Nervous System and Tissue Polarity Dynamically Adapt to New Morphologies in Planaria

Abstract

1The coordination of tissue-level polarity with organism-level polarity is crucial in development, 2 disease, and regeneration. Exploiting the flexibility of the body plan in regenerating planarians, we used 3 mirror duplication of the primary axis to show how established tissue-level polarity adapts to new 4 organism-level polarity. Tracking of cilia-driven flow to characterize planar cell polarity of the epithelium 5 revealed a remarkable reorientation of tissue polarity in double-headed planarians. This reorientation is 6 driven by signals produced by the intact brain and is not hampered by radiation-induced removal of stem 7 cells. The nervous system itself adapts its polarity to match the new organismal anatomy in these animals 8 as revealed by distinct regenerative outcomes driven by polarized nerve transport. Thus, signals from the 9 central nervous system can dynamically control and re-orient tissue-level polarity to match the organism-10 level anatomical configuration, illustrating a novel role of the nervous system in the regulation of 11 patterning. 12 13 14 6 130 Figure 1: Flow driven by the multiciliated epithelium can be tracked and epithelial polarity dynamically remodels 131 in DH animals. A) (i) Morphological differences in head development in DHs can be observed at Day 7 (days after 132 amputation -dpa), revealing that the primary head (ii) is more developed than the secondary head (iii). (iv) In DHs 133 at Day 49 both heads (v, vi) are equally developed. Scale bars 1 mm. B) Cilia of the multiciliated ventral surface 134 epithelium stained with antibody against acetylated-tubulin at (i) low and (ii) high magnification. Scale bar 100 μm 135 in (i) and 25 μm in (ii). C) Flow driven by cilia beat can be visualized with carmine powder and tracked with particle 136 image velocimetry (PIV) in a single-headed animal (red arrows). D) Opposing flow directions in DH animals lead to 137 the accumulation of particles at the point where the opposing flow fields meet. This "collision zone" (asterisk) 138 repositions towards the middle of the animal from Day 7 until Day 49. E) Plot of position of the collision zone as 139

Does regeneration recapitulate phylogeny? Planaria as a model of body-axis specification in ancestral eumetazoa

“…in the "posterior" direction from each head [31] as shown in Figure 1a. The nervous system is also duplicated, with both copies functional in directing behavior [72]. Crucially, the VNCs are not only duplicated but are continuous across the duplication point, yielding a nervous system with two complete brains connected by two uninterrupted and apparently fully functional VNCs [31,65,72].…”

“…The nervous system is also duplicated, with both copies functional in directing behavior [72]. Crucially, the VNCs are not only duplicated but are continuous across the duplication point, yielding a nervous system with two complete brains connected by two uninterrupted and apparently fully functional VNCs [31,65,72]. Hence, not only has a head grown from the posterior wound, but the entire anatomy anterior to the anterior-facing wound has been duplicated from the posterior wound.…”

“…The axis of rotation is the preserved D-V axis. This "rotation" of the A-P axis is implemented by regenerative growth from the posterior-facing blastema, while regenerative growth from the anterior-facing blastema reproduces the original A-P axis [31,65,72]. Symmetrization of the A-P axis does not erase the distinction between anterior and posterior; it rather duplicates it to produce a bidirectional A-P-A axis with its midpoint at 70% of the original length.…”

An insight into planarian regeneration

“…Levin et al created double head planarians to demonstrate the flexibility of the body polarity. By visualizing the orientation of cilia beat and cilia‐driven flow in living planarians, they found that ciliary beat reorientated within several weeks to match the new axial body plan, and the progresses is independent from cilia beating 38 …”

Bistability of somatic pattern memories: stochastic outcomes in bioelectric circuits underlying regeneration

“…Indeed, the basic phenomenon of head/tail regeneration reveals that it is not a local, cell-level decision because the two wounds produced by bisection of a normal worm have radically different anatomical outcomes (head from one wound, tail from the other) despite the fact that the cells were immediately adjacent neighbours before the cut and thus were at the same positional information level along the axis. Thus, proper regeneration in the normal case, as in the modified scenarios described above, requires cells to communicate across significant distances to determine what structures exist, and which must be made anew [62,81,85,86].…”