Genomic analysis of Hox clusters in the sea lamprey Petromyzon marinus

Abstract

The sea lamprey Petromyzon marinus is among the most primitive of extant vertebrates. We are interested in the organization of its Hox gene clusters, because, as a close relative of the gnathostomes, this information would help to infer Hox cluster organization at the base of the gnathostome radiation. We have partially mapped the P. marinus Hox clusters using phage, cosmid, and P1 artificial chromosome libraries. Complete homeobox sequences were obtained for the 22 Hox genes recovered in the genomic library screens and analyzed for cognate group identity. We estimate that the clusters are somewhat larger than those of mammals (roughly 140 kbp vs. 105 kbp) but much smaller than the single Hox cluster of the cephalochordate amphioxus (at more than 260 kb). We never obtained more than three genes from any single cognate group from the genomic library screens, although it is unlikely that our screen was exhaustive, and therefore conclude that P. marinus has a total of either three or four Hox clusters. We also identify four highly conserved non-coding sequence motifs shared with higher vertebrates in a genomic comparison of Hox 10 genes.

Timing and mechanism of ancient vertebrate genome duplications – the adventure of a hypothesis

“…Both hagfish and lamprey genomes have been sampled so far mainly for Hox genes. Lamprey has at least four Hox clusters [53,54]. One study suggests that at least one Hox-cluster duplication occurred before the divergence of gnathostome and jawless vertebrates, whereas an independent cluster duplication occurred in the lamprey lineage, after it diverged from the gnathostome lineage [53].…”

“…The existence of one HoxA and one HoxD cluster (which implies that HoxB and HoxC should be present) in shark (Heterodontus francisci) places the 2R duplication before the emergence of cartilaginous fish [62]. For information on the number of Hox clusters in other species, see the following references: lamprey (Petromyzon marinus) [53,54], hagfish (Eptatretus stoutii) [61], zebrafish (Danio rerio) [50], pufferfish (S. nephalus) [51], medaka (Oryzia latipes) [52], Ciona (Ciona intestinalis) [79], coelocanth (Latimeria menadoensis) [80], amphioxus (Branchiostoma floridae) [3].…”

Organization of Hox genes in ascidians: Present, past, and future

“…The cluster organization of Hox genes has been investigated in a variety of chordates: larvacean (Seo et al, 2004), amphioxus (Garcia-Fernandez and Holland, 1994;Ferrier et al, 2000), lamprey (Force et al, 2002;Irvine et al, 2002), horn shark (Kim et al, 2000;Chiu et al, 2002), coelacanth (Koh et al, 2003), ray-fin fish, bichir (Chiu et al, 2004), zebrafish (Amores et al, 1998;Chiu et al, 2002), medaka (Misof and Wagner, 1996), cichlid (Malaga-Trillo and Meyer, 2001), puffer fish (Aparicio et al, 1997), newt (Belleville et al, 1992), mouse (Duboule and Dolle, 1989), and human (Acampora et al, 1989). Nonchordate Hox clusters have been reported with Drosophila (Lewis, 1978;Von Allmen et al, 1996), mosquito (Devenport et al, 2000;Powers et al, 2000), red flour beetle (Brown et al, 2002), silk moth (Ueno et al, 1992), a grasshopper (Ferrier and Akam, 1996), nematode, Caenorhabditis elegans (Wang et al, 1993;Van Auken et al, 2000), ribbon worm (Kmita-Cunisse et al, 1998), and sea urchin (Popodi et al, 1996;Martinez et al, 1999).…”

The duplication of the Hox gene clusters in teleost fishes*1

“…Higher ray-finned fishes, however, have 6 or 7 Hox clusters that arose by means of duplication from the ancestral gnathostome clusters [3]. The two agnathan lineages, lampreys and hagfish, also exhibit multiple Hox clusters which, however, apparently arose through duplication events independent of those leading to the gnathostome clusters [24,15,16,63]. Since Ohno's book on the role of gene duplication in evolution, the idea that gene and genome duplication played a major role in the origin of vertebrates has grown in support [46].…”