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Meis homeobox genes control progenitor competence in the retina

Significance The retina is derived from the neuroepithelium in the vertebrate. During retinal development, three spatially patterned domains are formed, namely the ciliary margin zone, the optic disc, and a region that contains retinal progenitor cells. Little is known about the mechanisms that regulate this patterning and specification. In this study, we show that retinal regionalization is impaired in the Meis1 and Meis2 compound-null retina in mice. By analyzing transcriptomic and epigenomic profiles, we map and characterize the Meis-dependent gene regulatory network within the embryonic retina. We propose that Meis1 and Meis2 function redundantly to promote expression of retinal progenitor cell-specific genes, while simultaneously restricting ciliary margin zone- and optic disc-specific genes. The vertebrate eye is derived from the neuroepithelium, surface ectoderm, and extracellular mesenchyme. The neuroepithelium forms an optic cup in which the spatial separation of three domains is established, namely, the region of multipotent retinal progenitor cells (RPCs), the ciliary margin zone (CMZ)—which possesses both a neurogenic and nonneurogenic potential—and the optic disk (OD), the interface between the optic stalk and the neuroretina. Here, we show by genetic ablation in the developing optic cup that Meis1 and Meis2 homeobox genes function redundantly to maintain the retinal progenitor pool while they simultaneously suppress the expression of genes characteristic of CMZ and OD fates. Furthermore, we demonstrate that Meis transcription factors bind regulatory regions of RPC-, CMZ-, and OD-specific genes, thus providing a mechanistic insight into the Meis-dependent gene regulatory network. Our work uncovers the essential role of Meis1 and Meis2 as regulators of cell fate competence, which organize spatial territories in the vertebrate eye.