Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates

Abstract

Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal axis of animal embryos. They are generally expressed in restricted spatial domains according to their position in the cluster (spatial colinearity)-a feature that is conserved across bilaterians. In jawed vertebrates (gnathostomes), the position in the cluster also determines the onset of expression of Hox genes (a feature known as whole-cluster temporal colinearity (WTC)), while in invertebrates this phenomenon is displayed as a subcluster-level temporal colinearity. However, little is known about the expression profile of Hox genes in jawless vertebrates (cyclostomes); therefore, the evolutionary origin of WTC, as seen in gnathostomes, remains a mystery. Here, we show that Hox genes in cyclostomes are expressed according to WTC during development. We investigated the Hox repertoire and Hox gene expression profiles in three different species-a hagfish, a lamprey and a shark-encompassing the two major groups of vertebrates, and found that these are expressed following a whole-cluster, temporally staggered pattern, indicating that WTC has been conserved during the past 500 million years despite drastically different genome evolution and morphological outputs between jawless and jawed vertebrates.

An atlas of anteriorhoxgene expression in the embryonic sea lamprey head:hox-code evolution in vertebrates

“…The two lamprey species examined to date both have 6 Hox clusters and appear to share an identical Hox gene complement, reflecting their close phylogenetic relationship (Kuraku and Kuratani, 2006; Mehta et al, 2013; Pascual-Anaya et al, 2018; Smith et al, 2018). Despite lamprey having 6 Hox clusters compared to 4 in most tetrapods, paralogue loss has resulted in the total number of Hox genes being similar between these taxa: 43 in lamprey and 39 in mouse (Fig.…”

“…For PG1-4, lamprey and mouse have both retained a remarkably similar number of genes in each paralogy group. It remains unclear precisely how the 6 lamprey Hox clusters relate to the 4 Hox clusters that were presumably present in the common ancestor of gnathostomes, and to the 4 clusters in mouse, since phylogenetic analyses could not resolve 1:1 orthology between lamprey and gnathostome Hox genes/proteins (Mehta et al, 2013; Pascual-Anaya et al, 2018; Smith et al, 2018). This does not necessarily imply that lamprey and gnathostome Hox clusters arose from independent duplication events, since ancient duplication, when followed quickly by lineage separation and subsequent divergence, coupled with species-specific patterns of codon and amino acid usage, could weaken the signal of these phylogenetic events (Qiu et al, 2011).…”

Evolution of vertebrate spinal cord patterning

“…Embryos grow from anterior to posterior via a tailbud, forming new somites and spinal cord over more than 2 weeks of development. RA appears to be synthesized by somite cells and Hox gene expression has been identified in the hindbrain and spinal cord, though posterior Hox genes have not been well studied …”

“…RA appears to be synthesized by somite cells 52 and Hox gene expression has been identified in the hindbrain and spinal cord, though posterior Hox genes have not been well studied. 100,102,126 Some Ciona Hox genes are expressed in the CNS, but the ascidian Hox cluster is fragmented 127,128 and this is not an ancestral state. Manipulation of RA and FGF signaling in Ciona can affect AP patterning, including Hox expression.…”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…This is especially intriguing taking into account that Ph. australis has highly organized Hox cluster and collinear expression (especially in its temporal aspect) has been proposed as a main evolutionary factor responsible for conservation of organization of Hox cluster (9,(11)(12)(13)(14)(15)(16)49). Therefore, either another mechanism is responsible for Hox cluster conservation in Phoronida or the two discussed phoronid species varies greatly in the cluster organization and/or Hox gene expression patterns.…”