Unusual coelom formation in the direct‐type developing sand dollar Peronella japonica

Abstract

Peronella japonica is a sand dollar with a zygote that develops into an abbreviated pluteus but then metamorphoses on day three. The adult rudiment formation is unique; it uses a median position of the hydrocoel and a stomodeum-like invagination of vestibule that covers the dorsal side of the hydrocoel. However, the developmental processes underlying coelom formation remain unclear. In this study, we examined this process by reconstructing three-dimensional images from serial sections of larvae. We show that the left coelom developed by both schizocoely and enterocoely from the archenteron tip, whereas the hydrocoel and right coelom formed by enterocoely from the archenteron. This coelom formation arranged the coelomic compartments directly along the adult oral-aboral axis by skipping the initial bilateral phases. Furthermore, our data indicate P. japonica retains ancestral asymmetry along the left-right axis in the location of the adult rudiment.

Patterning of anteroposterior body axis displayed in the expression of Hox genes in sea cucumber Apostichopus japonicus

“…In the sea lily Metacrinus rotundus, the sequential expression of MrHox5, MrHox7, MrHox8, and MrHox9/10 along the anterior/posterior axis in mesodermal somatocoels has been observed in auricularia larvae (Hara et al 2006). In the sand dollar Peronella japonica, the five posterior Hox genes PjHox7, PjHox8, PjHox9/10, PjHox11/13a, and PjHox11/13b are known to be expressed in the left somatocoel in numerical order (Tsuchimoto and Yamaguchi, 2014) as observed in S. purpuratus . Here, we showed that the sea cucumber A. japonicus also expresses AjHox1, AjHox7, AjHox8, AjHox11/13a, and AjHox11/13b sequentially along the anteroposterior axis in early larval stages (Fig.…”

“…However, such sequential expression along the digestive tract has not been described in sea urchins. In addition, the sequential expression of PjHox7, PjHox8, PjHox9/10, PjHox11/13a, and PjHox11/13b in the sand dollar P. japonica is known to be downregulated after metamorphosis (Tsuchimoto and Yamaguchi 2014). The number of Hox genes sequentially expressing along the anteroposterior axis, together with the continuous sequential expression of Hox genes along the digestive tract after metamorphosis, might determine the obvious A/P axis observed in adult sea cucumber.…”

“…In echinoderms, previous studies on the molecular structure and the expression patterns of Hox genes have mainly focused on sea urchins (Popodi et al 1996;Arenas-Mena et al 1998;Hano et al 2001; Byrne 2005, 2014;Wilson et al 2005;Cameron et al 2006). Spatial sequential expression of Hox genes have been reported from two species, Strongylocentrotus purpuratus (Arenas- and Peronella japonica (Tsuchimoto and Yamaguchi 2014), based on gene expression in the somatocoel of the pluteus larva. In addition to sea urchins, spatial sequential expression patterns of Hox genes have been also described from the somatocoel of the auricularia larva of the sea lily Metacrinus rotundus (Hara et al 2006).…”

“…The order of expression of AjHox genes along the anteroposterior axis in pentactula larvae was similar to that observed in doliolaria larvae. Comprehensive analysis of Hox gene expression in echinoderm larvae has been reported in sea urchins (Arenas-Mena et al 1998Ishii et al 1999), sea lilies (Hara et al 2006), and sand dollars (Tsuchimoto and Yamaguchi 2014). In sea urchins, only Hox7 and Hox11/13b are known to be expressed in prism and early pluteus stages.…”

“…In sea stars, Hox4 is expressed in the pentaradial hydrocoel in juvenile (Cisternas and Byrne 2009). In the adult rudiment of echinoids, Hox1, Hox5, and Hox11/13b are expressed pentameraly in the vestibule ectoderm (adult ectoderm), and Hox3 is also expressed pentameraly in mesodermal tissue (dental sac and/or spine) (Arenas-Mena et al 1998;Byrne 2005, 2014;Tsuchimoto and Yamaguchi 2014). In S. purpuratus, unusual gene order and organization of the Hox cluster was reported: Hox4 is lost, Hox1, Hox2, and Hox3 are translocated to the opposite end of the cluster and their transcriptional orientation is inversed, while Hox5 and Hox11/13b are inversed in situ .…”