Molecular evolution of troponin I and a role of its N‐terminal extension in nematode locomotion

Abstract

Summary The troponin complex, composed of troponin T (TnT), troponin I (TnI), and troponin C (TnC), is the major calcium-dependent regulator of muscle contraction, which is present widely in both vertebrates and invertebrates. Little is known about evolutionary aspects of troponin in the animal kingdom. Using a combination of data mining and functional analysis of TnI, we report evidence that an N-terminal extension of TnI is present in most of bilaterian animals as a functionally important domain. Troponin components have been reported in species in most of representative bilaterian phyla. Comparison of TnI sequences shows that the core domains are conserved in all examined TnIs, and that N- and C-terminal extensions are variable among isoforms and species. In particular, N-terminal extensions are present in all protostome TnIs and chordate cardiac TnIs but lost in a subset of chordate TnIs including vertebrate skeletal-muscle isoforms. Transgenic rescue experiments in C. elegans striated muscle show that the N-terminal extension of TnI (UNC-27) is required for coordinated worm locomotion but not in sarcomere assembly and single muscle-contractility kinetics. These results suggest that N-terminal extensions of TnIs are retained from a TnI ancestor as a functional domain.

Deuterostome Genomics: Lineage-Specific Protein Expansions That Enabled Chordate Muscle Evolution

“…Considering the presence of the troponin C gene in almost all reported bilaterians, the estimated gene tree of troponin C ( fig. 2 B 6) suggests that troponin C was present in the bilaterian ancestor and has been lost in the ambulacrarian ancestor, as suggested previously ( Barnes et al. 2016 ; Yaguchi et al.…”

“…Although the expression and function of troponin I are confirmed in sea urchin larval muscle ( Yaguchi et al. 2017 ), troponin I and other components of the troponin complex have not been found in other ambulacrarians ( Barnes et al. 2016 ).…”

Tropomyosin isoforms differentially affect muscle contractility in the head and body regions of the nematodeCaenorhabditis elegans

“…The troponin complex, consisting of troponin T, troponin I, and troponin C, is a calcium-dependent regulator for muscle contraction ( Ebashi, 1984 ). C. elegans has four genes encoding troponin I, a troponin component that cooperates with tropomyosin to inhibit actomyosin interaction ( Burkeen et al , 2004 ; Ruksana et al , 2005 ; Obinata et al , 2010 ; Barnes et al , 2016 ). Among them, tni-3 is preferentially expressed in the head region, whereas unc-27 (also known as tni-2 ) is expressed as a major isoform in most of body wall muscle cells ( Burkeen et al , 2004 ; Ruksana et al , 2005 ).…”

Invertebrate troponin: Insights into the evolution and regulation of striated muscle contraction

“…1). This timeline corresponds to the emergence of bilaterians in animals (the phyla of Platyhelminthes and Nematoda), concurrent with the emergence of central nervous system (13,14). This notion suggests a critical role of the troponin regulation of muscle contraction and relaxation in coordinated movement of animals.…”