Embryos assist morphogenesis of others through calcium and ATP signaling mechanisms in collective teratogen resistance

Angela Tung, Megan M. Sperry, Wesley Clawson, Ananya Pavuluri, Sydney Bulatao, Michelle Yue, Ramses Martinez Flores, Vaibhav P. Pai, Patrick McMillen, Franz Kuchling and Michael Levin ()
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Angela Tung: Allen Discovery Center at Tufts University
Megan M. Sperry: Allen Discovery Center at Tufts University
Wesley Clawson: Allen Discovery Center at Tufts University
Ananya Pavuluri: Allen Discovery Center at Tufts University
Sydney Bulatao: Allen Discovery Center at Tufts University
Michelle Yue: Wyss Institute for Biologically Inspired Engineering, Harvard University
Ramses Martinez Flores: Wyss Institute for Biologically Inspired Engineering, Harvard University
Vaibhav P. Pai: Allen Discovery Center at Tufts University
Patrick McMillen: Allen Discovery Center at Tufts University
Franz Kuchling: Allen Discovery Center at Tufts University
Michael Levin: Allen Discovery Center at Tufts University

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: Abstract Information for organismal patterning can come from a variety of sources. We investigate the possibility that instructive influences for normal embryonic development are provided not only at the level of cells within the embryo, but also via interactions between embryos. To explore this, we challenge groups of embryos with disruptors of normal development while varying group size. Here, we show that Xenopus laevis embryos are much more sensitive to a diverse set of chemical and molecular-biological perturbations when allowed to develop alone or in small groups, than in large groups. Keeping per-embryo exposure constant, we find that increasing the number of exposed embryos in a cohort increases the rate of survival while incidence of defects decreases. This inter-embryo assistance effect is mediated by short-range diffusible signals and involves the P2 ATP receptor. Our data and computational model emphasize that morphogenesis is a collective phenomenon not only at the level of cells, but also of whole bodies, and that cohort size is a crucial variable in studies of ecotoxicology, teratogenesis, and developmental plasticity.

Date: 2024
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DOI: 10.1038/s41467-023-44522-2

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