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MBE Advance Access first published online on October 31, 2007
This version published online on November 2, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm234
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Published by Oxford University Press 2007.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

Evolutionary Dynamics of Introns in Plastid-Derived Genes in Plants: Saturation Nearly Reached But Slow Intron Gain Continues

Malay Kumar Basu1, Igor B. Rogozin1, Oliver Deusch2, Tal Dagan2, William Martin2 and Eugene V. Koonin1,*

1 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda MD, USA
2 Institute of Botany III, University of Düsseldorf, Düsseldorf, Germany

* To whom correspondence should be addressed: koonin{at}ncbi.nlm.nih.gov

Received for publication July 2, 2007. Revision received October 10, 2007. Accepted for publication October 22, 2007.

Some of the principal transitions in the evolution of eukaryotes are characterized by engulfment of prokaryotes by primitive eukaryotic cells. In particular, ~ 1.6 billion years ago, engulfment of a cyanobacterium that became the ancestor of chloroplasts and other plastids gave rise to Plantae, the major branch of eukaryotes comprised of glaucophytes, red algae, green algae, and green plants. After endosymbiosis, there was large scale migration of genes from the endosymbiont to the nuclear genome of the host such that ~18% of the nuclear genes in Arabidopsis appear to be of chloroplast origin. To gain insight into the process of evolution of gene structure in these, originally, intronless genes, we compared the properties and the evolutionary dynamics of introns in genes of plastid origin and ancestral eukaryotic genes in Arabidopsis, poplar, and rice genomes. We found that intron densities in plastid-derived genes were slightly but significantly lower than those in ancestral eukaryotic genes. Although most of the introns in both categories of genes were conserved between monocots (rice) and dicots (Arabidopsis and poplar), lineage-specific intron gain was more pronounced in plastid-derived genes than in ancestral genes, whereas there was no significant difference in the intron loss rates between the two classes of genes. Thus, after the transfer to the nuclear genome, the plastid-derived genes have undergone a massive intron invasion that, by the time of the divergence of dicots and monocots (150-200 million years ago), yielded intron densities only slightly lower than those in ancestral genes. Nevertheless, the accumulation of introns in plastid-derived genes appears not to have reached saturation and continues to this time, albeit at a low rate. The overall pattern of intron gain and loss in the plastid-derived genes is shaped by this continuing gain and the more general tendency for loss that is characteristic of the recent evolution of plant genes.

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