The planarian dorsal–ventral boundary regulates anterior–posterior axis growth and patterning

TL;DR

This study shows how the dorsal-ventral boundary in planarians controls the growth and patterning of the front-back body axis during regeneration.

Contribution

The study reveals a hierarchical model where the dorsal-ventral boundary directs anterior-posterior axis formation during regeneration.

Findings

The dorsal-ventral boundary (DVB) is necessary and sufficient for anterior-posterior axis growth in low Wnt conditions.

Ectopic DVB can induce head formation at experimentally dictated locations after Wnt inhibition.

DVB removal blocks anterior positional information during head regeneration.

Abstract

Regeneration can involve the coordination of pattern formation in an outgrowth with the spatial pattern of pre-existing tissues, such as along body axes. Planarian adult axis patterning serves as a robust context for uncovering the mechanisms of such pattern integration. We investigated how the dorsal–ventral boundary (DVB), which surrounds the animal periphery at the dorsal–ventral (DV) median plane, regulates anterior–posterior (AP) axis growth and patterning. We define a spatial DVB gene expression atlas that includes genes encoding signaling, adhesion, and transcription factors. Wnt inhibition results in anterior positional information induction and ectopic head formation that is restricted to the DVB. DVB can be transplanted, and DVB identity can be experimentally induced at ectopic locations. Ectopic DVB is competent for anterior positional identity induction following Wnt inhibition, enabling the generation of animals with ectopic heads at experimentally dictated locations. DVB removal blocks the anteriorization that normally follows Wnt inhibition and prevents anterior positional information expression during head regeneration. Anterior positional information induction at the DVB after Wnt inhibition occurs independently from anterior pole formation, which promotes head patterning in regeneration. Our findings reveal a hierarchical model of pattern integration across body axes in which DV patterning is central by producing a DVB with competence to direct formation of large AP axis regions. This mechanism enables coordination of orthogonal positional information in the context of regeneration.

Regeneration in planarians requires alignment of new tissue axes with existing body axes. This study shows that such pattern integration is coordinated by the dorsal–ventral boundary (DVB). The DVB is necessary and sufficient for anterior–posterior axis outgrowth and patterning in a low Wnt environment.

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