MBE Advance Access published online on August 29, 2003
Molecular Biology and Evolution, doi:10.1093/molbev/msg227
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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1 Montreal Neurological Institute and Department of Biology, McGill University, 3801 University St, Montreal, Quebec, Canada H3A 2B4
* To whom correspondence should be addressed. E-mail: ken.hastings{at}mcgill.ca.
Ascidians are protochordates related to vertebrate ancestors. The ascidian larval tail, with its notochord, dorsal nerve cord, and flanking rows of sarcomeric muscle cells, exhibits the basic chordate body plan. Molecular characterization of ascidian larval tail muscle may provide insight into molecular aspects of vertebrate skeletal muscle evolution. We report studies of the Ci-TnI gene of the ascidian Ciona intestinalis, which encodes the muscle contractile regulatory protein troponin I (TnI). Previous studies of a distantly-related ascidian, Halocynthia roretzi, showed that different TnI genes were expressed in larval and adult muscles, the larval TnI isoforms having an unusual C-terminal truncation not seen in any vertebrate TnI. Here we show that, in contrast with Halocynthia, Ciona does not have a specialized larval TnI; the same TnI gene that is expressed in the heart and body-wall muscle of the sessile adult is also expressed in embryonic/larval tail muscle cells. Moreover the TnI isoform produced in embryonic/larval muscle is identical to that produced in adult body-wall muscle, i.e. a 182 residue protein with the characteristic chain length and overall structure of vertebrate skeletal muscle TnI isoforms. Phylogenetic analyses indicate that the unique features of Halocynthia larval TnI likely represent derived features, and hence that the vertebrate-skeletal-muscle-like TnI of Ciona is a closer reflection of the ancestral ascidian larval TnI. Our results indicate that characteristics of vertebrate skeletal muscle TnI emerged early in the evolution of chordate locomotory muscle, before the ascidian/vertebrate divergence. These features could be related to a basal chordate locomotory innovation, e.g. swimming by oscillation of an internal notochord skeleton, or they may be of even greater antiquity within the deuterostomes. Key Words:
contractile regulatory mechanism, muscle, chordate evolution, Ciona intestinalis, gene family evolution
© 2003 Society for Molecular Biology and Evolution
Original Articles
Ascidian Larva Reveals Ancient Origin of Vertebrate-Skeletal-Muscle Troponin I Characteristics in Chordate Locomotory Muscle
2 Biology Department, Rhode Island College, Providence, RI, USA 02908
3 Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan
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