Degenerate evolution of the hedgehog gene in a hemichordate lineage

Abstract

The discovery of a set of highly conserved genes implicated in patterning during animal development represents one of the most striking findings from the field of evolutionary developmental biology. Existence of these ''developmental toolkit'' genes in diverse taxa, however, does not necessarily imply that they always perform the same functions. Here, we demonstrate functional evolution in a major toolkit gene. hedgehog (hh) encodes a protein that undergoes autocatalytic cleavage, releasing a signaling molecule involved in major developmental processes, notably neural patterning. We find that the hh gene of a colonial pterobranch hemichordate, Rhabdopleura compacta, is expressed in a dramatically different pattern to its ortholog in a harrimaniid enteropneust hemichordate, Saccoglossus kowalevskii. These represent two of the three major hemichordate lineages, the third being the indirect developing ptychoderid enteropneusts. We also show that the normally well-conserved amino acid sequence of the autoproteolytic cleavage site has a derived change in S. kowalevskii. Using ectopic expression in Drosophila, we find that this amino acid substitution reduces the efficiency of Hh autocatalytic cleavage and its signaling function. We conclude that the Hh sequence and expression in S. kowalevskii represent the derived state for deuterostomes, and we argue that functional evolution accompanied secondary reduction of the central nervous system in harrimaniids.autoproteolysis ͉ central nervous system ͉ molecular evolution ͉ pterobranch ͉ Saccoglossus

Hemichordata

“…This will provide an important resource to identify the genetic toolkit and regulatory elements of acorn worms. Protocols have been developed and optimised for whole mount or section in situ hybridisation or immunocytochemistry and are now routinely applied on several hemichordate species (Tagawa et al 1998b ;Okai et al 2000 ;Lowe et al 2003 ;Smith et al 2003 ;Sato et al 2009 ;Miyamoto et al 2010 ;Miyamoto and Wada 2013 ). In order to determine relative spatial gene expression for a set of genes, double fl uorescent in situ hybridisation has been developed in S. kowalevskii (Pani et al 2012 ).…”

“…Within the last couple of years, Sato and colleagues have begun to develop Rhabdopleura compacta , a species that can be found in the south of England, as an emerging model organism that can be used for developmental studies (Sato et al , 2009.…”

Evolutionary crossroads in developmental biology: hemichordates

“…It was not until their discovery in shallow waters that their development was thoroughly characterized (Stebbing, 1970;Dilly, 1973;Lester, 1988b;Lester, 1988a). Recently, Sato and colleagues have begun to develop the pterobranch Rhabdopleura compacta as an important new hemichordate species that is amenable to developmental studies Sato et al, 2009). How and when fertilization occurs remains unknown, but developing larvae of this species can be observed year round, with a peak between April and July.…”

“…However, more recently, pterobranchs (Fig. 2C) as represented by Rhabdopleura compacta and other indirect-developing enteropneusts such as Balanoglossus misakiensis and Balanoglossus simodensis are being developed as valuable additional models, ensuring that, in the future, no one species is over emphasized in comparative analyses Ikuta et al, 2009;Sato et al, 2009;.…”

Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite

“…2009). Recent discovery of a degenerate form of the major body patterning gene hedgehog in Saccoglossus kowalevskii and comparison with its less‐modified ortholog in Rhabdopleura compacta suggests that this gene has a uniquely derived form in S. kowalevskii , the evolution of which has paralleled the evolution of the unique morphological features of the harrimanid enteropneusts (Sato et al. 2009).…”