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Lateral Transfer and Recompartmentalization of Calvin Cycle Enzymes of Plants and Algae

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Abstract

Certain Calvin cycle enzymes also function in glycolysis or gluconeogenisis, thus photosynthetic eukaryotes would be predicted to have ancestrally possessed cytosolic homologues of these enzymes derived from the eukaryotic host and plastid homologues from the cyanobacterial endosymbiont. In practice, the evolutionary histories of these enzymes are often more complex. Focusing on eukaryotes with secondary plastids, we have examined the evolution of four such genes: class I and II fructose bisphosphate aldolase (FBA), sedoheptulose bisphosphatase (SBPase), and fructose bisphosphatase (FBPase). We show that previously observed distributions of plastid and cytosolic homologues are not always found in algae with secondary plastids: there is evidence for multiple events of both lateral gene transfer and retargeting to a new cellular compartment for both cytosolic and plastid enzymes of plants and algae. In particular, we show that a clade of class II FBAs spans a greater diversity of eukaryotes that previously recognized and contains both plastid-targeted (Phaeodactylum, Odontella) and cytosolic (ascomycetes, oomycetes, Euglena, and Bigelowiella) forms. Lateral transfer events also gave rise to a subset of plant cytosolic FBA, as well as cytosolic FBPase in Toxoplasma and other coccidian apicomplexa. In contrast, it has recently been suggested that the Trypanosoma FBA and SBPase are derived from a plastid, however, greater taxonomic sampling shows that these enzymes provide no evidence for a plastid-containing ancestor of Trypanosoma. Altogether, the evolutionary histories of the FBA and SBPase/FBPase gene families are complex, including extensive paralogy, lateral transfer, and retargeting between cellular compartments.

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Acknowledgements

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (227301-00). P.J.K. is a Scholar of the Canadian Institute for Advanced Research and a new investigator of the Michael Smith Foundation for Health Research and the Canadian Institutes for Health Research. We thank J.M. Archibald, J.T. Harper, and B.S. Leander for critical reading of the manuscript.

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  1. Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada

    Matthew Rogers & Patrick J. Keeling

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Correspondence to Patrick J. Keeling.

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Rogers, M., Keeling, P.J. Lateral Transfer and Recompartmentalization of Calvin Cycle Enzymes of Plants and Algae . J Mol Evol 58, 367–375 (2004). https://doi.org/10.1007/s00239-003-2558-7

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