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MBE Advance Access published online on July 27, 2005

Molecular Biology and Evolution, doi:10.1093/molbev/msi223
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Accepted July 7, 2005

Research Article

The Co-evolution of Insect Muscle TpnT and TpnI Gene Isoforms

Raúl Herranz 1, Jesús Mateos 1, José A. Mas 1, Elena García-Zaragoza 1, Margarita Cervera 1*, and Roberto Marco 1

1 Departamento de Bioquímica e Instituto de Investigaciones Biomédicas "Alberto Sols" UAM-CSIC, Facultad de Medicina de la Universidad Autónoma de Madrid C/ Arzobispo Morcillo 4, 28029 Madrid. Spain

* To whom correspondence should be addressed.
Margarita Cervera, E-mail: margarita.cervera{at}uam.es


   Abstract

In bilaterians, the main regulator of muscle contraction is the troponin (Tpn) complex, comprising three closely-interacting subunits (C, T and I). To understand how evolutionary forces drive molecular change in protein complexes we have compared the gene structures and expression patterns of Tpn genes in insects. In this class, while TpnC is encoded by multiple genes, TpnT and TpnI are encoded by single genes. Their isoform expression pattern is highly conserved within the drosophilidae, and single orthologous genes were identified in the sequenced genomes of D. pseudoobscura, Anopheles gambiae and Apis mellifera. Apis expression patterns also support the equivalence of their exon organization throughout holometabolous insects. All TpnT genes include a previously unidentified indirect flight muscle (IFM) specific exon (10A) that has evolved an expression pattern similar to that of exon 9 in TpnI. Thus, expression patterns, sequence evolution trends and structural data indicate that Tpn genes and their isoforms have coevolved, building species and muscle specific troponin complexes. Furthermore, a clear case can be made for independent evolution of the IFM-specific isoforms containing alanine/proline-rich sequences. Dipteran genomes contain one tropomyosin gene that encodes one or two high molecular weight isoforms (TmH) incorporating APPAEGA rich sequences, specifically expressed in IFM. Corresponding exons do not exist in the Apis tropomyosin gene but equivalent sequences occur in a high molecular weight Apis IFM specific TpnI isoform (TpnH). Overall our approach to comparatively analyze supramolecular complexes reveals co-evolutionary trends not only in gene families but in isoforms generated by alternative splicing.

Keywords: Troponin; Tropomyosin; Co-evolution; Insecta; Drosophila; Anopheles; Apis; Phylogenetics.
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