Abstract
The phylogenetic positions of various fishes in the Teleostei are frequently confused. One such confusion is in the phylogenetic relationships among Salmoniformes, Esociformes, Osmeriformes, Argentiniformes and Alepocephaliformes. While morphology-based phylogenetic studies suggested that all of these belong to Euteleostei, molecule-based phylogenetic analyses indicated that the former four orders belong to the Euteleostei, and the Alepocephaliformes to the Otocephala. In addition, the phylogenetic relationships among the former four orders have not been established: morphological studies have proposed various hypotheses, while molecular analyses have suggested esociforms and salmoniforms to be sister groups at the basal position in euteleosts. In this study, we examined their controversial phylogenetic positions using exon-intron structures of hatching enzyme genes. The gene structures of alepocephaliforms were characteristic to those of lower otocephalans. Those of argentiniforms and osmeriforms were the same as those of higher euteleosts, but different from those of salmoniforms and esociforms. The results suggest that alepocephaliforms are closely related to otocephalans, and salmoniforms form a sister group to esociforms in euteleosts. Therefore, changes in exon-intron structure of hatching enzyme genes correspond well with the molecular phylogenetic relationship estimated from mitochondrial DNA sequences.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Chen WJ, Mayden RL (2010) A phylogenomic perspective on the new era of ichthyology. BioScience 60:421–432
Fu C, Luo J, Wu J, LopezJ A, Zhong Y, Lei G, Chen J (2005) Phylogenetic relationships of salangid fishes (Osmeridae, Salanginae) with comments on phylogenetic placement of the salangids based on mitochondrial DNA sequences. Mol Phylogenet Evol 35:76–84
Hall BG (2005) CodonAlign. In: Phylogenetic trees made easy, 2nd edn. Sinauer Associates, Inc., Sunderland, p 7
Hiroi J, Maruyama K, Kawazu K, Kaneko T, Ohtani-Kaneko R, Yasumasu S (2004) Structure and developmental expression of hatching enzyme genes of the Japanese eel Anguilla japonica: an aspect of the evolution of fish hatching enzyme gene. Dev Gene Evol 214:176–184
Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, Iuchi I, Yamagami K (1997) Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common. Dev Growth Differ 39:191–197
Ishiguro NB, Miya M, Nishida M (2003) Basal euteleostean relationships: a mitogenomic perspective on the phylogenetic reality of the “Protacanthopterygii”. Mol Phylogenet Evol 27:476–488
Johnson GD, Patterson C (1996) Relationships of lowever euteleostean fishes. Interrelationships of Fishes pp 251–332
Kawaguchi M, Yasumasu S, Hiroi J, Naruse K, Inoue M, Iuchi I (2006) Evolution of teleostean hatching enzyme genes and their paralogous genes. Dev Gene Evol 216:769–784
Kawaguchi M, Fujita H, Yoshizaki N, Hiroi J, Okouchi H, Nagakura Y, Noda T, Watanabe S, Katayama S, Iwamuro S, Nishida M, Iuchi I, Yasumasu S (2009) Different hatching strategies in embryos of two species, pacific herring Clupea pallasii and Japanese anchovy Engraulis japonicus, that belong to the same order Clupeiformes, and their environmental adaptation. J Exp Zool B Mol Dev Evol 312:95–107
Kawaguchi M, Hiroi J, Miya M, Nishida M, Iuchi I, Yasumasu S (2010) Intron-loss evolution of hatching enzyme genes in Teleostei. BMC Evol Biol 10:260
Krauss V, Thummler C, Georgi F, Lehmann J, Stadler PF, Eisenhardt C (2008) Near intron positions are reliable phylogenetic markers: an application to holometabolous insects. Mol Biol Evol 25:821–830
Lavoué S, Miya M, Inoue JG, Saitoh K, Ishiguro NB, Nishida M (2005) Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: implications for higher-level relationships within the Otocephala. Mol Phylogenet Evol 37:165–177
Lavoué S, Miya M, Saitoh K, Ishiguro NB, Nishida M (2007) Phylogenetic relationships among anchovies, sardines, herrings and their relatives (Clupeiformes), inferred from whole mitogenome sequences. Mol Phylogenet Evol 43:1096–1105
Lavoué S, Miya M, Poulsen JY, Moller PR, Nishida M (2008) Monophyly, phylogenetic position and inter-familial relationships of the Alepocephaliformes (Teleostei) based on whole mitogenome sequences. Mol Phylogenet Evol 47:1111–1121
Li J, Xia R, McDowall RM, López JA, Lei G, Fu C (2010) Phylogenetic position of the enigmatic Lepidogalaxias salamandroides with comment on the orders of lower euteleostean fishes. Mol Phylogenet Evol 57:932–936
Lopez JA, Chen W, Orti G (2004) Esociform phylogeny. Copeia 3:449–464
Nelson JS (2006) Fishes of the world, 4th edn. Wiley, Hoboken
Poulsen JY, Moller PR, Lavoué S, Knudsen SW, Nishida M, Miya M (2009) Higher and lower-level relationships of the deep-sea fish order Alepocephaliformes (Teleostei: Otocephala) inferred from whole mitogenome sequences. Biol J Linn Soc Lond 98:923–936
Santini F, Harmon LJ, Carnevale G, Alfaro ME (2009) Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol Biol 9:194
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Tanabe AS (2007) KAKUSAN: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mol Ecol Notes 7:962–964
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Venkatesh B, Ning Y, Brenner S (1999) Late changes in spliceosomal introns define clades in vertebrate evolution. Proc Natl Acad Sci USA 96:10267–10271
Waters JM, Saruwatari T, Kobayashi T, Oohara I, McDowall RM, Wallis GP (2002) Phylogenetic placement of retropinnid fishes: data set incongruence can be reduced by using asymmetric character state transformation costs. Syst Biol 51:432–449
Williams RRG (1987) The phylogenetic relationships of the salmoniform fishes based on the suspensorium and its muscles. Ph.D. Thesis, Dept. Zool., University of Alberta, Edmonton
Yamagami K (1996) Studies on the hatching enzyme (choriolysin) and its substrate, egg envelope, constructed of the precursors (choriogenins) in Oryzias latipes: a sequel to the information in 1991/1992. Zool Sci 13:331–340
Yasumasu S, Iuchi I, Yamagami K (1988) Medaka hatching enzyme consists of two kinds of proteases which act cooperatively. Zool Sci 5:191–195
Yasumasu S, Iuchi I, Yamagami K (1989a) Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J Biochem 105:204–211
Yasumasu S, Iuchi I, Yamagami K (1989b) Isolation and some properties of low choriolytic enzyme (LCE), a component of the hatching enzyme of the teleost, Oryzias latipes. J Biochem 105:212–218
Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992) Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatching enzyme of Oryzias latipes, and concurrent expression of their mRNAs during development. Dev Biol 153:250–258
Zaragueta-Bagils R, Lavoué S, Tillier A, Bonillo C, Lecointre G (2002) Assessment of otocephalan and protacanthopterygian concepts in the light of multiple molecular phylogenies. C R Biol 325:1191–1207
Acknowledgements
We express our thanks to Christopher A. Loretz, University at Buffalo, State University of New York for reading the manuscript. We thank T. P. Satoh, National Museum of Nature and Science, and N. B. Ishiguro, Fukui University of Technology, for supplying tissue sample of S. lanceolatus and G. semifasciatus. We thank Y. Yamanoue, Atmosphere and Ocean Research Institute, for giving valuable suggestions for phylogenetic analysis. The present study was supported in part by Grant-in-Aid for JSPS Fellows to M.K, and by Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology (19207007) to M.N.
Accession numbers
The nucleotide sequence data reported in the present paper will appear in the DDBJ/EMBL/GenBank nucleotide sequence databases with accession numbers from AB549216 to AB549235.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplemental Fig. 1
A multiple alignment of amino acid sequences of hatching enzymes. Identical residues are boxed. Dashes, asterisks and “X”s represent gaps, stop codons and unidentified amino acid residues, respectively. Two active site consensus sequences of the astacin family proteases are indicated in light blue (Zn-binding site) and green (methionine turn) boxes, and conserved cysteine residues are shaded in black. Open and solid triangles indicate putative signal-sequence cleavage sites and N-termini of mature enzymes, respectively. Red lines indicate intron insertion sites, and their intron names are shown at the top of the alignment together with their intron phases in parentheses. Arrows below the sequences indicate sites for primers designed for amplification of hatching enzyme gene fragments. All the protein coding regions were determined with the following exceptions: (1) The 5′-region of GsHE gene corresponding to signal-peptide and part of pro-peptide (exons 1 and 2) could not be identified, because amino acid sequence of this region was extremely variable among fish species. (2) The C-terminal region of GsLCE, AlHE2, MaHE2, NoHE2, PaHE2 and SaHE2 could not be determined, because the last exon (9th exon) of the genes usually has a short coding sequence, i.e., it encoded only two nucleotides for stop codon or a few amino acids followed by protease domain (Kawaguchi et al. 2010). (3) The 5′-region of GsHCE1 gene and 3′-region of GsHE gene were not extended by ACP-PCR. (EPS 1.21 mb)
ESM 2
(DOC 51.0 kb)
Appendix
Appendix
Nomenclature of ayu hatching enzymes
We previously reported that two LCE genes and one HCE gene were present in ayu, judged from phylogenetic analysis using only 6 species (Kawaguchi et al. 2006). In the present study, we obtained a more reliable tree constructed from 29 species, and found that one of their genes, previously called AyLCE1, did not locate within LCE subclade (Fig. 1). Therefore, this gene was renamed AyHE, and subsequently, AyLCE2 gene reported in the previous study was renamed AyLCE gene.
Exon-intron structure of AyLCE gene
In the previous study, we have reported that AyLCE gene has an 8-exon-7-intron structure, i.e., it lost one intron corresponding to the 1st intron of the ancestral hatching enzyme gene (Kawaguchi et al. 2006). In this study, we found that one of the characteristic structures of osmeriform LCE (HnLCE and SlLCE) genes is a very small 2nd exon (Supplementary Fig. 1), whose length was 7 bp (AAAAAAG). We re-examined the structure of AyLCE gene, and found a small 2nd exon composed of only 4 bp (AAAG). We corrected the structure of AyLCE gene so that it is composed of 9 exons interrupted by 8 introns.
Rights and permissions
About this article
Cite this article
Kawaguchi, M., Lavoué, S., Hiroi, J. et al. Remarkable consistency of exon-intron structure of hatching enzyme genes and molecular phylogenetic relationships of teleostean fishes. Environ Biol Fish 94, 567–576 (2012). https://doi.org/10.1007/s10641-011-9920-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-011-9920-1