Volume 41 Issue 8
Aug.  2022
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Shufeng Zhang, Yue Wu, Lin Lin, Dazhi Wang. Molecular insights into the circadian clock in marine diatoms[J]. Acta Oceanologica Sinica, 2022, 41(8): 87-98. doi: 10.1007/s13131-021-1962-4
Citation: Shufeng Zhang, Yue Wu, Lin Lin, Dazhi Wang. Molecular insights into the circadian clock in marine diatoms[J]. Acta Oceanologica Sinica, 2022, 41(8): 87-98. doi: 10.1007/s13131-021-1962-4

Molecular insights into the circadian clock in marine diatoms

doi: 10.1007/s13131-021-1962-4
Funds:  The National Natural Science Foundation of China under contract Nos 41425021 and 41706131; the National Key Research and Development Program of China under contract No. 2017YFC1404302; the “Ten Thousand Talents Program” for Leading Talents in Science and Technological Innovation to Dazhi Wang.
More Information
  • Corresponding author: E-mail: dzwang@xmu.edu.cn
  • Received Date: 2021-10-06
  • Accepted Date: 2021-11-18
  • Available Online: 2022-04-28
  • Publish Date: 2022-08-15
  • The circadian clock is a fundamental endogenous mechanism of adaptation that coordinates the physiology and behavior of most organisms with diel variations in the external environment to maintain temporal homeostasis. Diatoms are the major primary producers in the ocean. However, little is known about the circadian clock in marine diatoms compared with other organisms. Here, we investigated circadian clock genes, their expression patterns, and responses to environmental stimuli such as light, nitrogen and phosphorus in two marine diatoms, Skeletonema costatum and Phaeodactylum tricornutum, using a combination of qRT-PCR and bioinformatic analysis. We identified 17 and 18 circadian clock genes in P. tricornutum and S. costatum, respectively. Despite significant evolutionary differences, these genes were similar to those of the higher plant Arabidopsis. We also established a molecular model for the marine diatom circadian clock comprising an input pathway, core oscillator, output pathway, and valve effector. Notably, the expression patterns of core clock genes (circadian clock associated 1 (CCA1), late elongated hypocotyl (LHY) and timing of cab 1 (TOC1)) in both species differed from those of terrestrial plants. Furthermore, the expression of these genes was influenced by variations in ambient light, nitrogen and phosphorus availability. Although marine diatoms and higher plants share common circadian clock components, their clock genes have diverged throughout evolution, likely as a result of adapting to contrasting environments.
  • These authors contributed equally to this work.
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  • [1]
    Alabadí D, Oyama T, Yanovsky M J, et al. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science, 293(5531): 880–883. doi: 10.1126/science.1061320
    Annunziata R, Ritter A, Fortunato A E, et al. 2019. bHLH-PAS protein RITOM1 regulates diel biological rhythms in the marine diatom Phaeodactylum tricornutum. Proceedings of the National Academy of Sciences, 116(26): 13137–13142. doi: 10.1073/pnas.1819660116
    Basu D, Dehesh K, Schneider-Poetsch H J, et al. 2000. Rice PHYC gene: structure, expression, map position and evolution. Plant Molecular Biology, 44(1): 27–42. doi: 10.1023/a:1006488119301
    Boxall S F, Foster J M, Bohnert H J, et al. 2005. Conservation and divergence of circadian clock operation in a stress-inducible crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiology, 137(3): 969–982. doi: 10.1104/pp.104.054577
    Bruce V G. 1970. The biological clock in Chlamydomonas reinhardi. The Journal of Eukaryotic Microbiology, 17(2): 328–334. doi: 10.1111/j.1550-7408.1970.tb02380.x
    Dehesh K, Tepperman J, Christensen A H, et al. 1991. phy B is evolutionarily conserved and constitutively expressed in rice seedling shoots. Molecular and General Genetics, 225(2): 305–313. doi: 10.1007/BF00269863
    Demarsy E, Fankhauser C. 2009. Higher plants use LOV to perceive blue light. Current Opinion in Plant Biology, 12(1): 69–74. doi: 10.1016/j.pbi.2008.09.002
    Derveaux S, Vandesompele J, Hellemans J. 2010. How to do successful gene expression analysis using real-time PCR. Methods, 50(4): 227–230. doi: 10.1016/j.ymeth.2009.11.001
    Dodd A N, Salathia N, Hall A, et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309(5734): 630–633. doi: 10.1126/science.1115581
    Dong M A, Farré E M, Thomashow M F. 2011. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the c-repeat binding factor (CBF) pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 108(17): 7241–7246. doi: 10.1073/pnas.1103741108
    Falkowski P G, Barber R T, Smetacek V. 1998. Biogeochemical controls and feedbacks on ocean primary production. Science, 281(5374): 200–206. doi: 10.1126/science.281.5374.200
    Feldman J F, Hoyle M N. 1973. Isolation of circadian clock mutants of Neurospora crassa. Genetics, 75(4): 605–613. doi: 10.1093/genetics/75.4.605
    Field C B, Behrenfeld M J, Randerson J T, et al. 1998. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281(5374): 237–240. doi: 10.1126/science.281.5374.237
    Filonova A, Haemsch P, Gebauer C, et al. 2013. Protein disulfide isomerase 2 of Chlamydomonas reinhardtii is involved in circadian rhythm regulation. Molecular Plant, 6(5): 1503–1517. doi: 10.1093/mp/sst048
    Fujiwara S, Oda A, Yoshida R, et al. 2008. Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. The Plant Cell, 20(11): 2960–2971. doi: 10.1105/tpc.108.061531
    Goldman J C. 1993. Potential role of large oceanic diatoms in new primary production. Deep-Sea Research Part I: Oceanographic Research Papers, 40(1): 159–168. doi: 10.1016/0967-0637(93)90059-C
    Greenham K, McClung C R. 2015. Integrating circadian dynamics with physiological processes in plants. Nature Reviews Genetics, 16(10): 598–610. doi: 10.1038/nrg3976
    Harmer S L. 2009. The circadian system in higher plants. Annual Review of Plant Biology, 60(1): 357–377. doi: 10.1146/annurev.arplant.043008.092054
    Harmer S L, Hogenesch J B, Straume M, et al. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science, 290(5499): 2110–2113. doi: 10.1126/science.290.5499.2110
    Hazen S P, Schultz T F, Pruneda-Paz J L, et al. 2005. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proceedings of the National Academy of Sciences of the United States of America, 102(29): 10387–10392. doi: 10.1073/pnas.0503029102
    Hotta C T, Gardner M J, Hubbard K E, et al. 2007. Modulation of environmental responses of plants by circadian clocks. Plant, Cell & Environment, 30(3): 333–349,
    Irigoien X, Huisman J, Harris R P. 2004. Global biodiversity patterns of marine phytoplankton and zooplankton. Nature, 429(6994): 863–867. doi: 10.1038/nature02593
    Izawa T, Takahashi Y, Yano M. 2003. Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Current Opinion in Plant Biology, 6(2): 113–120. doi: 10.1016/S1369-5266(03)00014-1
    Kaczorowski K A, Quail P H. 2003. Arabidopsis PSEUDO-RESPONSE REGULATOR7 is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. The Plant Cell, 15(11): 2654–2665. doi: 10.1105/tpc.015065
    Kang Lee-Kuo, Tsui Feng-Hsiu, Chang Jeng. 2012. Quantification of diatom gene expression in the sea by selecting uniformly transcribed mRNA as the basis for normalization. Applied and Environmental Microbiology, 78(17): 6051–6058. doi: 10.1128/AEM.00935-12
    Kevei É, Nagy F. 2003. Phytochrome controlled signalling cascades in higher plants. Physiologia Plantarum, 117(3): 305–313. doi: 10.1034/j.1399-3054.2003.00049.x
    Kondo T, Tsinoremas N F, Golden S S, et al. 1994. Circadian clock mutants of cyanobacteria. Science, 266(5188): 1233–1236. doi: 10.1126/science.7973706
    Konopka R J, Benzer S. 1971. Clock mutants of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 68(9): 2112–2116. doi: 10.1073/pnas.68.9.2112
    Lin Chentao, Shalitin D. 2003. Cryptochrome structure and signal transduction. Annual Review of Plant Biology, 54(1): 469–496. doi: 10.1146/annurev.arplant.54.110901.160901
    Liu Hua, Wang Honggui, Gao Pengfei, et al. 2009. Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). Journal of Plant Physiology, 166(3): 278–289. doi: 10.1016/j.jplph.2008.06.003
    Lu S X, Liu Hongtao, Knowles S M, et al. 2011. A role for protein kinase casein kinase 2 α-subunits in the Arabidopsis circadian clock. Plant Physiology, 157(3): 1537–1545. doi: 10.1104/pp.111.179846
    Más P, Kim W Y, Somers D E, et al. 2003. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature, 426(6966): 567–570. doi: 10.1038/nature02163
    Martínez-García JF, Huq E, Quail PH. 2000. Direct targeting of light signals to a promoter element-bound transcription factor. Science, 288: 859–863. doi: 10.1126/science.288.5467.859
    Matsuo T, Okamoto K, Onai K, et al. 2008. A systematic forward genetic analysis identified components of the Chlamydomonas circadian system. Genes & Development, 22(7): 918–930. doi: 10.1101/gad.1650408
    Matsushika A, Murakami M, Ito S, et al. 2007. Characterization of circadian-associated pseudo-response regulators: I. Comparative studies on a series of transgenic lines misexpressing five distinctive PRR genes in Arabidopsis thaliana. Bioscience, Biotechnology, and Biochemistry, 71(2): 527–534,
    McClung C R. 2001. Circadian rhythms in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 52: 139–162. doi: 10.1146/annurev.arplant.52.1.139
    McClung C R. 2011. The genetics of plant clocks. Advances in Genetics, 74: 105–139. doi: 10.1016/B978-0-12-387690-4.00004-0
    Meyer H, Thienel U, Piechulla B. 1989. Molecular characterization of the diurnal/circadian expression of the chlorophyll a/b-binding proteins in leaves of tomato and other dicotyledonous and monocotyledonous plant species. Planta, 180(1): 5–15. doi: 10.1007/BF02411404
    Michael T P, Salomé P A, Yu H J, et al. 2003. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science, 302(5647): 1049–1053. doi: 10.1126/science.1082971
    Millar A J, Carré I A, Strayer C A, et al. 1995. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science, 267(5201): 1161–1163. doi: 10.1126/science.7855595
    Moulager M, Monnier A, Jesson B, et al. 2007. Light-dependent regulation of cell division in Ostreococcus: evidence for a major transcriptional input. Plant Physiology, 144(3): 1360–1369. doi: 10.1104/pp.107.096149
    Mulekar J J, Huq E. 2014. Expanding roles of protein kinase CK2 in regulating plant growth and development. Journal of Experimental Botany, 65(11): 2883–2893. doi: 10.1093/jxb/ert401
    Murakami M, Ashikari M, Miura K, et al. 2003. The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. Plant and Cell Physiology, 44(11): 1229–1236. doi: 10.1093/pcp/pcg135
    Murakami M, Tago Y, Yamashino T, et al. 2007. Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant and Cell Physiology, 48(1): 110–121. doi: 10.1093/pcp/pcl043
    Noordally Z B, Millar A J. 2015. Clocks in algae. Biochemistry, 54(2): 171–183. doi: 10.1021/bi501089x
    Para A, Farré E M, Imaizumi T, et al. 2007. PRR3 is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. The Plant Cell, 19(11): 3462–3473. doi: 10.1105/tpc.107.054775
    Ragni M, d’Alcalà M R. 2007. Circadian variability in the photobiology of Phaeodactylum tricornutum: pigment content. Journal of Plankton Research, 29(2): 141–156. doi: 10.1093/plankt/fbm002
    Salomé P A, Weigel D, McClung C R. 2010. The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. The Plant Cell, 22(11): 3650–3661. doi: 10.1105/tpc.110.079087
    Salter M G, Franklin K A, Whitelam G C. 2003. Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature, 426(6967): 680–683. doi: 10.1038/nature02174
    Sato E, Nakamichi N, Yamashino T, et al. 2002. Aberrant expression of the Arabidopsis circadian-regulated APRR5 gene belonging to the APRR1/TOC1 quintet results in early flowering and hypersensitiveness to light in early photomorphogenesis. Plant and Cell Physiology, 43(11): 1374–1385. doi: 10.1093/pcp/pcf166
    Schaffer R, Ramsay N, Samach A, et al. 1998. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell, 93(7): 1219–1229. doi: 10.1016/S0092-8674(00)81465-8
    Schweiger E, Wallraff H G, Schweiger H G. 1964. Endogenous circadian rhythm in cytoplasm of Acetabularia: influence of the nucleus. Science, 146(3644): 658–659. doi: 10.1126/science.146.3644.658
    Seo S, Kim J, Lee J W, et al. 2020. Enhanced pyruvate metabolism in plastids by overexpression of putative plastidial pyruvate transporter in Phaeodactylum tricornutum. Biotechnology for Biofuels, 13: 120. doi: 10.21203/rs.3.rs-25111/v1
    Staiger D. 2002. Circadian rhythms in Arabidopsis: time for nuclear proteins. Planta, 214(3): 334–344. doi: 10.1007/s004250100662
    Strayer C, Oyama T, Schultz T F, et al. 2000. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science, 289(5480): 768–771. doi: 10.1126/science.289.5480.768
    Troein C, Locke J C W, Turner M S, et al. 2009. Weather and seasons together demand complex biological clocks. Current Biology, 19(22): 1961–1964. doi: 10.1016/j.cub.2009.09.024
    Turek F W, Joshu C, Kohsaka A, et al. 2005. Obesity and metabolic syndrome in circadian Clock mutant mice. Science, 308(5724): 1043–1045. doi: 10.1126/science.1108750
    Wada T, Shimono K, Kikukawa T, et al. 2011. Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga. Journal of Molecular Biology, 411(5): 986–998. doi: 10.1016/j.jmb.2011.06.028
    Wang Zhiyong, Tobin E M. 1998. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell, 93(7): 1207–1217. doi: 10.1016/S0092-8674(00)81464-6
    Wang Dazhi, Zhang Yingjiao, Zhang Shufei, et al. 2013. Quantitative proteomic analysis of cell cycle of the dinoflagellate Prorocentrum donghaiense (Dinophyceae). PLoS ONE, 8(5): e63659. doi: 10.1371/journal.pone.0063659
    Wright K P, Mchill A W, Birks B R, et al. 2013. Entrainment of the human circadian clock to the natural light-dark cycle. Current Biology, 23(16): 1554–1558. doi: 10.1016/j.cub.2013.06.039
    Zhang Shufeng, Yuan Chunjuan, Chen Ying, et al. 2016. Comparative transcriptomic analysis reveals novel insights into the adaptive response of Skeletonema costatum to changing ambient phosphorus. Frontiers in Microbiology, 7: 1476. doi: 10.3389/fmicb.2016.01476
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