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mRNAs encoding polarity and secretion factors (POLs) target the incipient bud site in yeast for localized translation during division. In pheromone-treated cells we now find that these mRNAs are also localized to the yeast-mating projection (shmoo) tip. However, in contrast to the budding program, neither the She2 nor She3 proteins are involved. Instead, the Scp160 RNA-binding protein binds POL and mating pathway mRNAs and regulates their spatial distribution in a Myo4- and cortical ER-dependent fashion. RNA binding by Scp160 is stimulated by activation of Gpa1, the G protein α subunit regulated by the pheromone receptor, and is required for pheromone gradient sensing, as well as subsequent chemotropic growth and cell-cell mating. These effects are incurred independently of obvious changes in translation; thus, mRNA trafficking is required for chemotropism and completion of the mating program. This is, to our knowledge, the first demonstration of ligand-activated RNA targeting in the development of a simple eukaryote.