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Title: Evolutionary instability of CUG-Leu in the genetic code of budding yeasts

Abstract

The genetic code used in nuclear genes is almost universal, but here we report that it changed three times in parallel during the evolution of budding yeasts. All three changes were reassignments of the codon CUG, which is translated as serine (in 2 yeast clades), alanine (1 clade), or the ‘universal’ leucine (2 clades). The newly discovered Ser2 clade is in the final stages of a genetic code transition. Most species in this clade have genes for both a novel tRNA Ser(CAG) and an ancestral tRNA Leu(CAG) to read CUG, but only tRNA Ser(CAG) is used in standard growth conditions. The coexistence of these alloacceptor tRNA genes indicates that the genetic code transition occurred via an ambiguous translation phase. We propose that the three parallel reassignments of CUG were not driven by natural selection in favor of their effects on the proteome, but by selection to eliminate the ancestral tRNA Leu(CAG).

Authors:
 [1];  [1]; ORCiD logo [2];  [2]; ORCiD logo [3];  [3];  [4]; ORCiD logo [5]; ORCiD logo [1];  [1];  [6]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. College Dublin (Ireland)
  2. Vanderbilt Univ., Nashville, TN (United States)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Amyris, Emeryville, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Dept. of Agriculture, Peoria, IL (United States). Agricultural Research Station
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1500012
Grant/Contract Number:  
FC02-07ER64494; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Krassowski, Tadeusz, Coughlan, Aisling Y., Shen, Xing-Xing, Zhou, Xiaofan, Kominek, Jacek, Opulente, Dana A., Riley, Robert, Grigoriev, Igor V., Maheshwari, Nikunj, Shields, Denis C., Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Wolfe, Kenneth H. Evolutionary instability of CUG-Leu in the genetic code of budding yeasts. United States: N. p., 2018. Web. doi:10.1038/s41467-018-04374-7.
Krassowski, Tadeusz, Coughlan, Aisling Y., Shen, Xing-Xing, Zhou, Xiaofan, Kominek, Jacek, Opulente, Dana A., Riley, Robert, Grigoriev, Igor V., Maheshwari, Nikunj, Shields, Denis C., Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, & Wolfe, Kenneth H. Evolutionary instability of CUG-Leu in the genetic code of budding yeasts. United States. doi:10.1038/s41467-018-04374-7.
Krassowski, Tadeusz, Coughlan, Aisling Y., Shen, Xing-Xing, Zhou, Xiaofan, Kominek, Jacek, Opulente, Dana A., Riley, Robert, Grigoriev, Igor V., Maheshwari, Nikunj, Shields, Denis C., Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Wolfe, Kenneth H. Mon . "Evolutionary instability of CUG-Leu in the genetic code of budding yeasts". United States. doi:10.1038/s41467-018-04374-7. https://www.osti.gov/servlets/purl/1500012.
@article{osti_1500012,
title = {Evolutionary instability of CUG-Leu in the genetic code of budding yeasts},
author = {Krassowski, Tadeusz and Coughlan, Aisling Y. and Shen, Xing-Xing and Zhou, Xiaofan and Kominek, Jacek and Opulente, Dana A. and Riley, Robert and Grigoriev, Igor V. and Maheshwari, Nikunj and Shields, Denis C. and Kurtzman, Cletus P. and Hittinger, Chris Todd and Rokas, Antonis and Wolfe, Kenneth H.},
abstractNote = {The genetic code used in nuclear genes is almost universal, but here we report that it changed three times in parallel during the evolution of budding yeasts. All three changes were reassignments of the codon CUG, which is translated as serine (in 2 yeast clades), alanine (1 clade), or the ‘universal’ leucine (2 clades). The newly discovered Ser2 clade is in the final stages of a genetic code transition. Most species in this clade have genes for both a novel tRNASer(CAG) and an ancestral tRNALeu(CAG) to read CUG, but only tRNASer(CAG) is used in standard growth conditions. The coexistence of these alloacceptor tRNA genes indicates that the genetic code transition occurred via an ambiguous translation phase. We propose that the three parallel reassignments of CUG were not driven by natural selection in favor of their effects on the proteome, but by selection to eliminate the ancestral tRNALeu(CAG).},
doi = {10.1038/s41467-018-04374-7},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {5}
}

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Works referenced in this record:

The ‘polysemous’ codon—a codon with multiple amino acid assignment caused by dual specificity of tRNA identity
journal, March 1997

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A novel nuclear genetic code alteration in yeasts and the evolution of codon reassignment in eukaryotes
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