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.
Highlights
Small bioactive peptides such as neuropeptides, peptide hormones or pheromones, and antimicrobial peptides are generally expressed as parts of larger proproteins because their small sizes prevent direct transmission to the secretory pathway (Wegener and Gorbashov 2008)
Examples of bioactive peptides derived from polyproteins include many FMRFamide-related peptides (Walker et al 2009); endogenous opioids including endorphins, enkephalins, and dynorphins (Rossier 1988); tachykinins such as substance P and neurokinin A (Krause et al 1989); and many different antimicrobial peptides including naegleriapores (Herbst et al 2004), apidaecins (CasteelsJosson et al 1993), and magainins (Zasloff 1987)
A repeat encoding the peptide WHWLRLKPGQPMY was observed in two strains of S. cerevisiae from the Sake clade and another repeat encoding the peptide WHWLQLKPGQPIY was observed in every strain of S. paradoxus in the American C group
Summary
Small bioactive peptides such as neuropeptides, peptide hormones or pheromones, and antimicrobial peptides are generally expressed as parts of larger proproteins because their small sizes prevent direct transmission to the secretory pathway (Wegener and Gorbashov 2008). The difference in pheromone production associated with adding or removing a single repeat can have dramatic consequences for competitive mating success and repeat number polymorphism at MFa1 may be an important determinant of fitness.
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