Bifacial stem cell niches in fish and plants

Abstract

Embryonic development is key for determining the architecture and shape of multicellular bodies. However, most cells are produced postembryonically in, at least partly, differentiated organs. In this regard, organismal growth faces common challenges in coordinating expansion and function of body structures. Here we compare two examples for postembryonic growth processes from two different kingdoms of life to reveal common regulatory principles: lateral growth of plants and the enlargement of the fish retina. In both cases, growth is based on stem cell systems mediating radial growth by a bifacial mode of tissue production. Surprisingly, although being evolutionary distinct, we find similar patterns in regulatory circuits suggesting the existence of preferable solutions to a common developmental problem.

Figure 1. Schematic overview of the bifacial cambial and retinal stem cell niches of plants and fish.

The geometry of the cylindrical plant stem (here Arabidopsis thaliana) and the hemispherical vertebrate eye (here Oryzias latipes) is provided by a radial niche of stem cells located inside the tissue. From here, coordinated growth occurs in two directions (centrally and peripherally) giving rise to distinct tissues. (a–a’) For plants, cambial stem cells (CAM, magenta) give rise to central xylem (wood, blue) and to peripheral phloem (bast, green). (b–b’) In the juvenile fish, retinal stem cells reside in the ciliary marginal zone (CMZ, magenta) producing both, the lens-facing neuroretina (NR, blue) and the lens-averted retinal pigment epithelium (RPE, green) that are physically separated by the cavity of the ventricle (gray line in (b’)). Growth is driven by both, preferential asymmetric cell divisions that result in one stem and one progenitor cell (white arrows, periclinal in plants, radial in fish) and rare symmetric cell divisions to expand the stem cell pool (black arrow, anticlinal in plants, circumferential in fish). Immediate descendants are further subjected to massive proliferation and subsequent differentiation. (a’) In plants, progenitors (purple) on either side of the cambium undergo differentiation into a variety of specialized cell types. (b’) In contrast, the retinal progenitor cells (RPCs, purple) differentiate into only one cell type in case of the RPE and into six neuronal and one glial cell type for the NR. These are organized in a stereotypical layering (ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; RGC, retinal ganglion cell layer; ON, optic nerve). a’ modified from Ref. [19], with permission from Elsevier b drawing of adult medaka reprinted from Ref. [45], with permission from Elsevier

Figure 2. Domain formation and patterning of the bifacial stem cell niches.

Expression of homeobox transcription factors (WOX4, Rx2) confers stem cell properties in the bifacial niche. Signaling originating from the neighboring differentiated tissue limits the extent of the stem cell niche. (a) CLE41/44-PXY signaling promotes proliferation through WOX4 and, in parallel, blocks xylem differentiation through GSK activation. Spatial differences in plant hormone signaling may define the boundaries between phloem, cambium and xylem. (b) Cross-regulation between Wnt and Hh signaling pathways through expression of the antagonists Gli3 and Sfrp-1, fine-tunes proliferative activity of stem cells (SC) and progenitors. CMZ, ciliary marginal zone; NR, neuroretina; RPE, retinal pigment epithelium; white arrow, asymmetric cell division