Evolutionary biology: lamprey Hox genes and the evolution of jaws.
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Amino Acid Sequence↗
Biomedical subjects
Shigeru Kuratani
Publications and source records attributed to Shigeru Kuratani.
Lamprey contractile protein genes mark different populations of skeletal muscles during development.
Agnathan lampreys retain ancestral characteristics of vertebrates in the morphology of skeletal muscles derived from two mesodermal regions: trunk myotomes and unsegmented head mesoderm. During lamprey development, some populations of myoblasts migrate via pathways that differ from those of gnathostomes. To investigate the evolution of skeletal muscle differentiation in vertebrates, we characterize multiple contractile protein genes expressed in the muscle cells of the Japanese lamprey, Lethenteron japonicum. Lamprey actin gene LjMA2, and myosin heavy chain (MyHC) genes LjMyHC1 and LjMyHC2 are all expressed in the developing skeletal muscle cells of early embryos. However, LjMyHC1 and LjMyHC2 are expressed only in cells originating from myotomes, while LjMA2 is expressed in both myotomal and head musculature. Thus, in lampreys, myotomes and head mesoderm differ in the use of genes encoding contractile protein isoforms. Phylogenetic tree analyses including lamprey MyHCs suggest that the variety of muscle MyHC isoforms in different skeletal muscles may correspond to the morphological complexity of skeletal muscles of different vertebrate species. Another lamprey actin gene LjMA1 is likely to be the first smooth muscle actin gene isolated from non-tetrapods. We conclude that, in vertebrate evolution, the different regulatory systems for striated and smooth muscle-specific genes may have been established before the agnathan/gnathostome divergence.
Actins↗
Evolution of the vertebrate jaw: comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty.
It is generally believed that the jaw arose through the simple transformation of an ancestral rostral gill arch. The gnathostome jaw differentiates from Hox-free crest cells in the mandibular arch, and this is also apparent in the lamprey. The basic Hox code, including the Hox-free default state in the mandibular arch, may have been present in the common ancestor, and jaw patterning appears to have been secondarily constructed in the gnathostomes. The distribution of the cephalic neural crest cells is similar in the early pharyngula of gnathostomes and lampreys, but different cell subsets form the oral apparatus in each group through epithelial-mesenchymal interactions: and this heterotopy is likely to have been an important evolutionary change that permitted jaw differentiation. This theory implies that the premandibular crest cells differentiate into the upper lip, or the dorsal subdivision of the oral apparatus in the lamprey, whereas the equivalent cell population forms the trabecula of the skull base in gnathostomes. Because the gnathostome oral apparatus is derived exclusively from the mandibular arch, the concepts 'oral' and 'mandibular' must be dissociated. The 'lamprey trabecula' develops from mandibular mesoderm, and is not homologous with the gnathostome trabecula, which develops from premandibular crest cells. Thus the jaw evolved as an evolutionary novelty through tissue rearrangements and topographical changes in tissue interactions.
Animals↗
Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain.
During development, the vertebrate hindbrain is subdivided along its anteroposterior axis into a series of segmental bulges called rhombomeres. These segments in turn generate a repeated pattern of rhombomere-specific neurons, including reticular and branchiomotor neurons. In amphioxus (Cephalochordata), the sister group of the vertebrates, a bona fide segmented hindbrain is lacking, although the embryonic brain vesicle shows molecular anteroposterior regionalization. Therefore, evaluation of the segmental patterning of the central nervous system of agnathan embryos is relevant to our understanding of the origin of the developmental plan of the vertebrate hindbrain. To investigate the neuronal organization of the hindbrain of the Japanese lamprey, Lethenteron japonicum, we retrogradely labeled the reticulospinal and branchial motoneurons. By combining this analysis with a study of the expression patterns of genes identifying specific rhombomeric territories such as LjKrox20, LjPax6, LjEphC and LjHox3, we found that the reticular neurons in the lamprey hindbrain, including isthmic, bulbar and Mauthner cells, develop in conserved rhombomere-specific positions, similar to those in the zebrafish. By contrast, lamprey trigeminal and facial motor nuclei are not in register with rhombomere boundaries, unlike those of gnathostomes. The trigeminal-facial boundary corresponds to the rostral border of LjHox3 expression in the middle of rhombomere 4. Exogenous application of retinoic acid (RA) induced a rostral shift of both the LjHox3 expression domain and branchiomotor nuclei with no obvious repatterning of rhombomeric segmentation and reticular neurons. Therefore, whereas subtype variations of motoneuron identity along the anteroposterior axis may rely on Hox-dependent positional values, as in gnathostomes, such variations in the lamprey are not constrained by hindbrain segmentation. We hypothesize that the registering of hindbrain segmentation and neuronal patterning may have been acquired through successive and independent stepwise patterning changes during evolution.
Animals↗
Development of the adenohypophysis in the lamprey: evolution of epigenetic patterning programs in organogenesis.
In gnathostomes, the adenohypophysis, a component of the hypothalamo-hypophysial complex, is believed to develop through hierarchically organized epigenetic interactions based primarily on the topographical relationships between tissues. From a comparison of developmental processes and gene expression patterns of pituitary-related genes between the agnathan species, lampreys and gnathostomes, we speculate on the evolutionary pathway of the vertebrate adenohypophysis. In the lamprey, this is derived from the nasohypophysial placode (NHP) that develops anterior to the oral ectoderm. The NHP can be identified by the expression of LjPitxA, before actual histogenesis, but it is initially distant from the future hypothalamic region. Subsequently, the NHP expresses both LjFgf8/17 and LjBmp2/4a gene transcripts, and grows caudally to establish a de novo contact with the hypothalamic region by the mid-pharyngula stage. Later, the NHP gives rise to both the adenohypophysis and an unpaired nasal organ. Thus, the topographical relationship between the NHP and the hypothalamic region is established secondarily in the lamprey, unlike gnathostomes in which the equivalent relationship appears early in development. Comparing the developmental pattern of the amphioxus homologue of the adenohypophysis, we hypothesize that a modification of the regulation of the growth factor encoding gene lies behind the evolutionary changes recognized as heterochrony and heterotopy, which leads to the gnathostome hypophysial developmental pattern.
Animals↗
Expression of foreign genes in lamprey embryos: an approach to study evolutionary changes in gene regulation.
Evolution in development can be viewed as a sequence of changes in gene regulation. To investigate the cross-species compatibility of 5' upstream regulatory regions, we introduced exogenous gene constructs derived from a gnathostome genome into fertilized eggs of the Japanese lamprey, Lampetra japonica, a sister group of the gnathostomes. Eggs were injected with gene constructs in which a sequence encoding the green fluorescent protein (GFP) had been located downstream of either a virus promoter or 5' regulatory regions of medaka actin genes. Reporter gene expression was recorded for more than a month starting two days after injection. Although the expression patterns were highly mosaic and differed among individuals, GFP was expressed predominantly in the striated muscles of lamprey embryos when driven by the 5' upstream regions of the medaka muscle actin genes. This implies that a pan-vertebrate muscle-specific gene regulatory mechanism may have evolved before the agnathan/gnathostome divergence. This gene-transfer technique potentially facilitates the visualization of cells in various differentiating tissues throughout development. The introduction of developmental genes of the lamprey or other animals into lamprey embryos is another potentially important application, one that could provide us with information on the evolutionary changes in functions of genes or gene cascades.
Actins↗
Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution.
Genes involved in late specification of the mandibular arch, the source of the vertebrate jaw, are expressed with similar patterns in the oral regions of chick and lamprey embryos. However, morphological comparisons indicate that apparently orthologous homeobox genes were expressed in different subdivisions of the ectomesenchyme in the two species. Therefore, the homology and gene expression of the oral region are uncoupled during the transition from agnathan to gnathostome; we conclude that a heterotopic shift of tissue interaction was involved in the evolution of the jaw.
Animals↗
Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics.
Lamprey, the living jawless vertebrate, has been regarded as one of the most primitive groups of vertebrates. The evolutionary phylogenetic position of the lamprey promises to provide hints about the origin of the vertebrate genome as well as the origin of the body plan, a part of which may be written in the genome. Since the lamprey split from the gnathostome lineage early in the history of vertebrates, the shared developmental mechanisms in lampreys and gnathostomes can be regarded as possessed by the hypothetical common ancestor of these animals, whereas the gnathostome-specific developmental mechanisms that are absent from lampreys indicate that they are relatively new, added to the developmental program only after the split of gnathostomes. Thus, the sequential establishment of the gnathostome body plan is inherently related to the history of genomic duplication events. In this review, recent molecular developmental and evolutionary molecular research on the living lampreys are summarized and discussed, taking vertebrate comparative morphology and embryology into consideration.
Animals↗
Compartments in the lamprey embryonic brain as revealed by regulatory gene expression and the distribution of reticulospinal neurons.
The vertebrate neural tube consists of a series of neuromeres along its anteroposterior axis. Between amphioxus that possesses no neuromeres and gnathostomes, the lamprey occupies a critical position in the phylogeny for the origin of the segmented brain. To clarify the rhombomeric configuration of the Japanese lamprey, Lampetra japonica, we injected rhodamine- and fluorescein-labeled dextrans into the larval spinal cord, and retrogradely labeled the reticulospinal neurons. We also isolated prosomere marker genes from the embryonic cDNA library of L. japonica, and performed in situ hybridization on the embryonic brain. Of the genes examined, LjOtxA, LjPax6, LjPax2/5/8, LjDlx1/6, and LjTTF-1 were expressed in clearly demarcated polygonal domains. In the telencephalon, LjDlx1/6, LjPax6, and a putative paralogue of LjEmx were expressed in different domains; the LjEmx paralogue was expressed in the dorsal region, and LjDlx1/6 and LjPax6 in a complimentary fashion of the middle part. These expression patterns implied existence of a tripartite configuration of the lamprey telencephalon similar to that in gnathostomes. All these evidences strongly suggest that the segmental and compartmental architecture of the vertebrate brain was already established before the divergence of agnathans and gnathostomes.
Animals↗
Comprehensive survey of carapacial ridge-specific genes in turtle implies co-option of some regulatory genes in carapace evolution.
The turtle shell is an evolutionary novelty in which the developmental pattern of the ribs is radically modified. In contrast to those of other amniotes, turtle ribs grow laterally into the dorsal dermis to form a carapace. The lateral margin of carapacial primordium is called the carapacial ridge (CR), and is thought to play an essential role in carapace patterning. To reveal the developmental mechanisms underlying this structure, we systematically screened for genes expressed specifically in the CR of the Chinese soft-shelled turtle, Pelodiscus sinensis, using microbead-based differential cDNA analysis and real-time reverse transcription-polymerase chain reaction. We identified orthologs of Sp5, cellular retinoic acid-binding protein-I (CRABP-I), adenomatous polyposis coli down-regulated 1 (APCDD1), and lymphoid enhancer-binding factor-1 (LEF-1). Although these genes are conserved throughout the major vertebrate lineages, comparison of their expression patterns with those in chicken and mouse indicated that these genes have acquired de novo expression in the CR in the turtle lineage. In association with the expression of LEF-1, the nuclear localization of beta-catenin protein was detected in the CR ectoderm, suggesting that the canonical Wnt signaling triggers carapace development. These findings indicate that the acquisition of the turtle shell did not involve the creation of novel genes, but was based on the co-option of pre-existing genes.
Animals↗
Unique features of Myf-5 in turtles: nucleotide deletion, alternative splicing, and unusual expression pattern.
Turtles characteristically possess a bony shell and show an extensive reduction of the trunk muscles. To gain insight into the evolution of this animal group, we focused on the underlying mechanism of the turtle-specific developmental pattern associated with the somitic mesoderm, which differentiates into both skeleton and muscle. We isolated Myf-5, a member of the myogenic-transcription-factor-encoding gene family expressed in the myotome, from the Chinese soft-shelled turtle Pelodiscus sinensis. We detected a deletion of 12 sequential nucleotides in P. sinensis Myf-5 (PsMyf-5), which appears to be shared by the turtle group. The expression pattern of PsMyf-5 in P. sinensis embryos differed from those of its orthologs in other amniotes, especially in the hypaxial region of the flank. We also identified two isoforms of the PsMyf-5 protein, a normal form similar to those of other vertebrates, and a short form produced by a translational frameshift. The short PsMyf-5 showed weaker myogenic activity in cultured cells than that of the normal protein, although the tissue distribution of the two isoforms overlapped perfectly. We propose that the unusual features of PsMyf-5 may be related to the unique developmental patterns of this animal group, and constitute one of the molecular bases for their evolutionary origin.
Alternative Splicing↗