximiliane ^a   Coyer, James A ^b,d   Olsen, Jeanine L ^b   Reusch, Thorsten B H ^c   Bornberg Bauer, Erich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^d Shoals Marine Laboratory Cornell University ^*  (United States)

Author keywords

Global warming; Heatwave; Inter species transcriptomics; Intra specific variability; RNA seq; Zostera marina and Nanozostera noltii

Indexed keywords

NANOZOSTERA NOLTII; ZOSTERA MARINA;

TRANSCRIPTOME;

DENMARK; GENE EXPRESSION PROFILING; GENETICS; HEAT; ITALY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PLANT GENOME; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; ZOSTERACEAE;

BASE SEQUENCE; DENMARK; GENE EXPRESSION PROFILING; GENOME, PLANT; HOT TEMPERATURE; ITALY; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; ZOSTERACEAE;

EID: 84901951946     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2014.03.004     Document Type: Article

References (79)

1. Ananthan J., Goldberg A.L., Voellmy R. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science (New York, N.Y.) 1986, 232:522-524.
2. Aviezer-Hagai K., Skovorodnikova J., Galigniana M., et al. Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol. Biol. 2007, 63:237-255.
3. Barua D., Heckathorn S.A., Coleman J.S. Variation in heat-shock proteins and photosynthetic thermotolerance among natural populations of Chenopodium album L. from contrasting thermal environments: implications for plant responses to global warming. J. Integr. Plant Biol. 2008, 50:1440-1451.
4. Bergmann N., Winters G., Rauch G., et al. Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming. Mol. Ecol. 2010, 19:2870-2883.
5. Bettencourt B.R., Feder M.E., Cavicchi S. Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster. Evolution 1999, 53:484-492.
6. Billingham M.R., Reusch T.B.H., Alberto F., Serro E.A. Is asexual reproduction more important at geographical limits? A genetic study of the seagrass Zostera marina in the Ria Formosa, Portugal. Mar. Ecol. Prog. Ser. 2003, 265:77-83.
7. Borum J., Duarte C.M., Krause-Jensen D., Greve T.M. European seagrasses: an introduction to monitoring and management. The M&MS project, EU project Monitoring and Managing of European Seagrasses (M&MS) 2004.
8. Bourquin V., Nishikubo N., Abe H., et al. Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell Online 2002, 14:3073-3088.
9. Caspi R., Foerster H., Fulcher C.A., et al. The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2008, 36:D623-D631.
10. Chelaifa H., Mahé F., Ainouche M. Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae). Mol. Ecol. 2010, 19:2050-2063.
11. Coyer J.A., Reusch T.B.H., Stam W.T., et al. Characterization of microsatellite loci in the dwarf eelgrass Zostera noltii (Zosteraceae) and cross-reactivity with Z. japonica. Mol. Ecol. Notes 2004, 4:497-499.
12. Coyer J.A., Hoarau G., Kuo J., et al. Phylogeny and temporal divergence of the seagrass family Zosteraceae using one nuclear and three chloroplast loci. Syst. Biodivers. 2013, 11:271-284.
13. Den Hartog C. Seagrasses of the world. Verhandelingen der koninklijke Nederlandse Akademie van Wetenschappen, Afd. Natuurkunde 1970, 59(1):1-275.
14. Easterling D.R., Meehl G.A., Parmesan C., et al. Climate extremes: observations, modeling, and impacts. Science 2000, 289:2068-2074.
15. Feder M.E., Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 1999, 61:243-282.
16. Feldmeyer B., Wheat C.W., Krezdorn N., Rotter B., Pfenninger M. Short read Illumina data for the de novo assembly of a non-model snail species transcriptome (Radix balthica, Basommatophora, Pulmonata), and a comparison of assembler performance. BMC Genomics 2011, 12:317.
17. Fields P.A. Review: protein function at thermal extremes: balancing stability and flexibility. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 129:417-431.
18. Franssen S.U., Gu J., Bergmann N., et al. Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:19276-19281.
19. Franssen S.U., Shrestha R.P., Bräutigam A., Bornberg-Bauer E., Weber A.P.M. Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing. BMC Genomics 2011, 12:227.
20. Gallo L.I., Lagadari M., Piwien-Pilipuk G., Galigniana M.D. The 90-kDa heat-shock protein (Hsp90)-binding immunophilin FKBP51 is a mitochondrial protein that translocates to the nucleus to protect cells against oxidative stress. J. Biol. Chem. 2011, 286:30152-30160.
21. Gehring W.J., Wehner R. Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proc. Natl. Acad. Sci. 1995, 92:2994-2998.
22. Grabherr M.G., Haas B.J., Yassour M., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29:644-652.
23. Grime J.P. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 1977, 111:1169-1194.
24. Gu J., Weber K., Klemp E., et al. Identifying core features of adaptive metabolic mechanisms for chronic heat stress attenuation contributing to systems robustness. Integr. Biol. 2012, 4(5):480-493.
25. Guttman M., Garber M., Levin J.Z., et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat. Biotechnol. 2010, 28:503-510.
26. Hensel R., König H. Thermoadaptation of methanogenic bacteria by intracellular ion concentration. FEMS Microbiol. Lett. 1988, 49:75-79.
27. Hoffmann A.A., Shirriffs J., Scott M. Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct. Ecol. 2005, 19:222-227.
28. Hofmann G.E., Somero G.N. Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat-shock response and protein ubiquitination. Mar. Biol. 1996, 126:65-75.
29. Jueterbock A., Kollias S., Smolina I., et al. Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: acclimatization potential to climate change. Mar. Genomics 2014, 13:27-36.
30. Kato Y., Aioi K., Omori Y., Takahata N., Satta Y. Phylogenetic analyses of Zostera species based on rbcL and matK nucleotide sequences: implications for the origin and diversification of seagrasses in Japanese waters. Genes Genet. Syst. 2003, 78:329-342.
31. Knight C.A. Small heat shock protein responses differ between chaparral shrubs from contrasting microclimates. J. Bot. 2010, 2010:1-7.
32. Kotak S., Larkindale J., Lee U., et al. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 2007, 10:310-316.
33. Krebs R.A. A comparison of Hsp70 expression and thermotolerance in adults and larvae of three Drosophila species. Cell Stress Chaperones 1999, 4:243-249.
34. Larkindale J., Hall J.D., Knight M.R., Vierling E. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 2005, 138:882-897.
35. Laugier T., Rigollet V., de Casabianca M.-L. Seasonal dynamics in mixed eelgrass beds, Zostera marina L. and Z. noltii Hornem., in a Mediterranean coastal lagoon (Thau lagoon, France). Aquat. Bot. 1999, 63:51-69.
36. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
37. Lohbeck K.T., Riebesell U., Reusch T.B.H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 2012, 5:346-351.
38. Martin J.A., Wang Z. Next-generation transcriptome assembly. Nat. Rev. Genet. 2011, 12:671-682.
39. Martin J.A., Bruno V.M., Fang Z., et al. Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads. BMC Genomics 2010, 11:663.
40. Massa S.I., Arnaud-Haond S., Pearson G.A., Serrao E.A. Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in Southern Europe (Ria Formosa, Portugal). Hydrobiologia 2008, 619:195-201.
41. Massa S.I., Pearson G.A., Aires T., et al. Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution range. Mar. Genomics 2011, 4:181-188.
42. Mazzuca S., Bjork M., Beer S., et al. Establishing research strategies, methodologies and technologies to link genomics and proteomics to seagrass productivity, community metabolism, and ecosystem carbon fluxes. Front. Plant Sci. 2013, 4.
43. McCarthy D.J., Chen Y., Smyth G.K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012, 1-10.
44. Mundry M., Bornberg-Bauer E., Sammeth M., Feulner P.G.D. Evaluating characteristics of de novo assembly software on 454 transcriptome data: a simulation approach. PLoS ONE 2012, 7:e31410.
45. Nejrup L.B., Pedersen M.F. Effects of salinity and water temperature on the ecological performance of Zostera marina. Aquat. Bot. 2008, 88:239-246.
46. Nicolaï M., Duprat A., Sormani R., et al. Higher plant chloroplasts import the mRNA coding for the eucaryotic translation initiation factor 4E. FEBS Lett. 2007, 581:3921-3926.
47. Oetjen K., Reusch T.B.H. Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol. Ecol. 2007, 16:5156-5157.
48. Oksanen J., Blanchet F.G., Kindt R., et al. Vegan: Community Ecology Package 2012.
49. Ouyang S., Zhu W., Hamilton J., et al. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 2007, 35:D883-D887.
50. Phillips R.C., Menez E.G. Seagrasses. Smithsonian Contributions to the Marine Science series, 1988, Smithsonian Institution Press, no. 34, Washington, D.C.
51. Phillips R.C., Stewart Grant W., Peter McRoy C. Reproductive strategies of eelgrass (Zostera marina L.). Aquat. Bot. 1983, 16:1-20.
52. Procaccini G., Beer S., Björk M., et al. Seagrass ecophysiology meets ecological genomics: are we ready?. Mar. Ecol. 2012, 33:522-527.
53. R Development Core Team RFFSC R: A Language and Environment for Statistical Computing. 2008, 1:2673.
54. Reusch T.B.H. Five microsatellite loci in eelgrass Zostera marina and a test of cross-species amplification in Z. noltii and Z. japonica. Mol. Ecol. 2000, 9:371-373.
55. Reusch T.B.H., Ehlers A., Haemmerli A., Worm B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2826-2831.
56. Robertson G., Schein J., Chiu R., et al. De novo assembly and analysis of RNA-seq data. Nat. Methods 2010, 7:909-912.
57. Robinson M.D., Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010, 11:R25.
58. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
59. Schwartz T.S., Tae H., Yang Y., et al. A garter snake transcriptome: pyrosequencing, de novo assembly, and sex-specific differences. BMC Genomics 2010, 11:694.
60. Sørensen J.G. Application of heat shock protein expression for detecting natural adaptation and exposure to stress in natural populations. Curr. Zool. 2010, 56:703-713.
61. Sørensen J.G., Kristensen T.N., Loeschcke V. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 2003, 6:1025-1037.
62. Sørensen J.G., Nielsen M.M., Loeschcke V. Gene expression profile analysis of Drosophila melanogaster selected for resistance to environmental stressors. J. Evol. Biol. 2007, 20:1624-1636.
63. Swarbreck D., Wilks C., Lamesch P., et al. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res. 2008, 36:1009-1014.
64. Trapnell C., Williams B.A., Pertea G., et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
65. Ulmasov K.A., Shammakov S., Karaev K., Evgen'ev M.B. Heat shock proteins and thermoresistance in lizards. Proc. Natl. Acad. Sci. 1992, 89:1666-1670.
66. Usadel B., Nagel A., Steinhauser D., et al. PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinforma. 2006, 7:535.
67. Usadel B., Poree F., Nagel A., et al. A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant Cell Environ. 2009, 32:1211-1229.
68. Vayda M.E., Yuan M.L. The heat shock response of an antarctic alga is evident at 5 degrees C. Plant Mol. Biol. 1994, 24:229-233.
69. Vega-Arreguin J.C., Ibarra-Laclette E., Jimenez-Moraila B., et al. Deep sampling of the Palomero maize transcriptome by a high throughput strategy of pyrosequencing. BMC Genomics 2009, 10:299.
70. Vierling E. The role of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991, 42:579-620.
71. Wahid A., Gelani S., Ashraf M., Foolad M.R. Heat tolerance in plants: an overview. Environ. Exp. Bot. 2007, 61:199-223.
72. Walther G.-R., Post E., Convey P., et al. Ecological responses to recent climate change. Nature 2002, 416:389-395.
73. Wang W., Wang Y., Zhang Q., Qi Y., Guo D. Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. BMC Genomics 2009, 10:465.
74. Whitehead A., Crawford D.L. Neutral and adaptive variation in gene expression. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5425-5430.
75. Wicke S., Schneeweiss G.M., dePamphilis C.W., Müller K.F., Quandt D. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol. Biol. 2011, 76:273-297.
76. Winters G., Nelle P., Fricke B., Rauch G., Reusch T.B.H. Effects of a simulated heat wave on photophysiology and gene expression of high- and low-latitude populations of Zostera marina. Mar. Ecol. Prog. Ser. 2011, 435:83-95.
77. Wissler L., Dattolo E., Moore A.D., et al. Dr. Zompo: an online data repository for Zostera marina and Posidonia oceanica ESTs. Database (Oxford) 2009, 2009:bap009.
78. Yang K.A., Lim C.J., Hong J.K., et al. Identification of cell wall genes modified by a permissive high temperature in Chinese cabbage. Plant Sci. 2006, 171:175-182.
79. Zatsepina O.G., Ulmasov K.A., Beresten S.F., et al. Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation. J. Exp. Biol. 2000, 203:1017-1025.