Summary
The ascidians Styela plicata, S. clava, and Mogula citrina are urochordates. The larvae of urochordates are considered to morphologically resemble the ancestral vertebrate. We asked whether larval and adult ascidian muscle actin sequences are nonmusclelike as in lower invertebrates, musclelike as in vertebrates, or possess characteristics of both. Nonmuscle and muscle actin cDNA clones from S. plicata were sequenced. Based on 27 diagnostic amino acids, which distinguish vertebrate muscle actin from other actins, we found that the deduced protein sequences of ascidian muscle actins exhibit similarities to both invertebrate and vertebrate muscle actins. A comparison to muscle actins from different vertebrate and invertebrate phylogenetic groups suggested that the urochordate muscle actins represent a transition from a nonmusclelike sequence to a vertebrate musclelike sequence. The ascidian adult muscle actin is more similar to skeletal actin and the larval muscle actin is more similar to cardiac actin, which indicates that the divergence of the skeletal and cardiac isoforms occurred before the emergence of urochordates. The muscle actin gene may be a powerful probe for investigating the chordate lineage.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alonso S (1987) Coexpression and evolution of the two sarcomeric actin genes in vertebrates. Biochimie 69:1119–1125
Baines W, Ponte P, Blau H, Kedes L (1984) Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol Cell Biol 4:1449–1461
Beach RL, Jeffery WR (1992) Multiple genes encoding the same α-muscle isoform are expressed during ascidian development. Dev Biol 151:55–66
Bergsma DJ, Chang KS, Schwartz RJ (1985) Novel chicken actin gene: third cytoplasmic isoform. Mol Cell Biol 5:1151–1162
Berrill NJ (1951) The origin of vertebrates. Clarendon Press, Oxford
Bone Q (1981) The neotenic origin of chordates. Atti Conv Lincei 49:465–486
Cavey MJ (1983) Ultrastructure and differentiation of ascidian muscle. Cell Tissue Res 230:77–94
Collins JH, Elzinga M (1975) The primary structure of actin from rabbit skeletal muscle. J Biol Chem 250:5915–5920
Cooper AD, Crain Jr WR (1982) Complete nucleotide sequence of a sea urchin actin gene. Nucleic Acids Res 10:4081–4092
Cox KH, Angerer LM, Lee JJ, Davidson EH, Angerer RC (1986) Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis. J Mol Biol 188:159–172
Crain Jr WR, Boshar MF, Cooper AD, Durica DS, Nagy A, Steffen D (1987) The sequence of a sea urchin muscle actin gene suggests a gene conversion with a cytoskeletal actin gene. J Mol Evol 25:37–45
Cross GS, Wilson C, Erba HP, Woodland HR (1988) Cytoskeletal actin gene families of Xenopus borealis and Xenopus laevis. J Mol Evol 27:17–28
Crowther RJ, Whittaker JR (1983) Developmental autonomy of muscle fine structure in muscle lineage cells of ascidian embryos. Dev Biol 96:1–10
Davidson EH (1986) Gene activity in early development, 3rd ed. Academic Press, Orlando, FL
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the vax. Nucleic Acids Res 12:387–395
Dibb NJ, Newman AJ (1989) Evidence that introns arose at proto-splice sites. EMBO J 8:2015–2021
Durica DS, Garza D, Restrepo MA, Hryniewicz MM (1988) DNA sequence analysis and structural relationships among the cytoskeletal actin genes of the sea urchin Strongylocentrotus purpuratus. J Mol Evol 28:72–86
Fisher DA, Bode HR (1989) Nucleotide sequence of an actin-encoding gene from Hydra attenuata: structural characteristics and evolutionary implications. Gene 84:55–64
Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N (1983) Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 33:115–123
Garstang W (1928) The morphology of the tunicata and its bearing on the phylogeny of the chordata. Quart J Microsc Sci 72:51–187
Gunning P, Ponte P, Blau H, Kedes L (1983) α-Skeletal and α-cardiac actin genes are coexpressed in adult human skeletal muscle and heart. Mol Cell Biol 3:1985–1995
Hayward LJ, Schwartz RJ (1986) Sequential expression of chicken actin genes during myogenesis. J Cell Biol 102:1485–1493
Maniatis T, Fritsch EF, Sambrook (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NY
Mayer Y, Czosnek H, Zeelon PE, Yaffe D, Nudel U (1984) Expression of the genes coding for the skeletal muscle and cardiac actins in the heart. Nucleic Acids Res 12:1087–1100
Mohun TJ, Garrett N, Stutz F, Spohr G (1988) A third striated muscle actin gene is expressed during early development in the amphibian Xenopus laevis. J Mol Biol 202:67–76
Mounier N, Gouy M, Mouchiroud D, Prudhomme JC (1992) Insect muscle actins differ distinctly from invertebrate and vertebrate cytoplasmic actins. J Mol Evol 34:406–415
Paterson BM, Eldridge JD (1984)α-cardiac actin is the major sarcomeric isoform expressed in embryonic avian skeletal muscle. Science 224:1436–1438
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Press, Cold Spring Harbor, NY
Sanchez F, Tobin SL, Rdest U, Zulauf E, McCarthy BJ (1983) Two Drosophila actin genes in detail: gene structure, protein structure and transcription during development. J Mol Biol 163:533–551
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Sassoon DA, Garner I, Buckingham M (1988) Transcripts of α-cardiac and α-skeletal actins are early markers for myogenesis in the mouse embryo. Development 104:155–164
Shott RJ, Lee JJ, Britten RJ, Davidson EH (1984) Differential expression of the actin gene family of Strongylocentrolus purpuratus. Dev Biol 101:295–306
Stutz F, Spohr G (1986) Isolation and characterization of sarcomeric actin genes expressed in Xenopus laevis embryos. J Mol Biol 187:349–361
Swofford DL (1991) PAUP: Phylogenetic analysis using parsimony, version 3.0r, Computer program distributed by the Illinois Natural History Survey, Champaign, IL
Tomlinson CR, Beach RL, Jeffery WR (1987a) Differential expression of a muscle actin gene in muscle cell lineages of ascidian embryos. Development 101:751–765
Tomlinson CR, Bates WR, Jeffery WR (1987b) Development of a muscle actin specified by maternal and zygotic mRNA ascidian embryos. Dev Biol 123:470–482
Vandekerckhove J, Weber K (1978) Mammalian cytoplasmic actins are the products of at least two genes and differ in primary structure in at least 25 identified positions from skeletal muscle actins. Proc Natl Acad Sci USA 75:1106–1110
Vandekerckhove J, Weber K (1979) The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle, and rabbit slow skeletal muscle. Differentiation 14:123–133
Vandekerckhove J, Weber K (1984) Chordate muscle actins differ distinctly from invertebrate muscle actins. J Mol Biol 179: 391–413
Vandekerckhove J, Franke WW, Weber K (1981) Diversity of expression of non-muscle actin in amphibia. J Mol Biol 152: 413–426
Vandekerckhove J, Bugaisky G, Buckingham M (1986) Simultaneous expression of skeletal muscle and heart actin proteins in various striated muscle tissues and cells. J Biol Chem 261: 1838–1843
Author information
Authors and Affiliations
Additional information
Offprint requests to: C.R. Tomlinson
Rights and permissions
About this article
Cite this article
Kovilur, S., Jacobson, J.W., Beach, R.L. et al. Evolution of the chordate muscle actin gene. J Mol Evol 36, 361–368 (1993). https://doi.org/10.1007/BF00182183
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00182183