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<p>The emergence of connectin, also called titin, a muscular spring and the largest protein in living organisms, is critical in metazoan evolution as it enables striated muscle-based locomotion. However, its evolutionary history remains unclear. Here, we investigated the evolutionary process using genomic analysis and deduced the ancestor of connectin. The region between the <i>HOX</i> and <i>WNT</i> clusters in the human genome, where the connectin gene (<i>CON</i> (<i>TTN</i>)) is located, was quadrupled by two rounds of whole-genome duplication (WGD) in the ancestor of jawed vertebrates. However, connectin ohnologs were deleted before the advent of jawed vertebrates, resulting in a single connectin gene. Additionally, one of the connectin ohnologs created by the third round of teleost WGD disappeared, while the other was duplicated on the same chromosome. We also discovered that the connectin and connectin family genes consistently underwent local duplication on the same chromosome, though the underlying mechanism remains unknown. Using synteny analysis, we identified <i>KALRN</i> and its ohnolog <i>TRIO</i> as putative ancestral paralogs of the connectin gene. <i>TRIO/KALRN</i> has a connected structure of <i>SESTD1</i>-<i>CCDC141</i>-<i>CON</i> (<i>TTN</i>), and its synteny is conserved in the <i>Drosophila</i> genome. Furthermore, we confirmed that this connected structure, termed ‘connectitin,’ (connected-connectin/titin) is conserved in cnidarians and placozoans. Molecular phylogenetic analysis revealed that it diverged from <i>TRIO/KALRN</i> prior to the emergence of these animals, suggesting that metazoan muscle may have a single origin. These findings enhance our understanding of the evolutionary processes of striated muscles in the animal kingdom.</p>

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The Ancestor and Evolution of the Giant Muscle Protein Connectin/Titin

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年4月27日

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  • Akira Hanashima,
  • Yuu Usui,
  • Ken Hashimoto,
  • Satoshi Mohri

摘要

The emergence of connectin, also called titin, a muscular spring and the largest protein in living organisms, is critical in metazoan evolution as it enables striated muscle-based locomotion. However, its evolutionary history remains unclear. Here, we investigated the evolutionary process using genomic analysis and deduced the ancestor of connectin. The region between the HOX and WNT clusters in the human genome, where the connectin gene (CON (TTN)) is located, was quadrupled by two rounds of whole-genome duplication (WGD) in the ancestor of jawed vertebrates. However, connectin ohnologs were deleted before the advent of jawed vertebrates, resulting in a single connectin gene. Additionally, one of the connectin ohnologs created by the third round of teleost WGD disappeared, while the other was duplicated on the same chromosome. We also discovered that the connectin and connectin family genes consistently underwent local duplication on the same chromosome, though the underlying mechanism remains unknown. Using synteny analysis, we identified KALRN and its ohnolog TRIO as putative ancestral paralogs of the connectin gene. TRIO/KALRN has a connected structure of SESTD1-CCDC141-CON (TTN), and its synteny is conserved in the Drosophila genome. Furthermore, we confirmed that this connected structure, termed ‘connectitin,’ (connected-connectin/titin) is conserved in cnidarians and placozoans. Molecular phylogenetic analysis revealed that it diverged from TRIO/KALRN prior to the emergence of these animals, suggesting that metazoan muscle may have a single origin. These findings enhance our understanding of the evolutionary processes of striated muscles in the animal kingdom.