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  Diminishing returns on intragenic repeat number expansion in the production of signaling peptides

Rogers, D. W., McConnell, E., Miller, E. L., & Greig, D. (2017). Diminishing returns on intragenic repeat number expansion in the production of signaling peptides. Molecular Biology and Evolution, 34(12), 3176-3185. Retrieved from http://dx.doi.org/10.1093/molbev/msx243.

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Item Permalink: http://hdl.handle.net/11858/00-001M-0000-002E-8F8B-E Version Permalink: http://hdl.handle.net/11858/00-001M-0000-002E-8F8C-C
Genre: Journal Article

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 Creators:
Rogers, David W.1, Author              
McConnell, Ellen1, Author              
Miller, Eric L.1, Author              
Greig, Duncan1, Author              
Affiliations:
1Max-Planck Research Group Experimental Evolution, Max Planck Institute for Evolutionary Biology, Max Planck Society, ou_1445640              

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Free keywords: protein tandem repeats; codon usage; genotype-to-phenotype; length-dependent translation; concerted evolution; copy number variation; YEAST SACCHAROMYCES-PARADOXUS; EXPERIMENTAL EVOLUTION; CEREVISIAE; TRANSLATION; PRECURSOR; GENE; AMPLIFICATION; EXPRESSION; GENERATION; PROTEINS
 Abstract: Signaling peptides enable communication between cells, both within and between individuals, and are therefore key to the control of complex physiological and behavioral responses. Since their small sizes prevent direct transmission to secretory pathways, these peptides are often produced as part of a larger polyprotein comprising precursors for multiple related or identical peptides; the physiological and behavioral consequences of this unusual gene structure are not understood. Here, we show that the number of mature-pheromone-encoding repeats in the yeast α-mating-factor gene MFα1 varies considerably between closely related isolates of both Saccharomyces cerevisiae and its sister species Saccharomyces paradoxus. Variation in repeat number has important phenotypic consequences: Increasing repeat number caused higher pheromone production and greater competitive mating success. However, the magnitude of the improvement decreased with increasing repeat number such that repeat amplification beyond that observed in natural isolates failed to generate more pheromone, and could actually reduce sexual fitness. We investigate multiple explanations for this pattern of diminishing returns and find that our results are most consistent with a translational trade-off: Increasing the number of encoded repeats results in more mature pheromone per translation event, but also generates longer transcripts thereby reducing the rate of translation—a phenomenon known as length-dependent translation. Length-dependent translation may be a powerful constraint on the evolution of genes encoding repetitive or modular proteins, with important physiological and behavioral consequences across eukaryotes.

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Language(s): eng - English
 Dates: 2017-09-142017-12
 Publication Status: Published in print
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Title: Molecular Biology and Evolution
  Other : Mol. Biol. Evol.
Source Genre: Journal
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Publ. Info: Oxford : Oxford University Press
Pages: - Volume / Issue: 34 (12) Sequence Number: - Start / End Page: 3176 - 3185 Identifier: ISSN: 0737-4038
CoNE: /journals/resource/954925536119