Gene transfer to the nucleus and the evolution of chloroplasts

Abstract

Photosynthetic eukaryotes, particularly unicellular forms, possess a fossil record that is either wrought with gaps or difficult to interpret, or both. Attempts to reconstruct their evolution have focused on plastid phylogeny, but were limited by the amount and type of phylogenetic information contained within single genes1,2,3,4,5. Among the 210 different protein-coding genes contained in the completely sequenced chloroplast genomes from a glaucocystophyte, a rhodophyte, a diatom, a euglenophyte and five land plants, we have now identified the set of 45 common to each and to a cyanobacterial outgroup genome. Phylogenetic inference with an alignment of 11,039 amino-acid positions per genome indicates that this information is sufficient — but just barely so — to identify the rooted nine-taxon topology. We mapped the process of gene loss from chloroplast genomes across the inferred tree and found that, surprisingly, independent parallel gene losses in multiple lineages outnumber phylogenetically unique losses by more than 4:1. We identified homologues of 44 different plastid-encoded proteins as functional nuclear genes of chloroplast origin, providing evidence for endosymbiotic gene transfer to the nucleus in plants.

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Figure 1: Plastid phylogeny interpreted from chloroplast proteins.
Figure 2: Phylogenetic distribution of gene loss from chloroplast genomes.

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Acknowledgements

We thank R. G. Herrmann for discussion, H. Phillipe for comments on the manuscript, the Rechenzentrum der Universität Braunschweig for use of computer facilities, and the Deutsche Forschungsgemeinschaft (W.M. and K.V.K.) and the Ministry of Education, Science, Sports and Culture of Japan (M.H.) for financial support. B.S. is the recipient of a psotdoctoral stipend from the DFG; V.G. is the recipient of a Ph.D. stipend from DAAD.

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Correspondence to William Martin.

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Martin, W., Stoebe, B., Goremykin, V. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162–165 (1998). https://doi.org/10.1038/30234

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