BMP signaling is required for amphioxus tail regeneration

Abstract

Amphioxus, a cephalochordate, is an ideal animal in which to address questions about the evolution of regenerative ability and the mechanisms behind the invertebrate to vertebrate transition in chordates. However, the cellular and molecular basis of tail regeneration in amphioxus remains largely ill-defined. We confirmed that the tail regeneration of amphioxus Branchiostoma japonicum is a vertebrate-like epimorphosis process. We performed transcriptome analysis of tail regenerates, which provided many clues for exploring the mechanism of tail regeneration. Importantly, we showed that BMP2/4 and its related signaling pathway components are essential for the process of tail regeneration, revealing an evolutionarily conserved genetic regulatory system involved in regeneration in many metazoans. We serendipitously discovered that bmp2/4 expression is immediately inducible by general wounds and that expression of bmp2/4 can be regarded as a biomarker of wounds in amphioxus. Collectively, our results provide a framework for understanding the evolution and diversity of cellular and molecular events of tail regeneration in vertebrates.

Tail regeneration in a cephalochordate, the Bahamas lancelet,Asymmetron lucayanum

“…The more recent studies of cephalochordate tail regeneration have concerned Branchiostoma lanceolatum cultured at 19°C (Somorjai, 2017; Somorjai et al, 2012) and B. japonicum (Liang et al, 2019) cultured at an unreported temperature. For both, the rate of tail regrowth was considerably slower than in A. lucayanum maintained at 28 ° C. For example, the regeneration stage reached in 4 days in A. lucayanum was equivalent to that reached in 14 days and 25 days, respectively, in B. lanceolatum and B. japonicum .…”

“…There are three genera of cephalochordates (Nishikawa, 2018). Their regeneration is best known for Branchiostoma (Bieberhofer, 1906; Bone & Azariah, 1992; Kaneto & Wada, 2011; Liang, Rathnayake, Huyang, Pathirana, & Zhang, 2019; Pegeta, 1992; Probst, 1930; Silva, Mendes, & Mariano, 1995; Somorjai, 2017; Somorjai, Somorjai, Garcia‐Fernàndez, & Escrivà, 2012), with only a single study being devoted to Asymmetron (Andrews, 1893) and none to Epigonichthys . This taxonomically lop‐sided coverage is unfortunate because details about regeneration can sometimes differ between close relatives.…”

The Diversity of Muscles and Their Regenerative Potential across Animals

“…As demonstrated in other organisms, amphioxus regeneration can vary among body parts and several variables affect the speed of healing such as species, animal age, and body size [ 146 , 147 , 148 , 149 ]. In amphioxus, two districts show the highest regenerative capacity: the oral cirri, skeletal structures surrounding the mouth, and the post-anal tail.…”

“…From a mechanistic viewpoint, Somorjai and coworkers [ 146 , 147 ] described a blastema-like structure in the amputated tail of B. lanceolatum , with proliferating cells from notochord, myotomes and nerve cord positive for phospho-histone H3. Subsequently, Liang and coworkers [ 148 ] confirmed cell proliferation in blastemal cells of the regenerating tail of B. japonicum by Bromodeoxyuridine (BrdU) labeling.…”

“…Thus, oral cirri seem to undergo tissue remodeling by morphallaxis, whereas the tail can respond to amputation injury by epimorphic regeneration. In addition, de-differentiation of existing structures but not trans-differentiation or lineage reprogramming seems to occur during amphioxus tail regeneration, as seen in amphibians [ 146 , 147 ].…”