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Proc Natl Acad Sci U S A. 2019 Jun 25;116(26):12925-12932. doi: 10.1073/pnas.1901919116. Epub 2019 Jun 12.

BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates.

Author information

1
Institute of Cellular and Organismic Biology, Academia Sinica, 11529 Taipei, Taiwan; yhsu@gate.sinica.edu.tw jkyu@gate.sinica.edu.tw.
2
Institute of Cellular and Organismic Biology, Academia Sinica, 11529 Taipei, Taiwan.
3
Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 26242 Yilan, Taiwan.

Abstract

A defining feature of chordates is the unique presence of a dorsal hollow neural tube that forms by internalization of the ectodermal neural plate specified via inhibition of BMP signaling during gastrulation. While BMP controls dorsoventral (DV) patterning across diverse bilaterians, the BMP-active side is ventral in chordates and dorsal in many other bilaterians. How this phylum-specific DV inversion occurs and whether it is coupled to the emergence of the dorsal neural plate are unknown. Here we explore these questions by investigating an indirect-developing enteropneust from the hemichordate phylum, which together with echinoderms form a sister group of the chordates. We found that in the hemichordate larva, BMP signaling is required for DV patterning and is sufficient to repress neurogenesis. We also found that transient overactivation of BMP signaling during gastrulation concomitantly blocked mouth formation and centralized the nervous system to the ventral ectoderm in both hemichordate and sea urchin larvae. Moreover, this mouthless, neurogenic ventral ectoderm displayed a medial-to-lateral organization similar to that of the chordate neural plate. Thus, indirect-developing deuterostomes use BMP signaling in DV and neural patterning, and an elevated BMP level during gastrulation drives pronounced morphological changes reminiscent of a DV inversion. These findings provide a mechanistic basis to support the hypothesis that an inverse chordate body plan emerged from an indirect-developing ancestor by tinkering with BMP signaling.

KEYWORDS:

BMP; chordate origins; dorsoventral patterning; indirect-developing hemichordates; neural patterning

PMID:
31189599
PMCID:
PMC6600983
[Available on 2019-12-12]
DOI:
10.1073/pnas.1901919116

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