172
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Gene expression stability of candidate reference genes under different culture conditions for quantitative PCR in the raphidophyte Chattonella marina

, , , , , , , & show all
Pages 556-565 | Received 24 Aug 2019, Accepted 24 Aug 2020, Published online: 29 Sep 2020

REFERENCES

  • Alexander H., Jenkins B.D., Rynearson T.A., Saito M.A., Mercier M.L. & Dyhrman A.T. 2012. Identifying reference genes with stable expression from high throughput sequence data. Frontiers in Microbiology 3: 385. DOI: 10.3389/fmicb.2012.00385.
  • Amano K., Watanabe M., Kohata K. & Harada S. 1998. Conditions necessary for Chattonella antiqua red tide outbreaks. Limnology and Oceanography 43: 117–128. DOI: 10.4319/lo.1998.43.1.0117.
  • Andersen C.L., Jensen J.L. & Ørntoft T.F. 2004. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research 64: 5245–5250. DOI: 10.1158/0008-5472.CAN-04-0496.
  • Aoki K., Onitsuka G., Shimizu M., Yamatogi T., Ishida N., Kitahara K. & Hirano K. 2015. Chattonella (Raphidophyceae) bloom spatio-temporal variations in Tachibana Bay and the southern area of Ariake Sea, Japan: interregional displacement patterns with Skeletonema (Bacillariophyceae). Marine Pollution Bulletin 99: 54–60. DOI: 10.1016/j.marpolbul.2015.07.063.
  • Baier M. & Dietz K.J. 1997. The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. The Plant Journal 12: 179–190. DOI: 10.1046/j.1365-313X.1997.12010179.x.
  • Basti L., Nagai K., Go J., Okano S., Oda T., Tanaka Y. & Nagai S. 2016. Lethal effects of ichthyotoxic raphidophytes, Chattonella marina, C. antiqua, and Heterosigma akashiwo, on post-embryonic stages of the Japanese pearl oyster Pinctada Fucata Martensii. Harmful Algae 59: 112–122. DOI: 10.1016/j.hal.2016.08.003.
  • Botella R.J. & Arteca N.R. 1994. Differential expression of two calmodulin genes in response to physical and chemical stimuli. Plant Molecular Biology 24: 757–766. DOI: 10.1007/BF00029857.
  • Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L. et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611–622. DOI: 10.1373/clinchem.2008.112797.
  • Chen L., Zhong H.Y., Kuang J.F., Li J.G., Lu W.J. & Chen J.Y. 2011. Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234: 377–390. DOI: 10.1007/s00425-011-1410-3.
  • Cho K., Sakamoto J., Noda T., Nishiguchi T., Ueno M., Yamasaki Y., Yagi M., Kim D. & Oda T. 2016. Comparative studies on the fish-killing activities of Chattonella marina isolated in 1985 and Chattonella antiqua isolated in 2010, and their possible toxic factors. Bioscience, Biotechnology, and Biochemistry 80: 811–817. DOI: 10.1080/09168451.2015.1116929.
  • Choi H.J., Kang S.W., Yang C.H., Rhee S.G. & Ryu S.E. 1998. Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution. Nature Structural Biology 5: 400–406. DOI: 10.1038/nsb0598-400.
  • Dekkers B.J., Willems L., Bassel G.W., van Bolderen-veldkamp R.P., Ligterink W., Hilhorst H.W. & Bentsink L. 2012. Identification of reference genes for RT–qPCR expression analysis in Arabidopsis and tomato seeds. Plant & Cell Physiology 53: 28–37. DOI: 10.1093/pcp/pcr113.
  • Deng W.W., Zhang M., Wu J.Q., Jiang Z.Z., Tang L., Li Y.Y., Wei C.L., Jiang C.J. & Wan X.C. 2013. Molecular cloning, functional analysis of three cinnamyl alcohol dehydrogenase (CAD) genes in the leaves of tea plant, Camellia sinensis. Journal of Plant Physiology 170: 272–282. DOI: 10.1016/j.jplph.2012.10.010.
  • Dhanasekaran S., Doherty T.M. & Kenneth J. 2010. Comparison of different standards for real-time PCR-based absolute quantification. Journal of Immunological Methods 354: 34–39. DOI: 10.1016/j.jim.2010.01.004.
  • Galluzzi L., Bertozzini E., Penna A., Perini F., Garcés E. & Magnani M. 2010. Analysis of rRNA gene content in the Mediterranean dinoflagellate Alexandrium catenella and Alexandrium taylori: implications for the quantitative real-time PCR-based monitoring methods. Journal of Applied Phycology 22: 1–9. DOI: 10.1007/s10811-009-9411-3.
  • Gao C., Zhang K., Yang G. & Wang Y. 2012. Expression analysis of four peroxiredoxin genes from Tamarix hispida in response to different abiotic stresses and exogenous abscisic acid (ABA). International Journal of Molecular Science 13: 3751–3764. DOI: 10.3390/ijms13033751.
  • García-Mendoza E., Cáceres-Martínez J., Rivas D., Fimbres-Martinez M., Sánchez-Bravo Y., Vásquez-Yeomans R. & Medina-Elizalde J. 2018. Mass mortality of cultivated northern bluefin tuna Thunnus thynnus orientalis associated with Chattonella species in Baja California, Mexico. Frontiers in Marine Science 5. DOI: 10.3389/fmars.2018.00454.
  • Gong H., Sun L., Chen B., Han Y., Pang J., Wu W., Qi R. & Zhang T.M. 2016. Evaluation of candidate reference genes for RT-qPCR studies in three metabolism related tissues of mice after caloric restriction. Scientific Report 6. DOI: 10.1038/srep38513.
  • Horling F., Lamkemeyer P., König J., Finkemeier I., Kandlbinder A., Baier M. & Dietz K.J. 2003. Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiology 131: 317–325. DOI: 10.1104/pp.010017.
  • Imai I. & Yamaguchi M. 2012. Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella. Harmful Algae 14: 46–70. DOI: 10.1016/j.hal.2011.10.014.
  • Ji N., Li L., Lin L. & Lin S. 2015. Screening for suitable reference genes for quantitative real-time PCR in Heterosigma akashiwo (Raphidophyceae). PLOS One 2. 10: e0132183. DOI: 10.1371/journal.pone.0132183.
  • Jing L.W., Chen S.H., Guo X.L., Zhang H. & Zhao Y.X. 2006. Overexpression of a chloroplast-located peroxiredoxin Q gene, SsPrxQ, increases the salt and low-temperature tolerance of Arabidopsis. Journal of Integrative Plant Biology 48: 1244–1249. DOI: 10.1111/j.1744-7909.2006.00357.x.
  • Jüppner J., Mubeen U., Leisse A., Caldana C., Brust H., Steup M., Herrmann M., Steinhauser D. & Giavalisco P. 2017. Dynamics of lipids and metabolites during the cell cycle of Chlamydomonas reinhardtii.. The Plant Journal 92: 331–343. DOI: 10.1111/tpj.13642.
  • Kevin J.P., Cary S.C. & Warner M.E. 2010. Antioxidant enzyme response and reactive oxygen species production in marine raphidophytes. Journal of Phycology 46: 1161–1171.
  • Kinoshita A., Niwa Y., Onai K., Yamano T., Fukuzawa H., Ishiura M. & Matsuo T. 2017. CSL encodes a leucine-rich-repeat protein implicated in red/violet light signaling to the circadian clock in Chlamydomonas. PLOS Genetics 13. DOI: 10.1371/journal.pgen.1006645.
  • Lee C., Kim J., Shin S.G. & Hwang S. 2006. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. Journal of Biotechnology 123: 273–280. DOI: 10.1016/j.jbiotec.2005.11.014.
  • Maghuly F., Borroto-Fernandez E.G. Khan M.A., Herndl A., Marzban G. & Laimer M. 2009. Expression of calmodulin and lipid transfer protein genes in Prunus incisa x serrula under different stress conditions. Tree Physiology 29: 437–444. DOI: 10.1093/treephys/tpn036.
  • Marshall J.A. & Hallegraeff G.M. 1999. Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) from South Australian and Japanese waters. Journal of Plankton Research 21: 1809–1822. DOI: 10.1093/plankt/21.10.1809.
  • Marshall J.A., Hovenden M., Oda T. & Hallegraeff G.M. 2002. Photosynthesis does influence superoxide production in the ichthyotoxic alga Chattonella marina (Raphidophyceae). Journal of Plankton Research 24: 1231–1236. DOI: 10.1093/plankt/24.11.1231.
  • Marshall J.A., Nichols P.D., Hamilton B., Lewis R.J. & Hallegraeffa J.M. 2003. Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): the synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2: 273–281. DOI: 10.1016/S1568-9883(03)00046-5.
  • Mayo S., Cominelli E., Sparvoli F., González-López O., Rodríguez-González A., Gutiérrez S. & Casquero P.A. 2016. Development of a qPCR strategy to select bean genes involved in plant defense response and regulated by the Trichoderma velutinum – Rhizoctonia solani interaction. Frontiers in Plant Science 7: 1109. DOI: 10.3389/fpls.2016.01109.
  • McCurley A.T. & Callard G.V. 2008. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Molecular Biology 9: 102. DOI: 10.1186/1471-2199-9-102.
  • Mittler R., Vanderauwera S., Gollery M. & Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science 9: 490–498. DOI: 10.1016/j.tplants.2004.08.009.
  • Mukai K., Shimasaki Y., Qiu X., Kato-Unoki Y., Chen K., Khanam M.R.M. & Oshima Y. 2019. Effects of light and hydrogen peroxide on gene expression of newly identified antioxidant enzymes in the harmful algal bloom species Chattonella marina. European Journal of Phycology 54: 393–403. DOI: 10.1080/09670262.2019.1576062.
  • Mukai K., Teramoto A., Qiu X., Shimasaki Y., Kato-Unoki Y., Lee J.M., Mizoguchi M., Khanam M.R.M., Satone H., Tatsuke T. et al. 2018. Gene structure and cDNA sequence of 2-Cys peroxiredoxin in the harmful algal bloom species Chattonella marina and its gene transcription under different light intensities. European Journal of Phycology 53: 29–38. DOI: 10.1080/09670262.2017.1346206.
  • Oda T., Nakamura A., Shikayama M., Kawano I., Ishimatsu A. & Muramatsu T. 1997. Generation of reactive oxygen species by raphidophycean phytoplankton. Bioscience, Biotechnology, and Biochemistry 61: 1658–1662. DOI: 10.1271/bbb.61.1658.
  • Ohmiya A., Hirashima M., Yagi M., Tanase K. & Yamamizo C. 2014. Identification of genes associated with chlorophyll accumulation in flower petals. PLOS One 9: e113738. DOI: 10.1371/journal.pone.0113738.
  • Okaichi T. 1997. Red tides in the Seto Inland Sea. Sustainable development in the Seto Inland Sea, Japan. Terra Scientific Publishing Company (TERRAPUB), Tokyo. 251–304 pp.
  • Onitsuka G., Aoki K., Matsuyama Y., Kimoto K., Matsuo H., Kitadai Y., Nishi H., Tahara Y. & Sakurada K. 2011. Short-term dynamics of a Chattonella antiqua bloom in the Yatsushiro Sea, Japan, in summer 2010: characteristics of its appearance in the southern area. Japanese Society of Fisheries Oceanography 75: 143.
  • Pfaffl M.W., Tichopad A., Prgomet C. & Neuvians T.P. 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestKeeper–Excel-based tool using pair-wise correlations. Biotechnology Letters 6: 509–515. DOI: 10.1023/B:BILE.0000019559.84305.47.
  • Qiu X., Chen C., Shimasaki Y., Mukai K., Teramoto A., Wu M. & Oshima Y. 2020. Time-series responses in photosynthetic activity, 2-cysteine peroxiredoxin gene expression, and proteomics of Chattonella marina var. antiqua under different oxidative stress. Harmful Algae 94. DOI: 10.1016/j.hal.2020.101808.
  • Qiu X., Shimasaki Y., Tsuyama M., Yamada T., Kuwahara R., Kawaguchi M., Honda M., Gunjikake H., Tasmin R., Shimizu M. et al. 2013. Growth-phase dependent variation in photosynthetic activity and cellular protein expression profile in the harmful raphidophyte Chattonella antiqua. Bioscience, Biotechnology, and Biochemistry 77: 46–52. DOI: 10.1271/bbb.120543.
  • Qiu X., Wu M., Mukai K., Shimasaki Y. & Oshima Y. 2019. Effects of elevated irradiance, temperature, and rapid shifts of salinity on the chlorophyll a fluorescence (OJIP) transient of Chattonella marina var. antiqua. Journal of the Faculty of Agriculture, Kyushu University 64: 293–300.
  • Rudd J.J. & Franklin-Tong V.E. 2001. Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytologist 151: 7–33. DOI: 10.1046/j.1469-8137.2001.00173.x.
  • Ruiz-Villalba A., Mattiotti A., Gunst Q.D., Cano-Ballesteros S., van den Hoff M.J. & Ruijter J.M. 2017. Reference genes for gene expression studies in the mouse heart. Scientific Reports 7: 24. DOI: 10.1038/s41598-017-00043-9.
  • Rydbirk R., Folke J., Winge K., Aznar S., Pakkenberg B. & Brudek T. 2016. Assessment of brain reference genes for RT-qPCR studies in neurodegenerative diseases. Scientific Reports 6. DOI: 10.1038/srep37116.
  • Silver N., Best S., Jiang J. & Thein S.L. 2006. Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Molecular Biology 7: 33. DOI: 10.1186/1471-2199-7-33.
  • Snedden W.A. & Fromm H. 2001. Calmodulin as a versatile calcium signal transducer in plants. New Phytologist 151: 35–66.
  • Tiffany M.A., Barlow S.B., Matey V.E. & Hurlbert S.H. 2001. Chattonella marina (Raphidophyceae), a potentially toxic alga in the Salton Sea, California. Hydrobiologia 466: 187–194. DOI: 10.1023/A:1014503920898.
  • Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. & Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: research0034.1. DOI: 10.1186/gb-2002-3-7-research0034.
  • von Gromoff E.D., Alawady A., Meinecke L., Grimm B. & Beck C.F. 2008. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. The Plant Cell 20: 552–567. DOI: 10.1105/tpc.107.054650.
  • Waite A.M. & Lindahl O. 2006. Bloom and decline of the toxic flagellate Chattonella marina in a Swedish fjord. Marine Ecology Progress Series 326: 77–83. DOI: 10.3354/meps326077.
  • Wang Y., Bouchard J.N. & Coyne K.J. 2018. Expression of novel nitrate reductase genes in the harmful alga Chattonella subsalsa. Scientific Reports 8: 13417. DOI: 10.1038/s41598-018-31735-5.
  • Yamasaki Y., Nagasoe S., Matsubara T., Shikata T., Shimasaki Y., Oshima Y. & Honjo T. 2007. Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series 339: 83–92. DOI: 10.3354/meps339083.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.