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Long-Term, Stochastic Editing of Regenerative Anatomy via Targeting Endogenous
Bioelectric Gradients
#MMPMID28538159
Durant F
; Morokuma J
; Fields C
; Williams K
; Adams DS
; Levin M
Biophys J
2017[May]; 112
(10
): 2231-2243
PMID28538159
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We show that regenerating planarians' normal anterior-posterior pattern can be
permanently rewritten by a brief perturbation of endogenous bioelectrical
networks. Temporary modulation of regenerative bioelectric dynamics in amputated
trunk fragments of planaria stochastically results in a constant ratio of
regenerates with two heads to regenerates with normal morphology. Remarkably,
this is shown to be due not to partial penetrance of treatment, but a profound
yet hidden alteration to the animals' patterning circuitry. Subsequent
amputations of the morphologically normal regenerates in water result in the same
ratio of double-headed to normal morphology, revealing a cryptic phenotype that
is not apparent unless the animals are cut. These animals do not differ from
wild-type worms in histology, expression of key polarity genes, or neoblast
distribution. Instead, the altered regenerative bodyplan is stored in seemingly
normal planaria via global patterns of cellular resting potential. This gradient
is functionally instructive, and represents a multistable, epigenetic anatomical
switch: experimental reversals of bioelectric state reset subsequent regenerative
morphology back to wild-type. Hence, bioelectric properties can stably override
genome-default target morphology, and provide a tractable control point for
investigating cryptic phenotypes and the stochasticity of large-scale epigenetic
controls.
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