Molecular characterization of heat shock protein 90 from the dinoflagellate Prorocentrum donghaiense and its transcriptional response to thermal, copper and nutrient stresses

References

• Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 25:3389–3402. doi: 10.1093/nar/25.17.3389
   PubMed Web of Science ®Google Scholar
• Bachvaroff TR, Gornik SG, Concepcion GT, Waller RF, Mendez GS, Lippmeier JC, Delwiche CF. 2014. Dinoflagellate phylogeny revisited: using ribosomal proteins to resolve deep branching dinoflagellate clades. Molecular Phylogenetics and Evolution. 70:314–322. doi: 10.1016/j.ympev.2013.10.007
   PubMed Web of Science ®Google Scholar
• Beszteri S, Yang I, Jaeckisch N, Tillmann U, Frickenhaus S, Glöckner G, Cembella A, John U. 2012. Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation. Harmful Algae. 18:1–15. doi: 10.1016/j.hal.2012.03.003
   Web of Science ®Google Scholar
• Boopathi T, Faria DG, Cheon JY, Youn SH, Ki JS. 2015. Implications of high molecular divergence of nuclear rRNA and phylogenetic structure for the dinoflagellate Prorocentrum (Dinophyceae, Prorocentrales). Journal of Eukaryotic Microbiology. 62:519–531. doi: 10.1111/jeu.12206
   PubMed Web of Science ®Google Scholar
• Burkholder JM, Glibert PM, Skelton HM. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae. 8:77–93. doi: 10.1016/j.hal.2008.08.010
   Web of Science ®Google Scholar
• Castro D, Vera D, Lagos N, García C, Vásquez M. 2004. The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon. 44:483–489. doi: 10.1016/j.toxicon.2004.06.005
   PubMed Web of Science ®Google Scholar
• Chai C, Yin X, Ge W, Wang J. 2013. Effects of nitrogen and phosphorus concentrations on the bioaccumulation of polybrominated diphenyl ethers by Prorocentrum donghaiense. Journal of Environmental Sciences. 25:376–385. doi: 10.1016/S1001-0742(12)60026-6
   Google Scholar
• Deng Y, Hu Z, Zhan Z, Ma Z, Tang Y. 2015. Differential expressions of an Hsp70 gene in the dinoflagellate Akashiwo sanguinea in response to temperature stress and transition of life cycle and its implications. Harmful Algae. 50:57–64. doi: 10.1016/j.hal.2015.10.007
   Web of Science ®Google Scholar
• Dyhrman ST, Haley ST, Birkeland SR, Wurch LL, Cipriano MJ, McArthur AG. 2006. Long serial analysis of gene expression for gene discovery and transcriptome profiling in the widespread marine coccolithophore Emiliania huxleyi. Applied and Environmental Microbiology. 72:252–260. doi: 10.1128/AEM.72.1.252-260.2006
   PubMed Web of Science ®Google Scholar
• Farcy E, Serpentini A, Fiévet B, Lebel JM. 2007. Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 146:540–550. doi: 10.1016/j.cbpb.2006.12.006
   PubMed Web of Science ®Google Scholar
• Fast NM, Xue L, Bingham S, Keeling PJ. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. The Journal of Eukaryotic Microbiology. 49:30–37. doi: 10.1111/j.1550-7408.2002.tb00336.x
   PubMed Web of Science ®Google Scholar
• Feng PM, Chen W, Lin H, Chou KC. 2013. iHSP-PseRAAAC: identifying the heat shock protein families using pseudo reduced amino acid alphabet composition. Analytical Biochemistry. 442:118–125. doi: 10.1016/j.ab.2013.05.024
   PubMed Web of Science ®Google Scholar
• Flynn K, Franco JM, Fernández P, Reguera B, Zapata M, Wood G, Flynn KL. 1994. Changes in toxin content, biomass and pigments of the dinoflagellate Alexandrium minutum during nitrogen refeeding and growth into nitrogen or phosphorus stress. Marine Ecology Progress Series. 111:99–109. doi: 10.3354/meps111099
   Web of Science ®Google Scholar
• Fu FX, Place AR, Garcia NS, Hutchins DA. 2010. CO2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum. Aquatic Microbial Ecology. 59:55–65. doi: 10.3354/ame01396
   Web of Science ®Google Scholar
• Fu FX, Tatters AO, Hutchins DA. 2012. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series. 470:207–233. doi: 10.3354/meps10047
   Web of Science ®Google Scholar
• Gaetke LM, Chow CK. 2003. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology. 189:147–163. doi: 10.1016/S0300-483X(03)00159-8
   PubMed Web of Science ®Google Scholar
• Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD, Bairoch A. 2005. In: Walker JM, editor. The proteomics protocols handbook. Totowa, NJ: Humana Press, p. 571–607.
   Google Scholar
• Gobler CJ, Burkholder JM, Davis TW, Harke MJ, Johengen T, Stow CA, Van de Waal DB. 2016. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae. 54:87–97. doi: 10.1016/j.hal.2016.01.010
   PubMed Web of Science ®Google Scholar
• Guillard RR. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH, editors. Culture of marine invertebrate animals. New York: Plenum Press, p. 26–60.
   Google Scholar
• Guo R, Lee MA, Ki JS. 2013. Different transcriptional responses of heat shock protein 70/90 in the marine diatom Ditylum brightwellii exposed to metal compounds and endocrine-disrupting chemicals. Chemosphere. 92:535–543. doi: 10.1016/j.chemosphere.2013.03.052
   PubMed Web of Science ®Google Scholar
• Guo RY, Youn SH, Ki JS. 2015. Heat Shock Protein 70 and 90 Genes in the Harmful Dinoflagellate Cochlodinium polykrikoides: Genomic Structures and Transcriptional Responses to Environmental Stresses. Int J Genomics. 2015:484626.
   Google Scholar
• Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK. 2010. Heat shock proteins in toxicology: how close and how far? Life Sciences. 86:377–384. doi: 10.1016/j.lfs.2009.12.015
   PubMed Web of Science ®Google Scholar
• Han MS, Wang P, Kim JH, Cho SY, Park BS, Kim JH, Katano T, Kim BH. 2016. Morphological and molecular phylogenetic position of Prorocentrum micans sensu stricto and description of Prorocentrum koreanum sp. nov. from Southern Coastal Waters in Korea and Japan. Protist. 167:32–50. doi: 10.1016/j.protis.2015.12.001
   PubMed Web of Science ®Google Scholar
• Hardison DR, Sunda WG, Shea D, Litaker RW. 2013. Increased toxicity of Karenia brevis during phosphate limited growth: ecological and evolutionary implications. PLoS One. 8:e58545. doi: 10.1371/journal.pone.0058545
   PubMed Web of Science ®Google Scholar
• Hernández I, Niell FX, Whitton BA. 2002. Phosphatase activity of benthic marine algae. An overview. Journal of Applied Phycology. 14:475–487. doi: 10.1023/A:1022370526665
   Web of Science ®Google Scholar
• Hoppenrath M, Leander BS. 2010. Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS One. 5:e13220. doi: 10.1371/journal.pone.0013220
   PubMed Web of Science ®Google Scholar
• Hu Z, Duan S, Xu N, Mulholland MR. 2014. Growth and nitrogen uptake kinetics in cultured Prorocentrum donghaiense. PLoS One. 9:e94030. doi: 10.1371/journal.pone.0094030
   PubMed Web of Science ®Google Scholar
• Hu Z, Mulholland MR, Xu N, Duan S. 2016. Effects of temperature, irradiance and pCO2 on the growth and nitrogen utilization of Prorocentrum donghaiense. Aquatic Microbial Ecology. 77:155–166. doi: 10.3354/ame01793
   Web of Science ®Google Scholar
• Huang B, Ou L, Hong H, Luo H, Wang D. 2005. Bioavailability of dissolved organic phosphorus compounds to typical harmful dinoflagellate Prorocentrum donghaiense Lu. Marine Pollution Bulletin. 51:838–844. doi: 10.1016/j.marpolbul.2005.02.035
   PubMed Web of Science ®Google Scholar
• Kang LK, Hwang SPL, Gong GC, Lin HJ, Chen PC, Chang J. 2007. Influences of nitrogen deficiency on the transcript levels of ammonium transporter, nitrate transporter and glutamine synthetase genes in Isochrysis galbana (Isochrysidales, Haptophyta). Phycologia. 46:521–533. doi: 10.2216/06-44.1
   Web of Science ®Google Scholar
• Kobiyama A, Tanaka S, Kaneko Y, Lim PT, Ogata T. 2010. Temperature tolerance and expression of heat shock protein 70 in the toxic dinoflagellate Alexandrium tamarense (Dinophyceae). Harmful Algae. 9:180–185. doi: 10.1016/j.hal.2009.09.002
   Web of Science ®Google Scholar
• Lai JX, Yu ZM, Song XX, Cao XH, Han XT. 2011. Responses of the growth and biochemical composition of Prorocentrum donghaiense to different nitrogen and phosphorus concentrations. Journal of Experimental Marine Biology and Ecology. 405:6–17. doi: 10.1016/j.jembe.2011.05.010
   Web of Science ®Google Scholar
• Legrand C, Graneli G, Carlsson P. 1998. Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra. Aquatic Microbial Ecology. 15:65–75. doi: 10.3354/ame015065
   Web of Science ®Google Scholar
• Li M, Li L, Shi X, Lin L, Lin S. 2015. Effects of phosphorus deficiency and adenosine 5′-triphosphate (ATP) on growth and cell cycle of the dinoflagellate Prorocentrum donghaiense. Harmful Algae. 47:35–41. doi: 10.1016/j.hal.2015.05.013
   Web of Science ®Google Scholar
• Li R, Chen GZ, Tam NFY, Luan TG, Shin PK, Cheung SG, Liu Y. 2009. Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotoxicology and Environmental Safety. 72:321–328. doi: 10.1016/j.ecoenv.2008.05.012
   PubMed Web of Science ®Google Scholar
• Li Y, Lü S, Jiang T, Xiao Y, You S. 2011. Environmental factors and seasonal dynamics of Prorocentrum populations in Nanji Islands National Nature Reserve, East China Sea. Harmful Algae. 10:426–432. doi: 10.1016/j.hal.2010.08.002
   Web of Science ®Google Scholar
• Lin X, Zhang H, Huang B, Lin S. 2011. Alkaline phosphatase gene sequence and transcriptional regulation by phosphate limitation in Amphidinium carterae (Dinophyceae). Journal of Phycology. 47:1110–1120. doi: 10.1111/j.1529-8817.2011.01038.x
   PubMed Web of Science ®Google Scholar
• Liu JS, Yang WD, Chen ZL. 2007. Inhibitory effect of acetone extract from Eichhornia crassipes roots on Prorocentrum donghaiense Lu and its mechanism. Journal of Oceanography. 24:84–88.
   Google Scholar
• Liu Z, Zhang L, Pu Y, Liu Z, Li Z, Zhao Y, Qin S. 2014. Cloning and expression of a Cytosolic HSP90 gene in Chlorella vulgaris. Biomed Research International. 140:187–220.
   Google Scholar
• Lou X, Hu C. 2014. Diurnal changes of a harmful algal bloom in the East China Sea: observations from GOCI. Remote Sensing of Environment. 140:562–572. doi: 10.1016/j.rse.2013.09.031
   Web of Science ®Google Scholar
• Lu D, Goebel J, Qi Y, Zou J, Han X, Gao Y, Li Y. 2005. Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae. 4:493–505. doi: 10.1016/j.hal.2004.08.015
   Web of Science ®Google Scholar
• Morales M, Planelló R, Martínez-Paz P, Herrero O, Cortés E, Martínez-Guitarte JL, Morcillo G. 2011. Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 153:150–158.
   PubMed Web of Science ®Google Scholar
• Morey JS, Monroe EA, Kinney AL, Beal M, Johnson JG, Hitchcock GL, Van Dolah FM. 2011. Transcriptomic response of the red tide dinoflagellate, Karenia brevis, to nitrogen and phosphorus depletion and addition. BMC Genomics. 12:346. doi: 10.1186/1471-2164-12-346
   PubMed Web of Science ®Google Scholar
• Ou L, Huang X, Huang B, Qi Y, Lu S. 2015. Growth and competition for different forms of organic phosphorus by the dinoflagellate Prorocentrum donghaiense with the dinoflagellate Alexandrium catenella and the diatom Skeletonema costatum s.l. Hydrobiologia. 754:29–41. doi: 10.1007/s10750-014-1994-2
   Web of Science ®Google Scholar
• Pistocchi R, Pezzolesi L, Guerrini F, Vanucci S, Dell’Aversano C, Fattorusso E. 2011. A review on the effects of environmental conditions on growth and toxin production of Ostreopsis ovata. Toxicon. 57:421–428. doi: 10.1016/j.toxicon.2010.09.013
   PubMed Web of Science ®Google Scholar
• Pratt WB, Morishima Y, Peng HM, Osawa Y. 2010. Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Experimental Biology and Medicine. 235:278–289. doi: 10.1258/ebm.2009.009250
   PubMed Web of Science ®Google Scholar
• Ras M, Steyer JP, Bernard O. 2013. Temperature effect on microalgae: a crucial factor for outdoor production. Reviews in Environmental Science and Bio/Technology. 12:153–164. doi: 10.1007/s11157-013-9310-6
   Web of Science ®Google Scholar
• Rombel IT, Sykes KF, Rayner S, Johnston SA. 2002. ORF-FINDER: a vector for high-throughput gene identification. Gene. 282:33–41. doi: 10.1016/S0378-1119(01)00819-8
   PubMed Web of Science ®Google Scholar
• Rosic NN, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O. 2011. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress and Chaperones. 16:69–80. doi: 10.1007/s12192-010-0222-x
   PubMed Web of Science ®Google Scholar
• Roy JS, Poulson-Ellestad KL, Sieg RD, Poulin RX, Kubanek J. 2013. Chemical ecology of the marine plankton. Natural Product Reports. 30:1364–1379. doi: 10.1039/c3np70056a
   PubMed Web of Science ®Google Scholar
• Sano J, Kato KH. 2009. Localization and copy number of the protein-coding genes actin, α-tubulin, and HSP90 in the nucleus of a primitive dinoflagellate, Oxyrrhis marina. Zoological Science. 26:745–753. doi: 10.2108/zsj.26.745
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW. 2000. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Analytical Biochemistry. 285:194–204. doi: 10.1006/abio.2000.4753
   PubMed Web of Science ®Google Scholar
• Sgherri C, Quartacci MF, Navari-Izzo F. 2007. Early production of activated oxygen species in root apoplast of wheat following copper excess. Journal of Plant Physiology. 164:1152–1160. doi: 10.1016/j.jplph.2006.05.020
   PubMed Web of Science ®Google Scholar
• Shalchian-Tabrizi K, Minge MA, Cavalier-Smith T, Nedreklepp JM, Klaveness D, Jakobsen KS. 2006. Combined heat shock protein 90 and ribosomal RNA sequence phylogeny supports multiple replacements of dinoflagellate platastids. Journal of Eukaryotic Microbiology. 53:217–224. doi: 10.1111/j.1550-7408.2006.00098.x
   PubMed Web of Science ®Google Scholar
• Shen A, Xing X, Li D. 2015. Allelopathic effects of Prorocentrum donghaiense and Karenia mikimotoi on each other under different temperature. Thalassas. 31:33–49.
   Web of Science ®Google Scholar
• Shi X, Li L, Guo C, Lin X, Li M, Lin S. 2015. Rhodopsin gene expression regulated by the light dark cycle, light spectrum and light intensity in the dinoflagellate Prorocentrum. Frontiers in Microbiology. 6:555. doi: 10.3389/fmicb.2015.00555
   PubMed Web of Science ®Google Scholar
• Shi X, Zhang H, Lin S. 2013. Tandem repeats, high copy number and remarkable diel expression rhythm of form II RuBisCO in Prorocentrum donghaiense (Dinophyceae). PLoS One. 8:e71232. doi: 10.1371/journal.pone.0071232
   PubMed Web of Science ®Google Scholar
• Sørensen JG, Kristensen TN, Loeschcke V. 2003. The evolutionary and ecological role of heat shock proteins. Ecology Letters. 6:1025–1037. doi: 10.1046/j.1461-0248.2003.00528.x
   Web of Science ®Google Scholar
• Stauber JL, Andrade S, Ramirez M, Adams MCJA, Correa JA. 2005. Copper bioavailability in a coastal environment of Northern Chile: comparison of bioassay and analytical speciation approaches. Marine Pollution Bulletin. 50:1363–1372. doi: 10.1016/j.marpolbul.2005.05.008
   PubMed Web of Science ®Google Scholar
• Tang D, Di B, Wei G, Ni IH, Wang S. 2006. Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia. 568:245–253. doi: 10.1007/s10750-006-0108-1
   Web of Science ®Google Scholar
• Tao B, Pan D, Mao Z, Shen Y, Zhu Q, Chen J. 2013. Optical detection of Prorocentrum donghaiense blooms based on multispectral reflectance. Acta Oceanologica Sinica. 32:48–56. doi: 10.1007/s13131-013-0365-6
   Web of Science ®Google Scholar
• Terasawa K, Minami M, Minami Y. 2005. Constantly updated knowledge of Hsp90. Journal of Biochemistry. 137:443–447. doi: 10.1093/jb/mvi056
   PubMed Web of Science ®Google Scholar
• Vanucci S, Pezzolesi L, Pistocchi R, Ciminiello P, Dell’ Aversano C, Iacovo ED, Guerrini F. 2012. Nitrogen and phosphorus limitation effects on cell growth, biovolume, and toxin production in Ostreopsis cf. ovata. Harmful Algae. 15:78–90. doi: 10.1016/j.hal.2011.12.003
   Web of Science ®Google Scholar
• Wang Q, Zhu L, Wang D. 2014. A numerical model study on multi-species harmful algal blooms coupled with background ecological fields. Acta Oceanologica Sinica. 33:95–105.
   Web of Science ®Google Scholar
• Wang R, Xiao H, Wang Y, Zhou W, Tang X. 2007. Effects of three macroalgae, Ulva linza (Chlorophyta), Corallina pilulifera (Rhodophyta) and Sargassum thunbergii (Phaeophyta) on the growth of the red tide microalga Prorocentrum donghaiense under laboratory conditions. Journal of Sea Research. 58:189–197. doi: 10.1016/j.seares.2007.03.002
   Web of Science ®Google Scholar
• Wang Y, Yu Z, Song X, Zhang S. 2006. Interactions between the bloom-forming dinoflagellates Prorocentrum donghaiense and Alexandrium tamarense in laboratory cultures. Journal of Sea Research. 56:17–26. doi: 10.1016/j.seares.2006.04.002
   Web of Science ®Google Scholar
• Watanabe M, Kohata K, Kunugi M. 1987. Nuclear magnetic resonance study of intracellular phosphate pools and polyphosphate metabolism in Heterosigma akashiwo (raphidophyceae). Journal of Phycology. 23:54–62. doi: 10.1111/j.0022-3646.1987.00054.x
   Web of Science ®Google Scholar
• Wei Y, Zhu N, Lavoie M, Wang J, Qian H, Fu Z. 2014. Copper toxicity to Phaeodactylum tricornutum: a survey of the sensitivity of various toxicity endpoints at the physiological, biochemical, molecular and structural levels. Biometals. 27:527–537. doi: 10.1007/s10534-014-9727-6
   PubMed Web of Science ®Google Scholar
• Wurch LL, Haley ST, Orchard ED, Gobler CJ, Dyhrman ST. 2011. Nutrient regulated transcriptional responses in the brown tide-forming alga Aureococcus anophagefferens. Environmental Microbiology. 13:468–481. doi: 10.1111/j.1462-2920.2010.02351.x
   PubMed Web of Science ®Google Scholar
• Xu N, Duan S, Li A, Zhang C, Cai Z, Hu Z. 2010. Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae. 9:13–17. doi: 10.1016/j.hal.2009.06.002
   Web of Science ®Google Scholar
• Yang I, Beszteri S, Tillmann U, Cembella A, John U. 2011. Growth- and nutrient- dependent gene expression in Alexandrium minutum. Harmful Algae. 12:55–69. doi: 10.1016/j.hal.2011.08.012
   Web of Science ®Google Scholar
• Young JC, Moarefi I, Hartl FU. 2001. Hsp90: a specialized but essential protein-folding tool. The Journal of Cell Biology. 154:267–274. doi: 10.1083/jcb.200104079
   PubMed Web of Science ®Google Scholar
• Zhang C, Lin SJ, Huang LM, Lu W, Li MZ, Liu S. 2014. Suppression subtraction hybridization analysis revealed regulation of some cell cycle and toxin genes in Alexandrium catenella by phosphate limitation. Harmful Algae. 39:26–39. doi: 10.1016/j.hal.2014.06.005
   Web of Science ®Google Scholar
• Zhang J, Hou Y, Miranda L, Campbell D, Sturm NR, Gaasterland T, Lin S. 2007. Spliced leader RNA trans-splicing in dinoflagellates. Proceedings of the National Academy of Sciences. 104:4618–4623. doi: 10.1073/pnas.0700258104
   PubMed Web of Science ®Google Scholar
• Zhang L, Fan Y, Shi F, Qin S, Liu B. 2012. Molecular cloning, characterization, and expression analysis of a cytosolic HSP90 gene from Haematococcus pluvialis. Journal of Applied Phycology. 24:1601–1612. doi: 10.1007/s10811-012-9821-5
   Web of Science ®Google Scholar
• Zhang YJ, Zhang SF, He ZP, Lin L, Wang DZ. 2015. Proteomic analysis provides new insights into the adaptive response of a dinoflagellate Prorocentrum donghaiense to changing ambient nitrogen. Plant, Cell & Environment. 38:2128–2142. doi: 10.1111/pce.12538
   PubMed Web of Science ®Google Scholar
• Zhao LY, Mi TZ, Zhen Y, Li MY, He SY, Sun J, Yu ZG. 2009. Cloning of proliferating cell nuclear antigen gene from the dinoflagellate Prorocentrum donghaiense and monitoring its expression profiles by real-time RT-PCR. Hydrobiologia. 627:19–30. doi: 10.1007/s10750-009-9712-1
   Web of Science ®Google Scholar
• Zhou C, Place AR, Yan X, Xu J, Luo Q, William E, Jiang Y. 2015. Interactions between Karlodinium veneficum and Prorocentrum donghaiense from the East China Sea. Harmful Algae. 49:50–57. doi: 10.1016/j.hal.2015.08.004
   PubMed Web of Science ®Google Scholar
• Zhou MJ, Zhu MY. 2006. Progress of the project “Ecology and oceanography of harmful algal blooms in China”. Advances in Earth Science. 21:673–679.
   Google Scholar
• Zhuang Y, Zhang H, Lin S. 2013. Cyclin B gene and its cell cycle-dependent differential expression in the toxic dinoflagellate Alexandrium fundyense Atama group I/clade I. Harmful Algae. 26:71–79. doi: 10.1016/j.hal.2013.04.002
   Web of Science ®Google Scholar