A genomewide survey of developmentally relevant genes in Ciona intestinalis

Abstract

Ascidians are simple chordates that are related to, and may resemble, vertebrate ancestors. Comparison of ascidian and vertebrate genomes is expected to provide insight into the molecular genetic basis of chordate/vertebrate evolution. We annotated muscle structural (contractile protein) genes in the completely determined genome sequence of the ascidian Ciona intestinalis, and examined gene expression patterns through extensive EST analysis. Ascidian muscle protein isoform families are generally of similar, or lesser, complexity in comparison with the corresponding vertebrate isoform families, and are based on gene duplication histories and alternative splicing mechanisms that are largely or entirely distinct from those responsible for generating the vertebrate isoforms. Although each of the three ascidian muscle types - larval tail muscle, adult body-wall muscle and heart - expresses a distinct profile of contractile protein isoforms, none of these isoforms are strictly orthologous to the smooth-muscle-specific, fast or slow skeletal muscle-specific, or heart-specific isoforms of vertebrates. Many isoform families showed larval-versus-adult differential expression and in several cases numerous very similar genes were expressed specifically in larval muscle. This may reflect different functional requirements of the locomotor larval muscle as opposed to the non-locomotor muscles of the sessile adult, and/or the biosynthetic demands of extremely rapid larval development.

Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: evidence for a unified theory of animal muscle development

“…Although orthologs of several vertebrate muscletype-specific structural protein isoforms can be traced to ascidians, there is remarkably little conservation in expression patterns relative to muscle type (Meedel and Hastings 1993). For example, structural protein isoforms indicative of vertebrate cardiac muscle are present in ascidian bodywall muscle and vice versa (Chiba et al 2003), even though the ascidian heart is dependent on factors related to Nkx2.5 and HAND (Davidson and Levine 2003;Satou et al 2004). Coupled with our results, a model emerges in which a single ancestral contractile cell was dependent on a transcriptional hierarchy comprised of factors we now associate with several different muscle types.…”

Lamprey contractile protein genes mark different populations of skeletal muscles during development

“…1). At amino acid position 17, LjMA2 possessed a Cys residue that is common in mammalian smooth muscle-and non-muscle actins, rather than a Val shared by the striated muscle actins of vertebrates (Vandekerckhove and Weber,'79), ascidians (Kusakabe, '97;Chiba et al, 2003), appendicularia (Nishino et al, 2000), and amphioxus (Kusakabe et al, '97a;Suzuki and Satoh, 2000). The Val at position 17 may have existed in the ancestral protein of chordate striated muscle actins, and been substituted by a Cys residue independently in the lamprey striated actin lineage.…”

“…Results from the phylogenetic analysis of the MyHCs provide new insights into protochordate MyHC evolution. Ascidian C. intestinalis genome contains six MyHC genes, among which Ci-MHC5 is expressed in the segmented tail muscles (Chiba et al, 2003). This gene represents an isoform most closely related to vertebrate striated muscle MyHCs (Fig.…”

“…One reason for this might lie in the fact that genes encoding relatively similar proteins are expressed differently in various types of muscles. Recent reports of genome-wide surveys of ascidian Ciona intestinalis muscle structural protein genes revealed that this animal contains 14 actin genes, consisting of six muscle-type and eight non-muscle-type genes, but no smooth muscle-type actin gene (Chiba et al, 2003). Another ascidian species Halocynthia roretzi has tandemly linked muscle actin genes whose tail muscle-specific expression patterns resemble each other (Kusakabe,'97;Kusakabe et al,'95).…”

Noncoding regulatory sequences of Ciona exhibit strong correspondence between evolutionary constraint and functional importance

“…TnI was chosen because a full-length cDNA and detailed annotation of the genomic locus have been reported previously (Maclean et al 1997;Chiba et al 2003;Cleto et al 2003), and because its strong expression in tadpole muscle permits semiquantitative analysis of variants from wild type.…”