The phenomenon of whole body regeneration (WBR) from minute soma fragments is a rare
event in chordates, confined to the subfamily of botryllid ascidians and is poorly
understood on the cellular and molecular levels. We assembled a list of 1326 ESTs
from subtracted mRNA, at early stages of Botrylloides leachi WBR, and classified them
into functional categories. Sixty-seven (15%) ESTs with roles in innate immunity signaling
were classified into a broad functional group, a result supported by domain search
and RT-PCR reactions. Gene ontology analysis for human homologous to the immune gene
category, identified 22 significant entries, of which "peptidase activity" and "protease
inhibitor activity", stood out as functioning during WBR. Analyzing expressions of
serine protease Bl-TrSP, a representative candidate gene from the "peptidase activity"
subgroup, revealed low transcript levels in naïve vasculature with upregulated expression
during WBR. This was confirmed by in situ hybridization that further elucidated staining
restricted to a circulating population of macrophage cells. Furthermore, Bl-TrSP was
localized in regeneration niches within vasculature, in regenerating buds, and in
buds, during blastogenesis. Functional inhibition of serine protease activity disrupts
early remodeling processes of the vasculature microenvironment and hinders WBR. Comparison
of genome-wide transcription of WBR with five other developmental processes in ascidians
(including metamorphosis, budding and blastogenesis), revealed a broad conservation
of immune signaling expressions, suggesting a ubiquitous route of harnessing immune-related
genes within a broader range of tunicate developmental context. This, in turn, may
have enabled the high diversity of life history traits represented by urochordate
ascidians.