Echiuran Hox genes provide new insights into the correspondence between Hox subcluster organization and collinearity pattern

Abstract

In many bilaterians, Hox genes are generally clustered along the chromosomes and expressed in spatial and temporal order. In vertebrates, the expression of Hox genes follows a whole-cluster spatio-temporal collinearity (WSTC) pattern, whereas in some invertebrates the expression of Hox genes exhibits a subcluster-level spatio-temporal collinearity pattern. In bilaterians, the diversity of collinearity patterns and the cause of collinearity differences in Hox gene expression remain poorly understood. Here, we investigate genomic organization and expression pattern of Hox genes in the echiuran worm Urechis unicinctus (Annelida, Echiura). Urechis unicinctus has a split cluster with four subclusters divided by non-Hox genes: first subcluster ( Hox1 and Hox2 ), second subcluster ( Hox3 ), third subcluster ( Hox4 , Hox5 , Lox5 , Antp and Lox4 ), fourth subcluster ( Lox2 and Post2 ). The expression of U. unicinctus Hox genes shows a subcluster-based whole-cluster spatio-temporal collinearity (S-WSTC) pattern: the anterior-most genes in each subcluster are activated in a spatially and temporally colinear manner (reminiscent of WSTC), with the subsequent genes in each subcluster then being very similar to their respective anterior-most subcluster gene. Combining genomic organization and expression profiles of Hox genes in different invertebrate lineages, we propose that the spatio-temporal collinearity of invertebrate Hox is subcluster-based.

Seeking Sense in the Hox Gene Cluster

“…Evidence for this is largely circumstantial and is that species displaying temporal collinearity have so far been found to have an intact, unbroken Hox gene cluster. Studies on the annelid Urechis unicinctus perhaps provide some evidence against this [ 52 ]. Its posterior Hox genes ( Lox2 and Post2 ) are separated from more anterior genes ( Hox1 to Lox4 ) by greater than 1Mb, as sub-clusters, yet the genes as a whole display spatial and temporal collinearities [ 52 ].…”

“…Studies on the annelid Urechis unicinctus perhaps provide some evidence against this [ 52 ]. Its posterior Hox genes ( Lox2 and Post2 ) are separated from more anterior genes ( Hox1 to Lox4 ) by greater than 1Mb, as sub-clusters, yet the genes as a whole display spatial and temporal collinearities [ 52 ]. Conversely, however, an intact cluster need not necessarily imply temporal collinearity.…”

EDomics: a comprehensive and comparative multi-omics database for animal evo-devo

“…ctenophore Mnemiopsis leidyi , placozoan Trichoplax adhaerens , ascidian Ciona robusta [ Ciona intestinalis type A] and mollusc Patinopecten yessoensis ) ( 7 , 8 ). Recently, the use of non-model organisms in evo-devo studies has generated many breakthrough findings or new theories, such as Hox subcluster-mediated body plan diversification ( 9 , 10 ), the convergent evolution of bilaterian nerve cords ( 11 ), the origin of animal multicellularity with pluripotency ( 12 ), the single intercalation origin of metazoan larvae ( 13 ), and the evolution of ancient homomorphic sex chromosomes ( 14 ). Although large amounts of multi-omics resources have been accumulated, which are rapidly increasing in diverse animal groups, integrative access and utilization of these scatteredly deposited genomic resources pose a great challenge for the animal evo-devo research community.…”

Identification and validation of the reference genes in the echiuran worm Urechis unicinctus based on transcriptome data

“…, and sul de metabolism [25] because of its characteristics such as a large number of eggs laid, high fertilization rate, biphasic life cycle, and high sul de tolerance ability. Recently, the use of U. unicinctus in evo-devo studies has generated many breakthrough [23,24,26]. Evolutionary transcriptome analysis of the trochophores of U. unicinctus and other metazoan animals reveal an adult-rst evolutionary scenario with a single metazoan larval intercalation [23].…”

“…Hox-mediated body plan diversi cation is an important developmental process [26]. In U. unicinctus, the expression of Hox genes exhibits a subcluster-based whole-cluster spatio-temporal collinearity pattern, suggesting that Hox subcluster play an important role in spatio-temporal collinearity pattern in invertebrates [24]. On the other hand, as a species living in the intertidal zone, U. unicinctus can tolerate, metabolize and utilize environmental sul de and is considered a model species for sul de adaptation [25,[27][28][29][30][31][32][33][34][35][36].…”