Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis

Abstract

Myosin heavy chain genes ( MYHs) are the most important functional domains of myosins, which are highly conserved throughout evolution. The human genome contains 15 MYHs, whereas the corresponding number in teleost appears to be much higher. Although teleosts comprise more than one-half of all vertebrate species, our knowledge of MYHs in teleosts is rather limited. A comprehensive analysis of the torafugu ( Takifugu rubripes) genome database enabled us to detect at least 28 MYHs, almost twice as many as in humans. RT-PCR revealed that at least 16 torafugu MYH representatives (5 fast skeletal, 3 cardiac, 2 slow skeletal, 1 superfast, 2 smooth, and 3 nonmuscle types) are actually transcribed. Among these, MYH M743-2 and MYH M5 of fast and slow skeletal types, respectively, are expressed during development of torafugu embryos. Syntenic analysis reveals that torafugu fast skeletal MYHs are distributed across five genomic regions, three of which form clusters. Interestingly, while human fast skeletal MYHs form one cluster, its syntenic region in torafugu is duplicated, although each locus contains just a single MYH in torafugu. The results of the syntenic analysis were further confirmed by corresponding analysis of MYHs based on databases from Tetraodon, zebrafish, and medaka genomes. Phylogenetic analysis suggests that fast skeletal MYHs evolved independently in teleosts and tetrapods after fast skeletal MYHs had diverged from four ancestral MYHs.

Fibre type-specific expression patterns of myosin heavy chain genes in adult torafugu Takifugu rubripes muscles

“…MYH M5 was a unique MYH as its phylogenetic position was independent of any other MYH genes, whereas MYH M880 was monophyletic with zebrafish atrial MYH (Fig.2). This phylogenetic relationship of torafugu MYH genes was in close agreement with that described by Ikeda and colleagues (Ikeda et al, 2007). MYH M5 and MYH M880 were found to have appeared in an early evolution of MYHs as far as the present phylogenetic tree was concerned, and these genes were regarded to belong to an ancestral slow/cardiac type (see Table1).…”

“…Three MYH genes, MYH M86-1 , MYH M8248 and MYH M880 , were cloned exclusively from fast, slow and cardiac muscles dissected from a single laboratoryreared adult specimen, respectively, whereas two MYH genes, MYH M2528-1 and MYH M1034 , were cloned from both fast and slow muscles and another two MYH genes, MYH M2126-2 and MYH M5 , were cloned from both slow and cardiac muscles. The nomenclature of torafugu MYH genes found in the present study follows Ikeda and colleagues (Ikeda et al, 2007).…”

“…MYH M86-1 , MYH M2528-1 and MYH M1034 belong to fast type as they were placed in the clade representing fast MYH genes (Nihei et al, 2006;Ikeda et al, 2007), whereas MYH M8248 belongs to slow type and MYH M2126-2 to cardiac type as they were monophyletic with slow-and cardiac-type MYH genes from other fish species, respectively (Fig.2). The phylogenetic tree shows that fast-type MYH genes, MYH M2528-1 and MYH M1034 , were placed in the same clade as fast-type MYHemb1 which is expressed in medaka from embryonic to adult stages , whereas MYH M86-1 was placed in the same clade as fast-type mMYH-11 which is expressed in adult medaka acclimated to 30°C (Liang et al, 2007).…”

“…Recently, we have investigated the genomic organization of sarcomeric and nonsarcomeric MYH genes of torafugu by in silico analysis of the total genome database, revealing that it contains 20 sarcomeric MYH genes which are organized in different clusters Ikeda et al, 2007). Common carp Cyprinus carpio is also known to possess a highly conserved MYH multigene family, although MYH gene types are much more numerous than their higher (Gerlach et al, 1990;Kikuchi et al, 1999;Ikeda et al, 2007), probably because teleosts have undergone an additional round of genome duplication. The question, then, is why so many genes are contained in fish, even in torafugu with its small sized genome.…”

Validation of Endogenous Reference Genes for qPCR Quantification of Muscle Transcripts in Atlantic Cod Subjected to Different Photoperiod Regimes

“…Another molecule of significant importance in muscle development is myosin heavy chain (myhc), which serves as marker of muscle development in several studies (Johnston, 1999). Myhc genes code for a family of ATP-dependent motor proteins that are involved in muscle contraction (Ikeda et al, 2007). Myhc activity can be used to monitor fish growth, since most fish have a continuous hyperplasic growth throughout their lifespan and myhc is actively involved in muscle protein synthesis (Dhillon et al, 2009).…”