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Edited by Michael S. Levine, Princeton University, Princeton, NJ, and approved June 21, 2017 (received for review March 13, 2017)
Significance
The lateral neural plate border (NPB) gives rise to the neural crest, one of the precursors of the peripheral nervous system (PNS) and generally considered an evolutionary innovation of the vertebrate lineage. Recently, it has been reported that a rudimentary neural crest exists in protovertebrate Ciona, but whether this is true in other invertebrates and there is conserved molecular machinery specifying the NPB lineage are unknown. We present evidence that orthologs of the NPB specification module specify lateral neural progenitor cells in several invertebrates, including worm, fly, and tunicate. We propose that an ancient lateral neuroblast gene regulatory module was coopted by chordates during the evolution of PNS progenitors.
Abstract
The lateral neural plate border (NPB), the neural part of the vertebrate neural border, is composed of central nervous system (CNS) progenitors and peripheral nervous system (PNS) progenitors. In invertebrates, PNS progenitors are also juxtaposed to the lateral boundary of the CNS. Whether there are conserved molecular mechanisms determining vertebrate and invertebrate lateral neural borders remains unclear. Using single-cell-resolution gene-expression profiling and genetic analysis, we present evidence that orthologs of the NPB specification module specify the invertebrate lateral neural border, which is composed of CNS and PNS progenitors. First, like in vertebrates, the conserved neuroectoderm lateral border specifier Msx/vab-15 specifies lateral neuroblasts in Caenorhabditis elegans. Second, orthologs of the vertebrate NPB specification module (Msx/vab-15, Pax3/7/pax-3, and Zic/ref-2) are significantly enriched in worm lateral neuroblasts. In addition, like in other bilaterians, the expression domain of Msx/vab-15 is more lateral than those of Pax3/7/pax-3 and Zic/ref-2 in C. elegans. Third, we show that Msx/vab-15 regulates the development of mechanosensory neurons derived from lateral neural progenitors in multiple invertebrate species, including C. elegans, Drosophila melanogaster, and Ciona intestinalis. We also identify a novel lateral neural border specifier, ZNF703/tlp-1, which functions synergistically with Msx/vab-15 in both C. elegans and Xenopus laevis. These data suggest a common origin of the molecular mechanism specifying lateral neural borders across bilaterians.
Footnotes
↵1Y.L., D.Z., T.H., and G.C. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: xiaoliu{at}mail.tsinghua.edu.cn.
Author contributions: Y.L., D.Z., T.H., and G.C. designed research; S.C., W.L., R.H., and B.D. performed research; H.B., T.L., and Q.F. analyzed data; and Q.T. and X.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1704194114/-/DCSupplemental.
Conserved regulatory module of neural borders
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