Eukaryotic evolutionary transitions are associated with extreme codon bias in functionally-related proteins

Hudson, N. J., Gu, Q. , Nagaraj, S. H., Ding, Y.-S., Dalrymple, B. P. and Reverter, A. (2011) Eukaryotic evolutionary transitions are associated with extreme codon bias in functionally-related proteins. PLoS ONE, 6(9), e25457. (doi: 10.1371/journal.pone.0025457) (PMID:21966531) (PMCID:PMC3179510)

Abstract

Codon bias in the genome of an organism influences its phenome by changing the speed and efficiency of mRNA translation and hence protein abundance. We hypothesized that differences in codon bias, either between-species differences in orthologous genes, or within-species differences between genes, may play an evolutionary role. To explore this hypothesis, we compared the genome-wide codon bias in six species that occupy vital positions in the Eukaryotic Tree of Life. We acquired the entire protein coding sequences for these organisms, computed the codon bias for all genes in each organism and explored the output for relationships between codon bias and protein function, both within- and between-lineages. We discovered five notable coordinated patterns, with extreme codon bias most pronounced in traits considered highly characteristic of a given lineage. Firstly, the Homo sapiens genome had stronger codon bias for DNA-binding transcription factors than the Saccharomyces cerevisiae genome, whereas the opposite was true for ribosomal proteins – perhaps underscoring transcriptional regulation in the origin of complexity. Secondly, both mammalian species examined possessed extreme codon bias in genes relating to hair – a tissue unique to mammals. Thirdly, Arabidopsis thaliana showed extreme codon bias in genes implicated in cell wall formation and chloroplast function – which are unique to plants. Fourthly, Gallus gallus possessed strong codon bias in a subset of genes encoding mitochondrial proteins – perhaps reflecting the enhanced bioenergetic efficiency in birds that co-evolved with flight. And lastly, the G. gallus genome had extreme codon bias for the Ciliary Neurotrophic Factor – which may help to explain their spontaneous recovery from deafness. We propose that extreme codon bias in groups of genes that encode functionally related proteins has a pathway-level energetic explanation.

• Item Type: Articles
• Additional Information: This work was supported by the National Nature Science Foundation of China (No. 60975059, 60775052), Specialized Research Fund for the Doctoral Program of Higher Education from Ministry of Education of China (No. 20090075110002), Project of the Shanghai Committee of Science and Technology (Nos. 10JC1400200, 10DZ0506500, 09JC1400900). Shivashankar H. Nagaraj is grateful to CSIRO for the award of an OCE Post-Doctoral Fellowship.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Gu, Dr Quan
• Authors: Hudson, N. J., Gu, Q., Nagaraj, S. H., Ding, Y.-S., Dalrymple, B. P., and Reverter, A.
• Subjects: Q Science > QH Natural history > QH301 Biology
• College/School: College of Medical Veterinary and Life Sciences > School of Infection & Immunity; College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research
• Journal Name: PLoS ONE
• Publisher: Public Library of Science
• ISSN: 1932-6203
• ISSN (Online): 1932-6203
• Copyright Holders: Copyright © 2011 Hudson et al.
• First Published: First published in PLoS ONE 6(9): e25457
• Publisher Policy: Reproduced under a Creative Commons License