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The long protostomic-type cytoplasmic intermediate filament (cIF) protein in Branchiostoma supports the phylogenetic transition between the protostomic- and the chordate-type cIFs

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Abstract

We identified 23 and 20 cytoplasmic IF (cIF) genes in the two Branchiostoma belcheri and Branchiostoma lanceolatum cephalochordates, respectively. Combining these results with earlier data on the related Branchiostoma floridae, the following conclusions can be drawn. First, the Branchiostoma N4 protein with a long lamin-like coil 1B segment is the only protostomic-type cIF found so far in any analysed chordate or vertebrate organism. Second, Branchiostoma is the only organism known so far containing both the long protostomic- and the short chordate-prototypes of cIFs. This finding provides so far missing molecular evidence for the phylogenetic transition between the protostomic- and the chordate-type IF sequences at the base of the cephalochordates and vertebrates. Third, this finding also brings some support for another hypothesis, that the long protostomic-type cIF is subjected to evolutionary constraints in order to preclude inappropriate interactions with lamin and that the latter complexes might be prevented by a several heptad-long rod deletion, which released the selective constraints on it and promoted, at least in part, its expansion in nematodes, cephalochordates, and in vertebrates. Finally, here-presented data confirmed our previous results that cephalochordates do not have any vertebrate type III or type IV IF homolog.

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Acknowledgements

We would like to thank the team from Medirex, a.s. for support.

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  1. Medirex, a.s., Kosice, Magnezitarska 2/C, 04013, Kosice, Slovakia

    Anton Karabinos

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  1. Anton Karabinos
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ESM 1

Fig. S. Alignment of the protein sequences of the B. floridae (Bf), B. belcheri (Bb) and B. lanceolatum (Bl) IF proteins (panel a) D1, C1, C2 and N2, (panel b) E2 and E3, (panel c) E1 and Y1, (panel d) X1, (panel e) D1 and XP_019633116.1-krt-81, (panel f) N1, (panel g) N2, (panel h) N3 and (panel i) B1 and AѰ. Moreover, panels j a k present the phylogenetic tree generated by the maximum-likelihood and neighbour-joining analysis, respectively. Identical amino acids between the compared Branchiostoma proteins, are marked in bold, while dashes are used to optimize the sequence alignment. The arrowhead pointing down indicates the start and the end position of the corresponding IF rod coil 1A, 1B, col 2A and 2B segments, which are connected by linkers L1, L12 and L2. Asterisks below the rod segments mark the a and d positions of the heptad repeat pattern (panels a-i), while asterisks above the two C tail-sequences mark their two degenerate repeats, exhibiting a heptad repeat pattern participating in the formation of a double-stranded coiled coil dimer (panel a; for details see Karabinos 2013; Karabinos and Schünemann 2014). The “QxW” motifs of the ricin-type carbohydrate-binding domain of the C, D1 and N2 IF tail-sequences are boxed (panel a; for details see Fig. 1). A manual comparison of the BfD1 IF protein and the uncharacterized 1318-residue-long B. belcheri XP_019633116.1 sequence, which corresponds to the recently reported krt-81 gene (panel e), revealed the poorly conserved helix initiation motif in the proposed coil 1A segment and a pure sequence similarity of this sequence (revealing very poor heptads with many polar residues at the heptad positions a and d, 5 prolines and no conserved helix termination motif in the proposed coil 2 segment) to the rest of the compared prototypic Branchiostoma BfD1 cIF protein. Moreover, a unique long tail-like domain terminating with the nuclear envelope localisation domain KASH (Razafsky and Hodzic 2009), shared with the B. floridae (XP_035657632) and B. lanceolatum (CAH1252602.1) orthologs (data not shown), collectively indicate that this uncharacterized XP_019633116.1/krt-81 protein is not an IF. In panel h, both the BfN3 and BbN3 sequences have unusually long tail domains, so we think that identification of final amino acid sequences of these terminal sequences might await cloning of the corresponding full-length cDNAs. In panel i, positions of the BfB1 rod gene introns are marked by arrows pointing down, while positions of the four conserved rod BfAѰ-new introns, as well as the two novel rod BfAѰ-new introns, positioned to the divergent C-terminal part of this protein, are marked by arrows pointing up. The BfAѰ-new gene represents a revised version of the previously reported B. floridae sequence 81362-AѰ (named here as BfAѰ-old). As documented here, all four Branchiostoma sequences still retained a divergent C-terminus in which the last 13 residues VNLQINQHTNRGW of the original BfAѰ-old sequence have been replaced by 22 new residues, marked in the BfAѰ-new sequence (panel i; see text for details). In panel j is the phylogenetic tree generated by the maximum-likelihood analysis of the conserved rod domains of the IF proteins, derived from the B. floridae (Bf), B. belcheri (Bb) and B. lanceolatum (Bl) species (listed in Table 1) as well as the three protostomic sequences used as an outgroup. The bootstrap values (100 replications) are indicated above or below the internal nodes. The position of the Branchiostoma N4/N2, X1/N1, type I keratin, C1/C2, A/B, N3, type II keratin and the protostomic IF sequence groups are indicated. The arrows mark the monophyletic IF subgroups of the individual Branchiostoma species (see text for details). Note some phylogenetic evidence for a closer evolutionary relationship between the long protostomic-type N4 protein (marked by a double arrow) and the short chordate-type protein N2. Notably, this evolutionary N4/N2 relationship on the one hand, and the known ricin-type domain similarities of the N2, D1 and C IF tail sequences on the other hand, might potentially support an origin of all these five N4, N2, C1, C2 and D1 IF sequences from a common ancestor (see also Fig. 1, panel a above and the text for details). Note also a sister group relationship of the X1 and N1 with the type I keratins and the two keratin-like C IFs, in line with their keratin-like sequence features of the terminal domains (i.e. several glycine loops flanked by hydrophobic residues in panel d, g; for more details see Karabinos 2013). Finally, note that the phylogenetic attachment of the N3 sequences to the monophyletic A/B branch is also seen in the parallel neighbour-joining distance analysis (panel k below). However, none of the N1 to N4 positions had a bootstrap support, which indicates that any sister group relationship (e.g. N4/N2, N1/type I keratins, N3/A/B) drawn from this phylogeny, is interpreted as a provisional result. Finally, panel k presents the phylogenetic tree generated by the neighbour-joining analysis (for details, see panel j above and the text).

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Karabinos, A. The long protostomic-type cytoplasmic intermediate filament (cIF) protein in Branchiostoma supports the phylogenetic transition between the protostomic- and the chordate-type cIFs. Protoplasma 260, 1493–1500 (2023). https://doi.org/10.1007/s00709-023-01865-3

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