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Plastid-associated galactolipid composition in eyespot-containing dinoflagellates: a review

  • Graeff, Jori E. (Department of Biology, Middle Tennessee State University) ;
  • Elkins, Lindsey C. (Department of Biology, Middle Tennessee State University) ;
  • Leblond, Jeffrey D. (Department of Biology, Middle Tennessee State University)
  • Received : 2021.04.07
  • Accepted : 2021.05.25
  • Published : 2021.06.15

Abstract

Relative to the large number of photosynthetic dinoflagellate species, only a select few possess proteinaceous, carotenoid-rich eyespots which have been demonstrated in other algae to act in phototactic responses. The proteins comprising the different categories of dinoflagellate eyespots are positioned in or near the peridinin-containing photosynthetic plastid membranes which are composed primarily of two galactolipids, mono- and digalactosyldiacylglycerol (MGDG and DGDG). Within eyespot-containing dinoflagellates, this arrangement occurs mostly in those with secondary plastids, although some dinoflagellates with tertiary plastids of diatom origin are known to possess eyespots. We here provide an examination of the MGDG and DGDG composition of eyespot-containing dinoflagellates with secondary, peridinin-containing plastids and tertiary plastids of diatom origin to address the fundamental question of whether eyespots and their component proteins and carotenoids are associated with alterations in galactolipid composition when compared to eyespot-lacking photosynthetic dinoflagellates. This is an important question because the dinoflagellate eyespot-plastid membrane system can be considered a more complicated and evolved state of plastid development. Included in this examination are data on the previously unexamined peridinin- and type A eyespot-containing dinoflagellate Margalefidinium polykrikoides, and the type D eyespot-containing, aberrant plastid "dinotom" Durinskia baltica. In addition, we have reviewed the galactolipid composition of algae from the Chlorophyceae, Cryptophyceae, and Euglenophyceae as a comparison to determine if algal classes apart from the Dinophyceae contain altered galactolipids in association with eyespots. We conclude that the presence of an eyespot in dinoflagellates and other algae is not associated with noticeable changes in galactolipid composition.

Keywords

References

  1. Allen, J. F. 2002. Photosynthesis of ATP: electrons, proton pumps, rotors, and poise. Cell 110:273-276. https://doi.org/10.1016/S0092-8674(02)00870-X
  2. Anesi, A., Obertegger, U., Hansen, G., Sukenik, A., Flaim, G. & Guella, G. 2016. Comparative analysis of membrane lipids in psychrophilic and mesophilic freshwater dinoflagellates. Front. Plant Sci. 7:524. https://doi.org/10.3389/fpls.2016.00524
  3. Beck, C. & Uhl, R. 1994. On the localization of voltage-sensitive calcium channels in the flagella of Chlamydomonas reinhardtii. J. Cell Biol. 125:1119-1125. https://doi.org/10.1083/jcb.125.5.1119
  4. Berthold, P., Tsunoda, S. P., Ernst, O. P., Mages, W., Gradmann, D. & Hegemann, P. 2008. Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 20:1665-1677. https://doi.org/10.1105/tpc.108.057919
  5. Bigogno, C., Khozin-Goldberg, I., Boussiba, S., Vonshak, A. & Cohen, Z. 2002a. Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60:497-503. https://doi.org/10.1016/S0031-9422(02)00100-0
  6. Bigogno, C., Khozin-Goldberg, I. & Cohen, Z. 2002b. Accumulation of arachidonic acid-rich triacylglycerols in the microalga Parietochloris incisa (Trebuxiophyceae, Chlorophyta). Phytochemistry 60:135-143. https://doi.org/10.1016/S0031-9422(02)00037-7
  7. Boudiere, L., Michaud, M., Petroutsos, D., Rebeille, F., Falconet, D., Bastien, O., Roy, S., Finazzi, G., Rolland, N., Jouhet, J., Block, M. A. & Marechal, E. 2014. Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim. Biophys. Acta Bioenerg. 1837:470-480. https://doi.org/10.1016/j.bbabio.2013.09.007
  8. Chesnick, J. M., Kooistra, W. H., Wellbrock, U. & Medlin, L. K. 1997. Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). J. Eukaryot. Microbiol. 44:314-320. https://doi.org/10.1111/j.1550-7408.1997.tb05672.x
  9. Cho, S. H. & Thompson, G. A. Jr. 1987. On the metabolic relationships between monogalactosyldiacylglycerol and digalactosyldiacylglycerol molecular species in Dunaliella salina. J. Biol. Chem. 262:7586-7593. https://doi.org/10.1016/S0021-9258(18)47606-5
  10. Chuecas, L. & Riley, J. P. 1969. Component fatty acids of the total lipids of some marine phytoplankton. J. Mar. Biol. Assoc. U. K. 49:97-116. https://doi.org/10.1017/S0025315400046439
  11. Craig, E. M., Dahmen, J. L. & Leblond, J. D. 2015. Temperature modulation and the presence of C20 fatty acids in mono- and digalactosyldiacylglycerol of Euglena gracilis and Lepocinclis acus: a modern interpretation of euglenid galactolipids using positive-ion electrospray ionization/mass spectrometry. Phycol. Res. 63:231-238. https://doi.org/10.1111/pre.12094
  12. Craveiro, S. C., Calado, A. J., Daugbjerg, N., Hansen, G. & Moestrup, O. 2011. Ultrastructure and LSU rDNAbased phylogeny of Peridinium lomnickii and description of Chimonodinium gen. nov. (Dinophyceae). Protist 162:590-615. https://doi.org/10.1016/j.protis.2011.03.003
  13. Craveiro, S. C., Calado, A. J., Daugbjerg, N. & Moestrup, O. 2009. Ultrastructure and LSU rDNA-based revision of Peridinium group Palatinum (Dinophyceae) with the description of Palatinus gen. nov. J. Phycol. 45:1175-1194. https://doi.org/10.1111/j.1529-8817.2009.00739.x
  14. Craveiro, S. C., Daugbjerg, N., Moestrup, O. & Calado, A. J. 2015. Fine-structural characterization and phylogeny of Peridinium polonicum, type species of the recently described genus Naiadinium (Dinophyceae). Eur. J. Protistol. 51:259-279. https://doi.org/10.1016/j.ejop.2015.05.001
  15. Craveiro, S. C., Moestrup, O., Daugbjerg, N. & Calado, A. J. 2010. Ultrastructure and large subunit rDNA-based phylogeny of Sphaerodinium cracoviense, an unusual freshwater dinoflagellate with a novel type of eyespot. J. Eukaryot. Microbiol. 57:568-585. https://doi.org/10.1111/j.1550-7408.2010.00512.x
  16. Dawut, M., Sym, S. D. & Horiguchi, T. 2018. Re-investigation of Gymnodinium natalense (Dinophyceae), a tidal pool dinoflagellate from South Africa and the proposal of a new combination Ansanella natalensis. Phycol. Res. 66:300-309. https://doi.org/10.1111/pre.12329
  17. Della Greca, M., Monaco, P., Pinto, G., Pollio, A. & Previtera, L. 1989. Lipid composition of the acidophilic alga Dunaliella acidophila. II. Molecular species of galactolipids. Biochim. Biophys. Acta Lipids Lipid Metabol. 1004:271-273. https://doi.org/10.1016/0005-2760(89)90277-4
  18. Deme, B., Cataye, C., Block, M. A., Marechal, E. & Jouhet, J. 2014. Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J. 28:3373-3383. https://doi.org/10.1096/fj.13-247395
  19. Dodge, J. D. 1974. Fine structure and phylogeny in the algae. Sci. Prog. 61:257-274.
  20. Dodge, J. D. 1984. The functional and phylogenetic significance of dinoflagellate eyespots. Biosystems 16:259-267. https://doi.org/10.1016/0303-2647(83)90009-6
  21. Dodson, V. J., Dahmen, J. L., Mouget, J. -L. & Leblond, J. D. 2013. Mono- and digalactosyldiacylglycerol composition of the marennine-producing diatom, Haslea ostrearia: comparison to a selection of pennate and centric diatoms. Phycol. Res. 61:199-207. https://doi.org/10.1111/pre.12015
  22. Dormann, P., Hoffmann-Benning, S., Balbo, I. & Benning, C. 1995. Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7:1801-1810. https://doi.org/10.1105/tpc.7.11.1801
  23. Dorrell, R. G. & Howe, C. J. 2015. Integration of plastids with their hosts: lessons learned from dinoflagellates. Proc. Natl. Acad. Sci. U. S. A. 112:10247-10254. https://doi.org/10.1073/pnas.1421380112
  24. Dunstan, G. A., Volkman, J. K., Barrett, S. M., Leroi, J. -M. & Jeffrey, S. W. 1993. Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155-161. https://doi.org/10.1016/S0031-9422(00)90525-9
  25. Erickson, E., Wakao, S. & Niyogi, K. K. 2015. Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J. 82:449-465. https://doi.org/10.1111/tpj.12825
  26. Foster, K. W. & Smyth, R. D. 1980. Light Antennas in phototactic algae. Microbiol. Rev. 44:572-630. https://doi.org/10.1128/mr.44.4.572-630.1980
  27. Fried, A., Tietz, A., Ben-Amotz, A. & Eichenberger, W. 1982. Lipid composition of the halotolerant alga, Dunaliella bardawil. Biochim. Biophys. Acta Lipids Lipid Metabol. 713:419-426. https://doi.org/10.1016/0005-2760(82)90261-2
  28. Gagat, P., Bodyl, A., Mackiewicz, P. & Stiller, J. W. 2014. Tertiary plastid endosymbioses in dinoflagellates. In Loffelhardt, W. (Ed.) Endosymbiosis. Springer, Vienna, pp. 233-290.
  29. Gaines, G. & Elbrachter M. 1987. Heterotrophic nutrition. In Taylor, F. J. R. (Ed.) The Biology of Dinoflagellates. Blackwell, Oxford, pp. 224-267.
  30. Gao, J., Wang, H., Yuan, Q. & Feng, Y. 2018. Structure and function of the photosystem supercomplexes. Front. Plant Sci. 9:357. https://doi.org/10.3389/fpls.2018.00357
  31. Gavelis, G. S., Hayakawa, S., White, R. A. 3rd., Gojobori, T., Suttle, C. A., Keeling, P. J. & Leander, B. S. 2015. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature 523:204-207. https://doi.org/10.1038/nature14593
  32. Giroud, C., Gerber, A. & Eichenberger, W. 1988. Lipids of Chlamydomonas reinhardtii: analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol. 29:587-595.
  33. Gray, C. G., Lasiter, A. D. & Leblond, J. D. 2009a. Mono- and digalactosyldiacylglycerol composition of dinoflagellates. III. Four cold-adapted, peridinin-containing taxa and the presence of trigalactosyldiacylglycerol as an additional glycolipid. Eur. J. Phycol. 44:439-445. https://doi.org/10.1080/09670260902787977
  34. Gray, C. G., Lasiter, A. D., Li, C. & Leblond, J. D. 2009b. Mono- and digalactosyldiacylglycerol composition of dinoflagellates. I. Peridinin-containing taxa. Eur. J. Phycol. 44:191-197. https://doi.org/10.1080/09670260802419481
  35. Greuet, C. 1967. Organisation ultrastructurale du tentacule d'Erythropsis pavillardi Kofoid et Swezy Peridinien Warnowiidae Lindemann. Protistologica 3:335-345.
  36. Guiry, M. D. & Guiry, G. M. 2020. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org. Accessed Dec 20, 2020.
  37. Harz, H. & Hegemann, P. 1991. Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351:489-491. https://doi.org/10.1038/351489a0
  38. Hehenberger, E., Imanian, B., Burki, F. & Keeling, P. J. 2014. Evidence for the retention of two evolutionary distinct plastids in dinoflagellates with diatom endosymbionts. Genome Biol. Evol. 6:2321-2334. https://doi.org/10.1093/gbe/evu182
  39. Holzl, G., Witt, S., Gaude, N., Melzer, M., Schottler, M. A. & Dormann, P. 2009. The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol. 150:1147-1159. https://doi.org/10.1104/pp.109.139758
  40. Hoppenrath, M., Bachvaroff, T. R., Handy, S. M., Delwiche, C. F. & Leander, B. S. 2009. Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evol. Biol. 9:116. https://doi.org/10.1186/1471-2148-9-116
  41. Imanian, B., Pombert, J. -F. & Keeling, P. J. 2010. The complete plastid genomes of the two 'dinotoms' Durinskia baltica and Kryptoperidinium foliaceum. PLoS ONE 5:e10711. https://doi.org/10.1371/journal.pone.0010711
  42. Iwataki, M., Hansen, G., Moestrup, O. & Matsuoka, K. 2010. Ultrastructure of the harmful unarmored dinoflagellate Cochlodinium polykrikoides (Dinophyceae) with reference to the apical groove and flagellar apparatus. J. Eukaryot. Microbiol. 57:308-321. https://doi.org/10.1111/j.1550-7408.2010.00491.x
  43. Iwataki, M., Kawami, H. & Matsuoka, K. 2007. Cochlodinium fulvescens sp. nov. (Gymnodiniales, Dinophyceae), a new chain-forming unarmored dinoflagellate from Asian coasts. Phycol. Res. 55:231-239. https://doi.org/10.1111/j.1440-1835.2007.00466.x
  44. Janero, D. R. & Barrnett, R. 1981. Cellular and thylakoidmembrane glycolipids of Chlamydomonas reinhardtii 137+. J. Lipid Res. 22:1119-1125. https://doi.org/10.1016/S0022-2275(20)40670-4
  45. Jang, S. H., Jeong, H. J., Moestrup, O., Kang, N. S., Lee, S. Y., Lee, K. H. & Seong, K. A. 2017. Yihiella yeosuensis gen. et sp. nov. (Suessiaceae, Dinophyceae), a novel dinoflagellate isolated from the coastal waters of Korea. J. Phycol. 53:131-145. https://doi.org/10.1111/jpy.12486
  46. Jarvis, P., Dormann, P., Peto, C. A., Lutes, J., Benning, C. & Chory, J. 2000. Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc. Nat. Acad. Sci. U. S. A. 97:8175-8179. https://doi.org/10.1073/pnas.100132197
  47. Jeong, H. J., Jang, S. H., Moestrup, O., Kang, N. S., Lee, S. Y., Potvin, E. & Noh, J. H. 2014. Ansanella granifera gen. et sp. nov. (Dinophyceae), a new dinoflagellate from the coastal waters of Korea. Algae 29:75-99. https://doi.org/10.4490/algae.2014.29.2.075
  48. Johansson, O. N., Topel, M., Egardt, J., Pinder, M. I. M., Andersson, M. X., Godhe, A. & Clarke, A. K. 2019. Phenomics reveals a novel putative chloroplast fatty acid transporter in the marine diatom Skeletonema marinoi involved in temperature acclimation. Sci. Rep. 9:15143. https://doi.org/10.1038/s41598-019-51683-y
  49. Kato, S., Ozasa, K., Maeda, M., Tanno, Y., Tamaki, S., Higuchi-Takeuchi, M., Numata, K., Kodama, Y., Sato, M., Toyooka, K. & Shinomura, T. 2020. Carotenoids in the eyespot apparatus are required for triggering phototaxis in Euglena gracilis. Plant J. 101:1091-1102. https://doi.org/10.1111/tpj.14576
  50. Kawai, H. & Inouye, I. 1989. Flagellar autofluorescence in forty-four chlorophyll c-containing algae. Phycologia 28:222-227. https://doi.org/10.2216/i0031-8884-28-2-222.1
  51. Keeling, P. J. 2010. The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:729-748. https://doi.org/10.1098/rstb.2009.0103
  52. Kreimer, G. 1994. Cell biology of phototaxis in flagellate algae. Int. Rev. Cytol. 148:229-310. https://doi.org/10.1016/S0074-7696(08)62409-2
  53. Kreimer, G. 1999. Reflective properties of different eyespot types in dinoflagellates. Protist 150:311-323. https://doi.org/10.1016/S1434-4610(99)70032-5
  54. Kremp, A., Elbrachter, M., Schweikert, M., Wolny, J. L. & Gottschling, M. 2005. Woloszynskia halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 41:629-642. https://doi.org/10.1111/j.1529-8817.2005.00070.x
  55. Kretschmann, J., Calasan, A. Z. & Gottschling, M. 2018. Molecular phylogenetics of dinophytes harboring diatoms as endosymbionts (Kryptoperidiniaceae, Peridiniales), with evolutionary interpretations and a focus on the identity of Durinskia oculata from Prague. Mol. Phylogenet. Evol. 118:392-402. https://doi.org/10.1016/j.ympev.2017.10.011
  56. Kumari, P., Kumar, M., Reddy, C. R. K. & Jha, B. 2013. Algal lipids, fatty acids and sterols. In Dominguez, H. (Ed.) Functional Ingredients from Algae for Foods and Nutraceuticals. Woodhead Publishing, Cambridge, pp. 87-134.
  57. LaJeunesse, T. C. 2017. Validation and description of Symbiodinium microadriaticum, the type species of Symbiodinium (Dinophyta). J. Phycol. 53:1109-1114. https://doi.org/10.1111/jpy.12570
  58. Lang, I., Hodac, L., Friedl, T. & Feussner, I. 2011. Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol. 11:124. https://doi.org/10.1186/1471-2229-11-124
  59. Leblond, J. D., Dodson, J. & Dahmen, J. I. 2013. Mono- and digalactosyldiacylglycerol composition of dinoflagellates. VII. Evidence against galactolipid production and plastid presence in the heterotrophic, basal dinoflagellate, Oxyrrhis marina. Eur. J. Phycol. 48:309-317. https://doi.org/10.1080/09670262.2013.833297
  60. Leblond, J. D. & Lasiter, A. D. 2009. Mono- and digalactosyldiacylglycerol composition of dinoflagellates. II. Lepidodinium chlorophorum, Karenia brevis, and Kryptoperidinium foliaceum, three dinoflagellates with aberrant plastids. Eur. J. Phycol. 44:199-205. https://doi.org/10.1080/09670260802524611
  61. Leblond, J. D., McDaniel, S. L., Lowrie, S. D., Khadka, M. & Dahmen, J. L. 2019. Mono-and digalactosyldiacylglycerol composition of dinoflagellates. VIII. Temperature effects and a perspective on the curious case of Karenia mikimotoi as a producer of the unusual, 'green algal' fatty acid hexadecatetraenoic acid [16:4(n-3)]. Eur. J. Phycol. 54:78-90. https://doi.org/10.1080/09670262.2018.1519602
  62. Lindberg, K., Moestrup, O. & Daugbjerg, N. 2005. Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 44:416-440. https://doi.org/10.2216/0031-8884(2005)44[416:SOWDIW]2.0.CO;2
  63. Loll, B., Kern, J., Saenger, W., Zouni, A. & Biesiadka, J. 2005. Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040-1044. https://doi.org/10.1038/nature04224
  64. Lucas, I. A. N. 1982. Observations on the fine structure of the Cryptophyceae. II. The eyespot. Br. Phycol. J. 17:13-19. https://doi.org/10.1080/00071618200650031
  65. Lum, W. M., Takahashi, K., Benico, G., Takayama, H. & Iwataki, M. 2019. Dactylodinium arachnoides sp. nov. (Borghiellaceae, Dinophyceae): a new marine dinoflagellate with a loop-shaped apical structure complex and tubular membranous extrusomes. Phycologia 58:661-674. https://doi.org/10.1080/00318884.2019.1658399
  66. Luo, Z., Mertens, K. N., Nezan, E., Gu, L., Pospelova, V., Thoha, H. & Gu, H. 2019. Morphology, ultrastructure and molecular phylogeny of cyst-producing Caladoa arcachonensis gen. et sp. nov. (Peridiniales, Dinophyceae) from France and Indonesia. Eur. J. Phycol. 54:235-248.
  67. Lynch, D. V., Gundersen, R. E. & Thompson, G. A. 1983. Separation of galactolipid molecular species by highperformance liquid chromatography. Plant Physiol. 72:903-905. https://doi.org/10.1104/pp.72.3.903
  68. Makshakova, O., Breton, C. & Perez, S. 2020. Unraveling the complex enzymatic machinery making a key galactolipid in chloroplast membrane: a multiscale computer simulation. Sci. Rep. 10:13514. https://doi.org/10.1038/s41598-020-70425-z
  69. McLachlan, J. L., Curtis, J. M., Boutilier, K., Keusgen, M. & Seguel, M. R. 1999. Tetreutreptia pomquetensis (Euglenophyta), a psychrophilic species: growth and fatty acid composition. J. Phycol. 35:280-286. https://doi.org/10.1046/j.1529-8817.1999.3520280.x
  70. McLachlan, J. L., Seguel, M. R. & Fritz, L. 1994. Tetreutreptia pomquetensis gen. et sp. nov. (Euglenophyceae): a quadriflagellate, phototrophic marine euglenoid. J. Phycol. 30:538-544. https://doi.org/10.1111/j.0022-3646.1994.00538.x
  71. Melkonian, M. & Robenek, H. 1984. The eyespot apparatus of flagellated green algae: a critical review. Prog. Phycol. Res. 3:193-268.
  72. Mitani, E., Nakayama, F., Matsuwaki, I., Ichi, I., Kawabata, A., Kawachi, M. & Kato, M. 2017. Fatty acid composition profiles of 235 strains of three microalgal divisions within the NIES Microbial Culture Collection. Microb. Res. Syst. 33:19-29.
  73. Moestrup, O. & Daugbjerg, N. 2007. On dinoflagellate phylogeny and classification. In Brodie, J. & Lewis, J. (Eds.) Unraveling the Algae: the Past, Present, and Future of Algal Systematics. CRC Press, Boca Raton, FL, pp. 215-230.
  74. Moestrup, O., Lindberg, K. & Daugbjerg, N. 2009. Studies on woloszynskioid dinoflagellates IV: the genus Biecheleria gen. nov. Phycol. Res. 57:203-220. https://doi.org/10.1111/j.1440-1835.2009.00540.x
  75. Murata, N. & Siegenthaler, P. -A. 1998. Lipids in photosynthesis: an overview. In Siegenthaler, P. -A. & Murata, N. (Eds.) Lipids in Photosynthesis: Structure, Function and Genetics. Kluwer Academic, Dordrecht, pp. 1-20.
  76. Murphy, D. J. 1982. The importance of non-planar bilayer regions in photosynthetic membranes and their stabilisation by galactolipids. FEBS Lett. 150:19-26. https://doi.org/10.1016/0014-5793(82)81297-0
  77. Nakamura, K., Bray, D. F., Costerton, J. W. & Wagenaar, E. B. 1973. The eyespot of Chlamydomonas eugametos: a freeze-etch study. Can. J. Bot. 51:817-819. https://doi.org/10.1139/b73-101
  78. Niyogi, K. K. 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:333-359. https://doi.org/10.1146/annurev.arplant.50.1.333
  79. Pandeirada, M. S., Craveiro, S. C., Daugbjerg, N., Moestrup, O. & Calado, A. J. 2021. Fine-structural characterization and phylogeny of Sphaerodinium (Suessiales, Dinophyceae), with the description of an unusual type of freshwater dinoflagellate cyst. Eur. J. Protistol. 78:125770. https://doi.org/10.1016/j.ejop.2021.125770
  80. Parke, M. 1949. Studies on marine flagellates. J. Mar. Biol. Assoc. U. K. 28:255-286. https://doi.org/10.1017/S0025315400055302
  81. Pienaar, R. N., Sakai, H. & Horiguchi, T. 2007. Description of a new dinoflagellate with a diatom endosymbiont, Durinskia capensis sp. nov. (Peridiniales, Dinophyceae) from South Africa. J. Plant Res. 120:247. https://doi.org/10.1007/s10265-006-0047-y
  82. Raho, N., Fraga, S., Abad, J. P. & Marin, I. 2018. Biecheleria tirezensis sp. nov. (Dinophyceae, Suessiales), a new halotolerant dinoflagellate species isolated from the athalassohaline Tirez natural pond in Spain. Eur. J. Phycol. 53:99-113. https://doi.org/10.1080/09670262.2017.1386328
  83. Ratha, S. K., Jena, M. & Adhikary, S. P. 2006. Euglenophytes from Orissa State, east coast of India. Algae 21:61-73. https://doi.org/10.4490/ALGAE.2006.21.1.061
  84. Sakurai, I., Mizusawa, N., Wada, H. & Sato, N. 2007. Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol. 145:1361-1370. https://doi.org/10.1104/pp.107.106781
  85. Schaller, K., David, R. & Uhl, R. 1997. How Chlamydomonas keeps track of the light once it has reached the right phototactic orientation. Biophys. J. 73:1562-1572. https://doi.org/10.1016/S0006-3495(97)78188-8
  86. Schaller, K. & Uhl, R. 1997. A microspectrophotometric study of the shielding properties of eyespot and cell body in Chlamydomonas. Biophys. J. 73:1573-1578. https://doi.org/10.1016/S0006-3495(97)78189-X
  87. Siano, R., Montresor, M., Probert, I., Not, F. & de Vargas, C. 2010. Pelagodinium gen. nov. and P. beii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385-399. https://doi.org/10.1016/j.protis.2010.01.002
  88. Taipale, S., Strandberg, U., Peltomaa, E., Galloway, A. W. E., Ojala, A. & Brett, M. T. 2013. Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquat. Microb. Ecol. 71:165-178. https://doi.org/10.3354/ame01671
  89. Takahashi, K., Benico, G., Lum, W. M. & Iwataki, M. 2019. Gertia stigmatica gen. et sp. nov. (Kareniaceae, Dinophyceae), a new marine unarmored dinoflagellate possessing the peridinin-type chloroplast with an eyespot. Protist 170:125680. https://doi.org/10.1016/j.protis.2019.125680
  90. Takahashi, K., Moestrup, O., Jordan, R. W. & Iwataki, M. 2015. Two new freshwater woloszynskioids Asulcocephalium miricentonis gen. et sp. nov. and Leiocephalium pseudosanguineum gen. et sp. nov. (Suessiaceae, Dinophyceae) lacking an apical furrow apparatus. Protist 166:638-658. https://doi.org/10.1016/j.protis.2015.10.003
  91. Takahashi, K., Moestrup, O., Wada, M., Ishimatsu, A., Nguyen, V. N., Fukuyo, Y. & Iwataki, M. 2017. Dactylodinium pterobelotum gen. et sp. nov., a new marine woloszynskioid dinoflagellate positioned between the two families Borghiellaceae and Suessiaceae. J. Phycol. 53:1223-1240. https://doi.org/10.1111/jpy.12575
  92. Takahashi, K., Sarai, C. & Iwataki, M. 2014. Morphology of two marine woloszynskioid dinoflagellates, Biecheleria brevisulcata sp. nov. and Biecheleriopsis adriatica (Suessiaceae, Dinophyceae), from Japanese coasts. Phycologia 53:52-65. https://doi.org/10.2216/13-192.1
  93. Tamura, M., Takano, Y. & Horiguchi, T. 2009. Discovery of a novel type of body scale in the marine dinoflagellate, Amphidinium cupulatisquama sp. nov. (Dinophyceae). Phycol. Res. 57:304-312. https://doi.org/10.1111/j.1440-1835.2009.00550.x
  94. Tomas, R. N. & Cox, E. R. 1973. Observations on the symbiosis of Peridinium balticum and its intracellular alga. I. Ultrastructure. J. Phycol. 9:304-323. https://doi.org/10.1111/j.1529-8817.1973.tb04098.x
  95. Ueki, N., Ide, T., Mochiji, S., Kobayashi, Y., Tokutsu, R., Ohnishi, N., Yamaguchi, K., Shigenobu, S., Tanaka, K., Minagawa, J., Hisabori, T., Hirono, M. & Wakabayashi, K. 2016. Eyespot-dependent determination of the phototactic sign in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U. S. A. 113:5299-5304. https://doi.org/10.1073/pnas.1525538113
  96. Waller, R. F. & Koreny, L. 2017. Plastid complexity in dinoflagellates: a picture of gains, losses, replacements and revisions. Adv. Bot. Res. 84:105-143. https://doi.org/10.1016/bs.abr.2017.06.004
  97. Walne, P. L. & Arnott, H. J. 1967. The comparative ultrastructure and possible function of eyespots: Euglena granulata and Chlamydomonas eugametos. Planta 77:325-353. https://doi.org/10.1007/BF00389319
  98. Wu, W., Ping, W., Wu, H., Li, M., Gu, D. & Xu, Y. 2013. Monogalactosyldiacylglycerol deficiency in tobacco inhibits the cytochrome b6f-mediated intersystem electron transport process and affects the photostability of the photosystem II apparatus. Biochim. Biophys. Acta Bioenerg. 1827:709-722. https://doi.org/10.1016/j.bbabio.2013.02.013
  99. Yamada, N., Sym, S. D. & Horiguchi, T. 2017. Identification of highly divergent diatom-derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Mol. Biol. Evol. 34:1335-1351. https://doi.org/10.1093/molbev/msx054
  100. Yokouchi, K., Onuma, R. & Horiguchi, T. 2018. Ultrastructure and phylogeny of a new species of mixotrophic dinoflagellate, Paragymnodinium stigmaticum sp. nov. (Gymnodiniales, Dinophyceae). Phycologia 57:539-554. https://doi.org/10.2216/17-140.1