Transcriptome analysis of the euryhaline alga, Prymnesium parvum (Prymnesiophyceae): effects of salinity on differential gene expression

REFERENCES

• Alper S.L. 2009. Molecular physiology and genetics of Na+-independent SLC4 anion exchangers. Journal of Experimental Biology 212: 1672–1683.
   Web of Science ®Google Scholar
• Baida G.E. & Kuzmin N.P. 1996. Mechanism of action of hemolysin III from Bacillus cereus. Biochimica et Biophysica Acta Biomembranes 1284: 122–124.
   PubMed Web of Science ®Google Scholar
• Barrowman J., Bhandari D., Reinisch K. & Ferro-novick S. 2010. TRAPP complexes in membrane traffic: convergence through a common Rab. Nature Reviews Molecular Cell Biology 11: 759–763.
   Web of Science ®Google Scholar
• Beszteri S., Yang I., Jaeckisch N., Tillmann U., Frickenhaus S., Glockner G., Gembella A. & John U. 2012. Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (Carter N.) to phosphorus and nitrogen starvation. Harmful Algae 18: 1–15.
   Web of Science ®Google Scholar
• Blüthgen N., Brand K., Čajavec B., Swat M., Herzel H. & Beule D. 2005. Biological profiling of gene groups utilizing gene ontology. Genome Informatics 16: 106–115.
   Google Scholar
• Bock A.K., Glasemacher J., Schmidt R. & Schonheit P. 1999. Purification and characterization of two extremely thermostable enzymes, phosphate acetyltransferase and acetate kinase, from the hyperthermophilic eubacterium Thermotoga maritima. Journal of Bacteriology 181: 1861–1867.
   Web of Science ®Google Scholar
• Conesa A. & Götz S. 2008. Blast2GO: a comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics 2008: 1–13.
   Google Scholar
• Dittami S.M., Gravot A., Goulitquer S., Rousvoal S., Peters A.F., Bouchereau A., Boyen C. & Tonon T. 2012. Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae). Plant Journal 71: 366–377.
   PubMed Web of Science ®Google Scholar
• Donaldson J.G. & Jackson C.L. 2011. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nature Reviews Molecular Cell Biology 12: 533.
   Web of Science ®Google Scholar
• Emanuelsson O., Nielsen H., Brunak S. & Von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300: 1005–1016.
   PubMed Web of Science ®Google Scholar
• Freitag M., Beszteri S., Vogel H. & John U. 2011. Effects of physiological shock treatments on toxicity and polyketide synthase gene expression in Prymnesium parvum (Prymnesiophyceae). European Journal of Phycology 46: 193–201.
   Web of Science ®Google Scholar
• Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., Di Palma F., Birren B.W., Nusbaum C., Lindblad-toh K., Friedman N. & Regev A. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29: 644–652.
   PubMed Web of Science ®Google Scholar
• Grierson D. 1990. Gel electrophoresis of RNA. In: Gel electrophoresis of nucleic acids. A practical approach (Ed. by D. Rickwood & B.D. Hames), pp. 1–49. IRL Press, Oxford, UK.
   Google Scholar
• Guillard R.R.L. & Ryther J.H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology 8: 229–239.
   PubMed Web of Science ®Google Scholar
• Guillaumot D., Guillon S., Deplanque T., Vanhee C., Gumy C., Masquelier D., Morsomme P. & Batoko H. 2009. The Arabidopsis TSPO-related protein is a stress and abscisic acid-regulated, endoplasmic reticulum-Golgi-localized membrane protein. Plant Journal 60: 242–256.
   PubMed Web of Science ®Google Scholar
• Igarashi T., Satake M. & Yasumoto T. 1996. Prymnesin-2: a potent ichthyotoxic and hemolytic glycoside isolated from the red alga Prymnesium parvum. Journal of the American Chemical Society 118: 479–480.
   Web of Science ®Google Scholar
• Jayanta T., Chandra K.M. & Chandra G.B. 2012. Growth, total lipid content and fatty acid profile of a native strain of the freshwater oleaginous microalgae Ankistrodesmus falcatus (Ralf) grown under salt stress condition. International Research Journal of Biological Sciences 1 (8): 27–35.
   Google Scholar
• Kunimoto S., Murofushi W., Kai H., Ishida Y., Uchiyama A., Kobayashi T., Kobayashi S., Murofushi H. & Murakami-murofushi K. 2002. Steryl glucoside is a lipid mediator in stress-responsive signal transduction. Cell Structure & Function 27: 157–162.
   PubMed Web of Science ®Google Scholar
• La Claire J.W., II. 2006. Analysis of expressed sequence tags from the harmful alga, Prymnesium parvum (Prymnesiophyceae, Haptophyta). Marine Biotechnology 8: 534–546.
   PubMed Web of Science ®Google Scholar
• La Claire J.W., II, Manning S.R. & Talarski A.E. 2015. Semi-quantitative assay for polyketide prymnesins isolated from Prymnesium parvum (Haptophyta) cultures. Toxicon 102: 74–80.
   Web of Science ®Google Scholar
• Langmead B., Trapnell C., Pop M. & Salzberg S.L. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25.
   PubMed Web of Science ®Google Scholar
• Li B. & Dewey C.N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
   PubMed Web of Science ®Google Scholar
• Liu C., Wang X., Huang X. & Liu J. 2011. Identification of hypo-osmotically induced genes in Kappaphycus alvarezii (Solieriaceae, Rhodophyta) through expressed sequence tag analysis. Botanica Marina 54: 557–562.
   Web of Science ®Google Scholar
• Liu Z., Jones A.C., Campbell V., Hambright D.K., Keidelberg K.B. & Caron D.A. 2015. Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability. Frontiers in Microbiology 6: 319.
   Web of Science ®Google Scholar
• Lowe C.D., Mello L.V., Samatar N., Martin L.E., Montagnes D.J.S. & Watts P.C. 2011. The transcriptome of the novel dinoflagellate Oxyrrhis marina (Alveolata: Dinophyceae): response to salinity examined by 454 sequencing. BMC Genomics 12: 519.
   Web of Science ®Google Scholar
• Manning S.R. & La Claire J.W. 2010. Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Marine Drugs 8: 678–704.
   PubMed Web of Science ®Google Scholar
• Martin J.A. & Wang Z. 2011. Next-generation transcriptome assembly. Nature Reviews Genetics 12: 671–682.
   PubMed Web of Science ®Google Scholar
• Masuda S., Harada J., Yokono M., Yazawa Y., Shimojima M., Murofushi K., Tanaka H., Masuda H., Murakawa M., Haraguchi T., Kondo M., Nishimura M., Yuasa H., Noguchi M., Oh-oka H., Tanaka A., Tamiaki H. & Ohta H. 2011. A monogalactosyldiacylglycerol synthase found in the green sulfur bacterium Chlorobaculum tepidum reveals important roles for galactolipids in photosynthesis. Plant Cell 23: 2644–2658.
   Web of Science ®Google Scholar
• Moellering E.R., Muthan B. & Benning C. 2010. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330: 226–228.
   PubMed Web of Science ®Google Scholar
• Oliver D.J., Nikolau B.J. & Wurtele E.S. 2009. Acetyl-CoA – life at the metabolic nexus. Plant Science 176: 597–601.
   Web of Science ®Google Scholar
• Pokotylo I., Pejchar P., Potocký M., Kocourková D., Krčková Z., Ruelland E., Kravets V. & Martinec J. 2013. The plant non-specific phospholipase C gene family. Novel competitors in lipid signalling. Progress in Lipid Research 52: 62–79.
   Web of Science ®Google Scholar
• Popov K.M., Kedishvill N.Y. & Harris R.A. 1992. Coenzyme A- and NADH-dependent esterase activity of methylmalonate semialdehyde dehydrogenase. Biochimica et Biophysica Acta 1119: 69–73.
   Google Scholar
• Read B.A., Kegel J., Klute M.J., Kuo A., Lefebvre S.C., Maumus F., Mayer C., Miller J., Monier A., Salamov A., Young J., Aguilar M., Claverie J.M., Frickenhaus S., Gonzalez K., Herman E.K., Lin Y.C., Napier J., Ogata H., Sarno A.F., Shmutz J., Schroeder D., De Vargas C., Verret F., Von Dassow P., Valentin K., Van De Peer Y., Wheeler G., Emiliania Huxleyi Annotation Consortium, Dacks J.B., Delwiche C.F., Dyhrman S.T., Glockner G., John U., Richards T., Worden A.Z., Zhang X. & Grigoriev I.V. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499: 209–213.
   PubMed Web of Science ®Google Scholar
• Renaud S.M. & Parry D.L. 1994. Microalgae for use in tropical aquaculture II: effect of salinity on growth, gross chemical composition and fatty acid composition of three species of marine microalgae. Journal of Applied Phycology 6: 347–356.
   Web of Science ®Google Scholar
• Robinson M.D., Mccarthy D.J. & Smyth G.K. 2009. EdgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.
   PubMed Web of Science ®Google Scholar
• Sambrook J. & Russell D.W. 2006. Purification of nucleic acids by extraction with phenol:chloroform. Cold Spring Harbor Protocols DOI:10.1101/pdb.prot4455.
   Google Scholar
• Schneider C.A., Rasband W.S. & Elicieri K.W. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
   PubMed Web of Science ®Google Scholar
• Schwer B., Bunkenborg J., Verdin R.O., Andersen J.S. & Verdin E. 2006. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proceedings of the National Academy of Sciences USA 103: 10224–10229.
   PubMed Web of Science ®Google Scholar
• Sharma K.K., Schuhmann H. & Schenk P.M. 2012. High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553.
   Web of Science ®Google Scholar
• Silva P. & Geros H. 2009. Regulation by salt of vacuolar H+-ATPase and H+- pyrophosphatase activities and Na+/H+ exchange. Plant Signaling & Behavior 4: 718–726.
   PubMedGoogle Scholar
• Summers P.S., Nolte K.D., Cooper A.J.L., Borgeas H., Leustek T., Rhodes D. & Hanson A.D. 1998. Identification and stereospecificity of the first three enzymes of 3-dimethylsulfoniopropionate biosynthesis in a chlorophyte alga. Plant Physiology 116: 369–378.
   Web of Science ®Google Scholar
• Teo S.S., Ho C.L., Teoh S. & Rahim R.A. 2009. Transcriptomic analysis of Gracilaria changii (Rhodophyta) in response to hyper- and hypoosmotic stresses. Journal of Phycology 45: 1093–1099.
   Web of Science ®Google Scholar
• Thorvaldsdóttir H., Robinson J.T. & Mesirov J.P. 2013. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 14: 178–192.
   PubMed Web of Science ®Google Scholar
• Tuteja R. 2005. Type I signal peptidase: an overview. Archives of Biochemistry and Biophysics 441: 107–111.
   PubMed Web of Science ®Google Scholar
• Van Dolah F.M., Lidie K.B., Monroe E.A., Bhattacharya D., Campbell L., Doucette G.J. & Kamykowski D. 2009. The Florida red tide dinoflagellate Karenia brevis: new insights into cellular and molecular processes underlying bloom dynamics. Harmful Algae 8: 562–572.
   Web of Science ®Google Scholar
• Warmka J., Hanneman J., Lee J., Amin D. & Ota I. 2001. Ptc1, a type 2C ser/thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Molecular & Cellular Biology 21: 51–60.
   Google Scholar
• Weissbach A. & Legrand C. 2012. Effect of different salinities on growth and intra- and extracellular toxicity of four strains of the haptophyte Prymnesium parvum. Aquatic Microbial Ecology 67: 139–149.
   Web of Science ®Google Scholar
• Zhang H., Hou Y., Miranda L., Campbell D.A., Sturm N.R., Gaasterland T. & Lin S. 2007. Spliced leader RNA trans-splicing in dinoflagellates. Proceedings of the National Academy of Sciences USA 104: 4618–4623.
   PubMed Web of Science ®Google Scholar
• Zhang J., Ruhlman T.A., Mower J.P. & Jansen R.K. 2013. Comparative analyses of two Geraniaceae transcriptomes using next-generation sequencing. BMC Plant Biology 13: 228.
   Web of Science ®Google Scholar
• Zhu G., Lagier M.J., Stejskal F., Millership J.J., Cai X. & Keithly J.S. 2002. Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298: 79–89.
   PubMed Web of Science ®Google Scholar