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

Abstract

The presence of an anteroposterior body axis is a fundamental feature of bilateria. Within this group, echinoderms have secondarily evolved pentameral symmetric body plans. Although all echinoderms present bilaterally symmetric larval stages, they dramatically rearrange their body axis and develop a pentaradial body plan during metamorphosis. Therefore, the location of their anteroposterior body axis in adult forms remains a contentious issue. Unlike other echinoderms, sea cucumbers present an obvious anteroposterior axis not rearranged during metamorphosis, thus representing an interesting group to study their anteroposterior axis patterning. Hox genes are known to play a broadly conserved role in anteroposterior axis patterning in deuterostomes. Here, we report the expression patterns of Hox genes from early development to pentactula stage in sea cucumber. In early larval stages, five Hox genes (AjHox1, AjHox7, AjHox8, AjHox11/13a, and AjHox11/13b) were expressed sequentially along the archenteron, suggesting that the role of anteroposterior patterning of the Hox genes is conserved in bilateral larvae of echinoderms. In doliolaria and pentactula stages, eight Hox genes (AjHox1, AjHox5, AjHox7, AjHox8, AjHox9/10, AjHox11/13a, AjHox11/13b, and AjHox11/13c) were expressed sequentially along the digestive tract, following a similar expression pattern to that found in the visceral mesoderm of other bilateria. Unlike other echinoderms, pentameral expression patterns of AjHox genes were not observed in sea cucumber. Altogether, we concluded that AjHox genes are involved in the patterning of the digestive tract in both larvae and metamorphosis of sea cucumbers. In addition, the anteroposterior axis in sea cucumbers might be patterned like that of other bilateria.

Anteroposterior molecular registries in ectoderm of the echinus rudiment

“…In echinoids, larvae lose larval mouth, foregut, hindgut, and anus during metamorphosis, whereas the adult digestive tract extends from the larval midgut/enteric sac in two directions along the mesentery to form adult mouth and anus (Hyman, ). In agreement, sequential hox expression was observed along the digestive tract in a sea cucumber (Kikuchi et al, ). According to this interpretation, the adult mouth–anus axis represents the AP axis in echinoderms, which corresponds with the AP/OA axis of the coelomic stacking model (Mooi and David, ; Peterson et al, ) in asteroids, echinoids, and holothuroids, because they form the adult anus on the aboral side.…”

Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited

“…A recent article on the holothuroid Apostichopus japonicus reports that Hox1 , Hox5 , Hox7 , Hox8 , Hox11/13a , Hox11/13b , and Hox11/13c are expressed at the blastula and gastrula stages (Kikuchi et al ). Most of these genes, in addition to Hox9/10 , are also expressed in the larvae including the terminal larva that transitions to the juvenile.…”

“…In the holothuroid, A. japonicus , Hox1 , Hox7 , and Hox11/13b are expressed in the ectoderm of the blastula or gastrula stages, whereas Hox8 is expressed in the endoderm of the archenteron (Kikuchi et al ). In larvae, Hox1 , Hox7 , Hox11/13b and Hox11/13c are expressed in the endoderm in an A/P array from Hox1 in the foregut to Hox11/13c in the hindgut.…”

“…In larvae, Hox1 , Hox7 , Hox11/13b and Hox11/13c are expressed in the endoderm in an A/P array from Hox1 in the foregut to Hox11/13c in the hindgut. Also in the larvae, Hox5 , Hox8 , Hox9/10 , Hox11/13a , Hox11/13b and Hox11/13c are expressed in the coelomic mesoderm (somatocoels) in an A/P array (Kikuchi et al ). Thus, in holothuroid development, Hox genes exhibit spatial colinear expression in endodermal (gut) and mesodermal (somatocoels) derivatives in nested domains following the order of the genes in the (ancestral‐type) cluster, with 3′ Hox genes expressed in anterior domains and 5′ Hox genes in posterior domains.…”

“…The new asteroid genomic sequence (Baughman et al ), together with our current understanding of echinoderm phylogeny (Fig. ) splitting the Echinozoa (echinoids + holothuroids) and Asterozoa (asteroids + ophiuroids) (Cannon et al ; Telford et al ; Reich et al ), and the recently reported Hox expression in holothuroids (Kikuchi et al ), prompted us to revisit the echinoderm HOX cluster, the role of these genes in development and the relationships between HOX cluster arrangement and body plan organization.…”