Many microbial communities contain organized patterns of cell types, yet relatively little is known about the mechanism or function of this organization. In colonies of the budding yeast Saccharomyces cerevisiae, sporulation occurs in a highly organized pattern, with a top layer of sporulating cells sharply separated from an underlying layer of nonsporulating cells. A mutant screen identified the Mpk1 and Bck1 kinases of the cell-wall integrity (CWI) pathway as specifically required for sporulation in colonies. The CWI pathway was induced as colonies matured, and a target of this pathway, the Rlm1 transcription factor, was activated specifically in the nonsporulating cell layer, here termed feeder cells. Rlm1 stimulates permeabilization of feeder cells and promotes sporulation in an overlying cell layer through a cell-nonautonomous mechanism. The relative fraction of the colony apportioned to feeder cells depends on nutrient environment, potentially buffering sexual reproduction against suboptimal environments.KEYWORDS cell-wall integrity; cell permeability; cell-cell signaling; Saccharomyces cerevisiae; sporulation A S embryos develop, cells of different fates organize into patterns [reviewed in Kicheva et al. (2012) and Perrimon et al. (2012)] . Intriguingly, even unicellular microbial species form communities in which different cell types are organized into patterns [reviewed in Kaiser et al. (2010), Honigberg (2011, and Loomis (2014)]. For example, colonies of the budding yeast Saccharomyces cerevisiae form an upper layer of larger cells (U cells) overlying a layer of smaller cells (L cells). U and L cells differ in their metabolism, gene expression, and resistance to stress, and U and L layers are separated by a strikingly sharp boundary Vachova et al. 2013). Patterns are also observed in yeast biofilms, where cells closest to the plastic surface grow as ovoid cells, whereas cells further from the surface differentiate into hyphae for Candida species [reviewed in Finkel and Mitchell (2011)] or pseudohyphae and eventually asci for S. cerevisiae (White et al. 2011).Sporulation also occurs in patterns within yeast colonies. Specifically, a narrow horizontal layer of sporulated cells forms through the center of the colony early during colony development. As colonies continue to mature, this layer progressively expands upward to include the top of the colony; this wave is driven by progressive alkalization and activation of the Rim101 signaling pathway . In contrast, cells at the bottom of the colony, i.e., directly contacting the agar substrate, also sporulate at early stages of colony development, but this narrow cell layer does not expand as the colony matures . The same colony sporulation pattern is observed in a range of laboratory yeasts as well as in S. cerevisiae and S. paradoxus isolated from the wild. Indeed, in these wild yeasts, the same colony sporulation pattern forms on a range of fermentable and nonfermentable carbon sources .The mechanism of sporulation patterning and its function remai...