Evolutionary perspectives from development of mesodermal components in the lamprey

Abstract

Lampreys, a jawless vertebrate species, lack not only jaws but also several other organs, including ventral migratory muscles shared by gnathostomes. In the lamprey embryo, the mesoderm consists primarily of unsegmented head mesoderm, segmented somites, and yet uncharacterized lateral plate mesoderm, as in gnathostomes. Although the adult lamprey possesses segmented myotomes in the head, the head mesoderm of this animal is primarily unsegmented, similar to that in gnathostomes. In the trunk, the large part of lamprey somites is destined to form myotomes, and the Pax3/7 gene expression domain in the lateral part of somites is suggested to represent a dermomyotome homologue. Lamprey myotomes are not segregated by a horizontal myoseptum, which has been regarded as consistent with the apparent absence of a migratory population of hypaxial muscles shared by gnathostomes. However, recent analysis suggests that lampreys have established the gene regulatory cascade necessary for the ventrally migrating myoblasts, which functions in part during the development of the primordial hypobranchial muscle. There have also been new insights on the developmental cascade of lamprey cartilages, in which the Sox family of transcription factors plays major roles, as in gnathostomes. Thus, mesoderm development in lampreys may represent the ancestral state of gene regulatory mechanisms required for the evolution of the complex and diverse body plan of gnathostomes. Developmental Dynamics 236:2410 -2420, 2007.

Programmed loss of millions of base pairs from a vertebrate genome

“…The results presented here suggest that considering the germline genome structure and how somatic changes alter this structure when using lamprey as a model for comparative developmental and genomic studies will be especially important. With ongoing progress toward complete sequencing of the lamprey somatic genome (21) and the recent development of several techniques for performing genetic manipulations of lamprey embryos (17)(18)(19)(20), we anticipate that the lamprey genome will prove fertile ground for identifying mechanisms that mediate the differential development of cell lineages and participate in large-scale rearrangement and stabilization of vertebrate genomes.…”

“…Experimentally validated computational screens for other germline-limited sequences uncovered several additional sequences that are lost during developmental restructuring of the lamprey genome, including one sequence that is homologous to SPOPL (speckle-type POZ protein-like) genes, which is transcribed in lamprey testes and lost during embryonic development. The presence of predictable and extensive reorganization events within the genome of the lamprey, coupled with its high fecundity (16) and amenable embryology (17)(18)(19)(20), present a uniquely tractable system for understanding the dynamics of genome stability and the consequences of reorganization in the context of ''normal'' vertebrate development and cell biology.…”

An eye on the head: the development and evolution of craniofacial muscles

“…With respect to the MRFs, a single ancestor was proposed to be conserved from Drosophila to jellyfish to tunicates (Atchley et al, 1994), undergoing two rounds of duplication events to yield the current MRFs in vertebrates. As for Pitx2, the AmphiPitx gene is not expressed in the expected region in the developing larval head (Yasui et al, 2000), but the lamprey Pitx (orthologue of Pitx1 or Pitx2) is expressed in the pre-mandibular mesoderm that apparently gives rise to EOMs (Boorman and Shimeld, 2002;Kusakabe and Kuratani, 2007). However, the development of the lamprey EOMs is not yet well understood, therefore, further investigation of lamprey craniofacial development could lead to a better understanding of EOM ontology in vertebrates.…”

Myogenic waves and myogenic programs during Xenopus embryonic myogenesis

“…The head somites or cavities present in the jawless fish lamprey and in the elasmobranchs could be the remnants of amphioxus somites (Holland et al, 2008). However, debates about evolutionary relationships between head mesodermal segments in these different species are still controversial (Kusakabe and Kuratani, 2007). The presence of head cavities is contested in lamprey and could be a synapomorphy in elasmobranchs (Kuratani, 2008).…”