Skip to main content Accessibility help
×
Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-24T13:27:24.170Z Has data issue: false hasContentIssue false

4 - The Appearance of Eukaryotic Microalgae

from Part I - Origins and Consequences of Early Photosynthetic Organisms

Published online by Cambridge University Press:  24 October 2024

Mario Giordano
Affiliation:
Università degli Studi di Ancona, Italy
John Beardall
Affiliation:
Monash University, Victoria
John A. Raven
Affiliation:
University of Dundee
Stephen C. Maberly
Affiliation:
UK Centre for Ecology & Hydrology, Lancaster
Get access

Summary

Microalgae, with cyanobacteria, are the major primary producers in aquatic, predominantly marine, ecosystems, contributing to the biogeochemical cycling of multiple elements despite their small instantaneous biomass. Their evolutionary history revealed by genomic analyses has shown a complex past that produces a polyphyletic group including organisms that have undergone primary, secondary and tertiary chloroplast endosymbiosis with genetic integration and also horizontal gene transfer. All but one genus of photosynthetic eukaryotes arose by endosymbiosis of a gloeomargarita-like β-cyanobacterium in a eukaryote with the retention of some genes in the plastid, the transfer of more genes to the eukaryote nucleus, and the loss of many others, to produce the Archaeplastida. A second, much later, endosymbiosis of an α-cyanobacterium in a euglyphid amoeba yielded Paulinella. The diversification of the Archaeplastida yielded Glaucophyta, Rhodophyta, Chlorophyta and Streptophyta. Secondary endosymbiosis of red algae in eukaryotes led to microalgae of the ‘red line’, that is, photosynthetic Ochrista (= stramenopiles), Haptophyta, Cryptophyta and Alveolata (dinoflagellates and chromerids). Secondary endosymbiosis of chlorophyte algae in eukaryotes yielded microalgae of the Chlorarachniophyta and Euglenophyta. The ‘red line’ of secondary endosymbionts are dominant marine phytoplankton, possibly related to the occurrence of chlorophyll c that has high absorbance of blue light that dominates in deep ocean waters.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2024

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, J. F., de Paula, W. B., Puthiyaveetil, S. et al. (2011). A structural phylogenetic map for chloroplast photosynthesis. Trends in Plant Science. 16: 645655.CrossRefGoogle ScholarPubMed
Archibald, J. M. (2015). Genomic perspectives on the birth and spread of plastids. Proceedings of the National Academy of Sciences USA 112:1014710153.CrossRefGoogle ScholarPubMed
Bar-On, Y. M., Phillips, R. & Milo, R. (2018). The biomass distribution on Earth. Proceedings of the National Academy of Sciences USA 115: 65066511.CrossRefGoogle ScholarPubMed
Badger, M. R. & Price, G. D. (2003). CO2 concentrating mechanisms in cyanobacteria: Molecular components, their diversity and evolution. Journal of Experimental Botany 54: 609622.CrossRefGoogle ScholarPubMed
Bell, G. (1988). Sex and Death in Protozoa: The History of Obsession. Cambridge University Press, Cambridge. 216 pp.Google Scholar
Bengtson, S., Dallstedt, T., Belivaera, V. et al. (2017). Three-dimensional preservation of cellular and subcellular structures suggest 1.6 billion-year-old crown group red algae. PLOS Biology 15: e20000735. https://doi.org/10.1371/journalpbio.2000735.CrossRefGoogle ScholarPubMed
Bhattacharya, D., Yoon, H. S. & Hackett, J. D. (2004). Photosynthetic eukaryotes unite: Endosymbiosis connects the dots. Bioessays 26: 5060. https://doi.org/10.1002/bies.10376.CrossRefGoogle ScholarPubMed
Bhattacharya, D., Qiu, H., Lee, J. M. et al. (2018.). When less is more: Red algae as models for studying gene loss and genome evolution in eukaryotes. Critical Reviews in Plant Sciences 37: 8199.CrossRefGoogle Scholar
Blanc, G., Duncan, G., Agarkova, I. et al. (2010). The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22: 29432955.CrossRefGoogle ScholarPubMed
Blank, C. E. (2013). Origin and early evolution of photosynthetic eukaryotes in freshwater environments: Reinterpreting Proterozoic palaeobiology and biogeochemical processes in light of trait evolution. Journal of Phycology 49: 10401055.CrossRefGoogle Scholar
Bock, R. & Timmis, J. N. (2008). Reconstructing evolution: Gene transfer from plastids to the nucleus. Bioessays 30: 556566.CrossRefGoogle ScholarPubMed
Brasier, M. D. (2013). Green algae (Chlorophyta) and the question of freshwater symbiogenesis in the early Proterozoic. Journal of Phycology 49: 10361039.CrossRefGoogle ScholarPubMed
Brown, J. E. & Sorhannus, U. (2010). A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): Substantive underestimation of putative fossil ages. PLOS ONE 9: e12759.Google Scholar
Butterfield, N. J., Knoll, A. H. & Swett, T. (1994). Palaeobiology of the Neoproterozoic Svanbergfyllet formation, Spitzbergen. Fossils and Strata 34: 134.CrossRefGoogle Scholar
Butterfield, N. J. (2000). Bangiomorpha pubescens n.gen. n.sp: Implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Palaeobiology 26: 368404.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N. J. (2004). A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: Implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Palaeobiology 30: 231252.2.0.CO;2>CrossRefGoogle Scholar
Butterfield, N. J. (2015). Early evidence of the Eukaryota. Palaeobology 58: 517.Google Scholar
Cavalier-Smith, T. (2000). Membrane heredity and early chloroplast evolution. Trends in Plant Science 5: 174182.CrossRefGoogle ScholarPubMed
Cavalier-Smith, T. (2018). Kingdom Chromista and its eight phyla: A new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergence. Protoplasma 255: 297357.CrossRefGoogle Scholar
Crowel, R. M., Nienow, J. A. & Cahoon, A. B. (2019). The complete chloroplast and mitochondrial genomes in the genome Nitzschia palea (Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotom Durinskia baltica. Journal of Phycology 55: 352364.CrossRefGoogle Scholar
Curtis, B. A., Tanifuji, G., Burki, F. et al. (2012). Algal genomes reveal evolutionary mosaicism and the fate of the nucleomorph. Nature 492: 5965.CrossRefGoogle Scholar
Dacks, J. B., Field, M. C., Buick, R. et al. (2016). The changing view of eukaryogenesis – fossils, cells, lineages and how they all come together. Journal of Cell Science 129: 36953703.CrossRefGoogle ScholarPubMed
Davy, S. K., Allemand, D. & Weis, V. M. (2012). Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews 76: 229261.CrossRefGoogle ScholarPubMed
De Clerck, O., Bogaert, K. A. & Leliaert, F. (2012). Diversity and evolution of algae: Primary endosymbiosis. Advances in Botanical Research 64: 5586.CrossRefGoogle Scholar
Delaye, L., Valadez-Cano, C. & Pérez-Zamorano, B. (2016). How really ancient is Paulinella chromatophora. PLOS Currents Tree of Life 2016 March 15 Edition 1. https://doi.org/10.1371/currents.tol.e68a68a099364bb1a129a17b4e06cbb.Google ScholarPubMed
Del Cortona, A., Jackson, C. J., Bucchini, F. et al. (2020). Neoproterozic orgin and multiple transitions to macroscopic growth in green seaweeds. Proceedings of the National Academy of Sciences USA 117: 25512559.CrossRefGoogle Scholar
Delwiche, C. F. (1999). Tracing the thread of plastid diversity through the tapestry of life. American Naturalist 154: S164S177. https://doi.org/10.1086/303291.CrossRefGoogle ScholarPubMed
Derelle, R., López-Garcia, P., Timpano, H. et al. (2016). A phylogenomic framework to study the diversity and evolution of stramenopiles (= heterokonts). Molecular Biology and Evolution 33: 28902898.CrossRefGoogle Scholar
Deschamps, P. & Moreira, D. (2012). Reevaluating the green contribution to diatom genomes. Genome Biology and Evolution 4: 683688.CrossRefGoogle ScholarPubMed
Dorrell, R. G. & Howe, C. J. (2015). Integration of plastids with their hosts: Lessons learned from dinoflagellates. Proceedings of the National Academy of Sciences USA 112: 1024710254.CrossRefGoogle ScholarPubMed
Dorrell, R. G., Gile, G., McCallum, G. et al. (2016a). Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. eLife 6 : article e23717.CrossRefGoogle Scholar
Dorrell, R. G., Klinger, C. M., Newby, R. J. et al. (2016b). Progressive and biased divergent evolution underpins the origin and diversification of peridinin dinoflagellate plastids. Molecular Biology and Evolution 34: 361379.Google Scholar
Edwards, D., Cherns, L. & Raven, J. A. (2015). Could land-based early photosynthesizing ecosystems have bioengineered the planet in mid-Palaeozoic times? Palaeontology 58: 803837.CrossRefGoogle Scholar
Falkowski, P. G., Katz, M. E., Knoll, A. H. et al. (2004). The evolution of modern eukaryotic phytoplankton. Science 305: 354360.CrossRefGoogle ScholarPubMed
Falkowski, P. G. & Raven, J. A. (2007). Aquatic Photosynthesis. Princeton University Press, Princeton, NJ.CrossRefGoogle Scholar
Field, C. B., Behrenfeld, M. J., Randerson, J. T. et al. (1998). Primary production of the biosphere of the biosphere: Integrating terrestrial and oceanic components. Science 251: 237240.CrossRefGoogle Scholar
Figueroa-Martinez, F., Jackson, C. & Reyes-Prieto, A. (2018). Plastid genomes from diverse glaucophyte genera reveal a largely conserved gene content and limited architectural diversity. Genome Biology and Evolution 11: 174188.CrossRefGoogle Scholar
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Clarendon, Oxford.CrossRefGoogle Scholar
Flombaum, P., Gallegas, J. L., Gordillo, R. A. et al. (2013). Present and future global distribution of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences USA 110: 98249829.CrossRefGoogle ScholarPubMed
Flynn, K. J., Stoecker, D. E., Mitra, A. et al. (2013). Misuse of the phytoplankton – zooplankton dichotomy: The need to assign organisms as mixotrophs within phytoplankton functional types. Journal of Plankton Research 35: 511.CrossRefGoogle Scholar
Font-Muñoz, J. S., Jeanneret, R., Arrieta, J. et al. (2019). Collective sinking promotes selective cell pairing in planktonic pennate diatoms. Proceedings of the National Academy of Sciences USA 116: 1599716002.CrossRefGoogle ScholarPubMed
Fučiková, K., Paźioutová, M. & Rindi, F. (2015). Meiotic genes and sexual reproduction in the green algal class Trebouxiophyceae (Chlorophyta). Journal of Phycology 51: 419430.CrossRefGoogle ScholarPubMed
Gabr, A., Grossman, A. R. & Bhattacharya, D. (2020). Paulinella, a model for understanding plastid primary endosymbiosis. Journal of Phycology 56: 837843.CrossRefGoogle Scholar
Gold, D. A., Grubenstater, J., de Mendoza, A. et al. (2016). Sterol and genomic analyses validate the sponge biomarker hypothesis. Proceedings National Academy of Sciences USA 113: 26842689.CrossRefGoogle ScholarPubMed
Grimsley, N., Péquin, B., Nachy, C. et al. (2010). Cryptic sex in the smallest eukaryotic marine green algae. Molecular Biology and Evolution 27: 4754.CrossRefGoogle Scholar
Hickey, D. A. & Golding, G. B. (2018). The advantages of recombination when selection is acting on many genetic loci. Journal of Theoretical Biology 442: 123138.CrossRefGoogle ScholarPubMed
Hovde, B. T., Hanschen, E. R., Steadman Tyler, C. R. et al. (2018). Genomic characterisation reveals significant divergence within Chlorella sorokiniana (Chlorellales, Trebouxiophyceae). Algal Research 35: 449461.CrossRefGoogle Scholar
Imanian, B., Pombeet, J.-F., Dorrell, R. G. et al. (2012). Tertiary endosymbiosis in two dinotoms has generated little change in the mitochondrial genomes of their dinoflagellate hosts and diatom endosymbionts. PLOS ONE 7: article e43763.CrossRefGoogle ScholarPubMed
Jackson, C., Knoll, A. H., Chan, C. X. et al. (2018). Plastid phylogenomics with broad taxon sampling further elucidates the distinct evolutionary origins and timing of secondary green plastids. Scientific Reports 8: article 1523.CrossRefGoogle ScholarPubMed
Janouškovec, J., Gavelis, G. S., Burki, F. et al. (2017). Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proceedings of the National Academy of Sciences USA 114: E1711180.CrossRefGoogle ScholarPubMed
Janouškovec, J., Paskerova, G. G., Miroliubova, T. S. et al. (2019). Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles. eLife 8: e49662.CrossRefGoogle ScholarPubMed
Johnson, P. W., Hargraves, P. E. & Sieburth, J. M. (1988). Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919 (Chrysophyceae) and its redescription as a testate Rhizopod, Paulinella ovalis N. Comb. (Filosea: Euglyphina). Journal of Protozoology 35: 618626. https://doi.org/10.1111/j.1550–7408.1988.tb04160.x.CrossRefGoogle Scholar
Kamikawa, R., Tanifuji, G., Kawachi, M. et al. (2015). Plastid genome-based phylogeny pinpointed the origin of the green-colored plastid in the dinoflagellate Lepidodinium chlorophorum. Genome Biology and Evolution 7: 11331140.CrossRefGoogle ScholarPubMed
Keeling, P. J. (2013). The number, speed and impact of plastid endosymbiosis in eukaryotic evolution. Annual Review of Plant Biology 64: 593607.CrossRefGoogle ScholarPubMed
Kooistra, W. H. C. F., Gersonde, R., Medlin, L. K. et al. (2007). The origin and evolution of the diatoms: Their adaptation to a planktonic existence. In: Falkowski, P. G. & Knoll, A. H. (eds.) Evolution of Primary Producers in the Sea. Elsevier/Academic Press, Amsterdam, Heidelberg, pp. 207249.CrossRefGoogle Scholar
Krasovec, M., Eyre-Walker, A., Sanchez-Freandin, S. et al. (2017). Spontaneous mutation rate in the smallest photosynthetic eukaryotes. Molecular Biology and Evolution 34: 17701779.CrossRefGoogle ScholarPubMed
Kwong, W. K., del Campo, J., Mathur, V. et al. (2019). A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568: 103107.CrossRefGoogle ScholarPubMed
Larkum, A. W. D., Lockhart, P. J. & Howe, C. J. (2007). Shopping for plastids. Trends in Plant Science 12: 189195.CrossRefGoogle ScholarPubMed
Law, R. & Lewis, D. H. (1983). Biotic environments and the maintenance of sex – some evidence from mutualistic symbioses. Biological Journal of the Linnean Society 20: 249276.CrossRefGoogle Scholar
Lax, G., Eglit, Y., Eme, L. et al. (2018). Hemimastigophora is a novel supra-kingdom level lineage of eukaryotes. Nature 564: 410414.CrossRefGoogle ScholarPubMed
Lee, J., Cho, C. H., Park, S. I. et al. (2016). Parallel evolution of highly conserved plastid genome architecture in red seaweeds and seed plants. BMC Biology 14: article 75.CrossRefGoogle ScholarPubMed
Lemieux, C., Otis, C. & Turmel, M. (2014). Chloroplast phylogenomic analysis resolves deep-level relationships in the green algal class Trebouxiophyceae. BMC Evolutionary Biology 14: article 211.CrossRefGoogle ScholarPubMed
Lhee, D., Ha, J.-S., Kim, S. et al. (2019). Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species. Scientific Reports 9: article number 2560.CrossRefGoogle ScholarPubMed
Liu, H., Probert, I., Claustre, H. et al. (2009). Extreme diversity in non-calcifying haptophytes explains a major pigment paradox in open oceans. Proceedings of the National Academy of. Sciences USA 106: 1280312808.CrossRefGoogle Scholar
Liu, H., Aris-Brosou, S., Probert, I. et al. (2010). A time line of the environmental genetics of the haptophytes. Molecular Biology and Evolution 27: 161176.CrossRefGoogle ScholarPubMed
Mann, D. G. & Vanormelingen, P. (2013). An inordinate fondness? The number, distributions and origins of diatom species. Journal of Eukaryotic Microbiology 60: 411420.CrossRefGoogle ScholarPubMed
Marin, B., Nowack, E. C. M. & Melkonian, M. (2005). A plastid in the making: Evidence for a second primary endosymbiosis. Protist 156: 425432.CrossRefGoogle ScholarPubMed
Maruyama, S. & Kim, E. (2013). A modern descendant of early green algal phagotrophs. Current Biology 23: 10511054.CrossRefGoogle ScholarPubMed
Matsumoto, T., Shinozaki, F., Chikuni, T. et al. (2011). Green-coloured plastids in the dinoflagellate Lepidodinium are of core chlorophyte origin. Protist 162: 268276.CrossRefGoogle Scholar
McGhee, G. R. Jr (2019). Convergent Evolution on Earth. Lessons for the Search for Extraterrestrial Life. MIT Press, Cambridge, MA. ISBN 9780262042734.CrossRefGoogle Scholar
Minge, M. A., Shatchian-Tabrizi, K., Tøttesen, O. K. et al. (2010). A phylogenetic mosaic plastid proteome and unusual plastid-targetting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMS Evolutionary Biology 10: article 191.CrossRefGoogle ScholarPubMed
Muller, H. (1932). Some genetic aspects of sex. American Naturalist 66: 118138.CrossRefGoogle Scholar
Muller, H. J. (1964). The relation of recombination to mutational advance. Mutation Research 1: 29.CrossRefGoogle Scholar
Muñoz-Gómez, S. A., Mejia-Franco, F. G., Durnin, K. et al. (2017). The new red algal subphylum Proteorhodophytina comprises the largest and most divergent plastid genomes known. Current Biology 27: 16771684.CrossRefGoogle ScholarPubMed
Nakov, T., Beaulieu, J. M. & Alverson, A. J. (2018). Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta). New Phytologist 219: 462473.CrossRefGoogle Scholar
Novák Vaneclová, A. M. G., Zoltner, M., Kelly, S. (2020). Metabolic quirks and the colourful history of the Euglena gracilis secondary plastids. New Phytologist 225: 15781592.CrossRefGoogle Scholar
Nowack, E. C., Melkonian, M. & Glockner, G. (2008). Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Current Biology 18:410418.CrossRefGoogle ScholarPubMed
Nowack, E. C., Price, D. C., Bhattacharya, D. et al. (2016). Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proceedings of the National Academy of Sciences USA 113: 1221412219.CrossRefGoogle ScholarPubMed
Pochon, X., Wecker, P., Stot, M. et al. (2019). Towards an in-depth characterization of Symbiodiniaceae in tropical clams via metabarcoding of pooled multigene amplicons. PeerJ 7: article e6898.CrossRefGoogle ScholarPubMed
Ponce-Toledo, R. I., Deschamps, P., López-Garcia, P. et al. (2017). An early-branching freshwater cyanobacterium at the origin of plastids. Current Biology 27: 386391.CrossRefGoogle ScholarPubMed
Ponce-Toledo, R. I., López-Garcia, P. & Moreira, D. (2019). Horizontal and endosymbiotic gene transfer in early plastid evolution. New Phytologist 224: 618624. https://doi.org/10.1111/nph.15965.CrossRefGoogle ScholarPubMed
Price, D. C., Goodenough, G. W., Roth, R. et al. (2019). Analysis of an improved Cyanophora paradoxa assembly. DNA Research 26: 287299.CrossRefGoogle ScholarPubMed
Qiu, H., Price, D. C., Weber, A. P. et al. (2013a). Assessing the bacterial contribution to the plastid proteome. Trends in Plant Science 18:680687.CrossRefGoogle Scholar
Qiu, H., Yoon, H. S. & Bhattacharya, D. (2013b). Algal endosymbionts as vectors of horizontal gene transfer to photosynthetic eukaryotes. Frontiers in Plant Science 4: article 366.CrossRefGoogle ScholarPubMed
Raven, J. A. & Waite, A. M. (2004). The evolution of silicification in diatoms: Inescapable sinking and sinking as escape? New Phytologist 162: 4561.CrossRefGoogle Scholar
Raven, J. A., Beardall, J., Flynn, K. J. et al. (2009). Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: Relation to Darwin’s Insectivorous Plants. Journal of Experimental Botany 60: 39753987.CrossRefGoogle ScholarPubMed
Reyes-Prieto, A., Weber, A. P. & Bhattacharya, D. (2007). The origin and establishment of the plastid in algae and plants. Annual Review of Genetics 41 : 147168.CrossRefGoogle ScholarPubMed
Rigby, S. (1997). A comparison of colonization of the planktic realm and the land. Lethaia 30: 1117.CrossRefGoogle Scholar
Rigby, S. & Milsom, C. (1996). Benthic origins of zooplankton: An environmentally determined macroevolutionary effort. Geology 24: 5254.2.3.CO;2>CrossRefGoogle Scholar
Rigby, S. & Milsom, C. (2000). Origins, evolution and diversification of zooplankton. Annual Review of Ecology and Evolution 31: 293313.CrossRefGoogle Scholar
Sánchez-Baracaldo, P. (2015). Origin of planktonic marine cyanobacteria. Scientific Reports 5: 17418.CrossRefGoogle Scholar
Sánchez-Baracaldo, P., Ridgwell, A. & Raven, J. A. (2014). A Neoproterozoic transition in the marine nitrogen cycle. Current Biology 24: 652657.CrossRefGoogle ScholarPubMed
Sánchez-Baracaldo, P., Raven, J. A., Pisani, D. et al. (2017). Early photosynthetic eukaryotes inhabited low-salinity habitats. Proceedings of the National Academy of Sciences USA 114: E7737E7745. https://doi.org/10.1073/pnas.1620089114.CrossRefGoogle ScholarPubMed
Sims, P. A., Mann, D. G. & Medlin, L. K. (2006). Evolution of the diatoms: Insight from fossil, biological and molecular data. Phycologia 45: 361402.CrossRefGoogle Scholar
Speijer, D., Lukeš, J. & Elias, M. (2015). Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proceedings of the National Academy of Sciences USA 112: 88278834.CrossRefGoogle ScholarPubMed
Stoecker, D. K., Hanson, P. J., Caron, D. A. et al. (2017). Mixotrophy in the marine plankton. Annual Review of Marine Science 9: 311335.CrossRefGoogle ScholarPubMed
Tang, Q., Pang, K., Yuan, X. et al. (2020). A one billion year old multicellular chlorophyte. Nature Ecology and Evolution 4:543549.CrossRefGoogle ScholarPubMed
Taylor, T. N., Taylor, E. L. & Kring, M. (2009). Palaeobotany: The Biology and Evolution of Fossil Plants, 2nd ed. Academic Press, Burlington, MA.Google Scholar
Watanabe, M. M., Suda, S., Inoya, I. et al. (1990). Lepidodinium viride Gen. et Sp. Nov. (Gymnodiniales), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. Journal of Phycology 26: 741751.CrossRefGoogle Scholar
Wetherbee, R., Jackson, C. J. & Repetti, S. I. (2019). The golden paradox – a new heterokont lineage with chloroplasts surrounded by two membranes. Journal of Phycology 55: 257278. https://doi.org/10.1111/jpy.12822.CrossRefGoogle ScholarPubMed
Yang, E. C., Boo, S. M., Bhatacharya, D. et al. (2016). Divergence time estimates and the evolution of lineages in the floridiophyte red algae. Scientific Reports 6: article 21361.CrossRefGoogle Scholar
Yoon, H. S., Hackett, J. D., Ciniglia, C. et al. (2004). A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21: 809818.CrossRefGoogle ScholarPubMed
Young, J. N., Rickaby, R. E. M., Kapralov, M. V. et al. (2012). Adaptive signals in Rubisco reveal a history of ancient atmospheric carbon dioxide. Philosophical Transactions of the Royal Society B 367: 483492.CrossRefGoogle ScholarPubMed
Zhang, R., Nowack, E. C., Price, D. C. et al. (2017). Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles. Plant Journal 90: 221234.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×