Summary
A cloned chicken δ-crystallin cDNA was used to identify two putative δ-crystallin genes in the duck by Southern blot hybridization. A DNA fragment containing most of one of these genes was isolated from a library made in bacteriophage λ Charon 28A containing genomic DNA from 14-day-old embryonic ducks. Electron microscopy, partial gene sequencing, primer extension analysis using duck mRNA, and comparison with the well-characterized chicken δ-crystallin genes suggest that our cloned duck δ-crystallin gene, like the chicken δ-crystallin genes, is 8–10 kb long and contains 17 exons. Hybridization and sequencing data show great similarity between the homologous 5′ untraslated and coding exons of the duck and chicken δ-crystallin genes. Overall, the homologous introns also appear to have approximately 30% sequence similarity, and have been subject to deletion/insertion events. Our partial characterization of duck δ-crystallin gene sequences suggests that this avian and reptilian crystallin family has been conserved during evolution, as have the other crystallin gene families that are expressed in the eye lens.
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References
Bhat SP, Piatigorsky J (1979) Molecular cloning and partial characterization of δ-crystallin cDNA sequences in a bacterial plasmid. Proc Natl Acad Sci USA 76:3299–3303
Bhat SP, Jones RE, Sullivan MA, Piatigorsky J (1980) Chicken lens crystallin DNA sequences show at least two δ-crystallin genes. Nature 284:234–238
Biggin MD, Gibson TJ, Hong GFP (1983) Buffer gradient gels and35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965
Bloemendal H (1977) The vertebrate eye lens. A useful system for the study of fundamental biological processes on a molecular level. Science 197:127–138
Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow G (1981) The molecular structure and stability of the eye lens: X-ray analysis of γ-crystallin II. Nature 289:771–777
Borras T, Nickerson JM, Chepelinsky AB, Piatigorsky J (1985) Structural and functional evidence for differential promoter activity of the two linked δ-crystallin genes in the chicken. EMBO J 4:445–452
Clayton RM (1974) Comparative aspects of lens proteins. In: Davson H, Graham LT (eds) The eye. Academic Press, New York, pp 399–494
de Jong WW, Hendriks W (1986) The eye lens crystallins: ambiguity as evolutionary strategy. J Mol Evol 24:121–129
de Jong WW, Stapel SO, Zweers A (1981) A comparison of avian and reptilian δ-crystallin. Comp Biochem Physiol 69B: 593–598
den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986a) Intron insertions and deletions in the β/γ-crystallin gene family: the rat βB1 gene. Proc Natl Acad Sci USA 83:2855–2859
den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986b) Concerted and divergent evolution within the rat γ-crystallin gene family. J Mol Biol 189:37–46
Denhardt DT (1966) A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23:641–646
Dodgson JB, Engel JD (1983) The nucleotide sequence of the adult chicken α-globin genes. J Biol Chem 258:4623–4629
Driessen HPC, Herbrink P, Bloemendal H, de Jong WW (1980) The β-crystallin Bp chain is internally duplicated and homologous with γ-crystallin. Exp Eye Res 31:243–246
Driessen HPC, Herbrink P, Bloemendal H, de Jong WW (1981) Primary structure of the bovine β-crystallin Bp chain. Internal duplication and homology with γ-crystallin. Eur J Biochem 121:83–91
Eden FC, Hendrick JP, Gottlieb SS (1978) Homology of single copy of repeated sequences in chicken, duck Japanese quail, and ostrich DNA. Biochemistry 17:5113–5121
Engel JD, Rusling DJ, McCune KC, Dodgson JB (1983) Unusual structure of the chicken embryonic α-globin gene, π. Proc Natl Acad Sci USA 80:1392–1396
Erbil C, Niessing J (1982) The complete nucleotide sequence of the duck αA-globin gene. Gene 20:211–217
Erbil C, Niessing J (1984) Chromosomal arrangement of the duck α-globin genes and primary structure of the embryonic α-globin gene π′. Gene 32:161–170
Harding JJ, Dilley KJ (1976) Structural proteins of the mammalian lens: a review with emphasis on changes in development, aging and cataract. Exp Eye Res 22:1–73
Hawkins JW, Nickerson JM, Sullivan MA, Piatigorsky J (1984) The chicken δ-crystallin gene family. Two genes of similar structure in close chromosomal approximation. J Biol Chem 259:9821–9825
Hogg D, Tsui L-C, Gorin M, Breitman ML (1986) Characterization of the human β-crystallin gene Hu\A3/A1 reveals ancestral relationships among the βγ-crystallin superfamily. J Biol Chem 261:12420–12427
Horwitz J, Piatigorsky J (1980) Evolutionary and development differences in delta-crystallin from bird and reptile lenses. Biochim Biophys Acta 624:21–29
Inana G, Shinohara T, Maizel JV Jr, Piatigorsky J (1982) Evolution and diversity of the crystallins. Nucleotide sequence of a β-crystallin mRNA from the mouse lens. J Biol Chem 257:9064–9071
Inana G, Piatigorsky J, Norman B, Slingsby C, Blundell T (1983) Gene and protein structure of a β-crystallin polypeptide in murine lens: relationship of exons and structural motifs. Nature 302:310–315
Jones RE, Bhat SP, Sullivan MA, Piatigorsky J (1980) Comparison of two δ-crystallin genes in the chicken. Proc Natl Acad Sci USA 77:5879–5883
Kondel DA, Maizel JV Jr, Leder P (1979) The evolution and sequence comparison of two recently diverged mouse chromosomal β-globin genes. Cell 18:865–873
Lin F-K, Paddock GV (1984) Characterization of duck genome fragments containing beta and epsilon globin genes. Gene 31:59–64
Lok S, Tsui L-C, Shinohara T, Piatigorsky J, Gold R, Breitman M (1984) Analysis of the mouse γ-crystallin gene family: assignment of multiple cDNAs to discrete genomic sequences and characterization of a representative gene. Nucleic Acids Res 12:4517–4529.
Lomedico P, Rosenthal N, Efstratiadis A, Gilbert W, Kolodner R, Tizard R (1979) The structure and evolution of the two nonallelic rat preproinsulin genes. Cell 18:545–558
Maxam AM, Gilbert W (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74:560–564
McDevitt DS, Croft LR (1977) On the existence of γ-crystallin in the bird lens. Exp Eyc Res 25:473–484
Meakin SW, Breitman ML, Tsui L-C (1985) Structural and evolutionary relationships among five members of the human γ-crystallin gene family. Mol Cell Biol 5:1408–1414
Moormann RJM, den Dunnen JT, Bloemendal H, Schoenmakers JGG (1982) Extensive intragenic sequence homology in two distinct rat lens γ-crystallin cDNAs suggests duplications of a primordial gene. Proc. Natl Acad Sci USA 79:6876–6880
Nickerson JM, Piatigorsky J (1984) Sequence of a complete chicken δ-crystallin cDNA. Proc Natl Acad Sci USA 81:2611–2615
Nickerson JM, Wawrousek EF, Hawkins JW, Wakil AS, Wistow GJ, Thomas G, Norman BL, Piatigorsky J (1985) The complete sequence of the chicken δ1 crystallin gene and its 5′ flanking region. J Biol Chem 260:9100–9105
Nickerson JM, Wawrousek EF, Borras T, Hawkins JW, Norman BL, Filpula DR, Nagle JW, Ally AH, Piatigorsky J (1986) Sequence of the chicken δ2 crystallin gene and its intergenic spacer. Extreme homology with the δ1 crystallin gene. J Biol Chem 261:552–557
Ohno M, Sakamoto H, Yasuda K, Okada TS, Shimura Y (1985) Nucleotide sequence of a chicken δ-crystallin gene. Nucleic Acids Res 13:1593–1606
Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproissulin gene. Cell 20:555–566
Piatigorsky J (1981) Structural and functional similarities of δ-crystallin messenger ribonucleic acids from duck and chicken lenses. Biochemistry 20:6427–6431
Piatigorsky J (1984a) Lens crystallins and their gene families. Cell 38:620–621
Piatigorsky J (1984b) Delta crystallins and their nucleic acids. Mol Cell Biochem 59:33–56
Piatigorsky J (1987) Gene expression and genetic engineering in the lens. Invest Ophthalmol & Visual Sci 28:9–28
Reszelbach R, Shinohara T, Piatigorsky J (1977) Resolution of two distinct embryonic chick δ-crystallin bands by polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulfate and urea. Exp Eye Res 25:583–593
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Shinohara T, Reszelbach R, Piatigorsky J (1980) Two tryptic peptide differences among the subunits of δ-crystallin of the embryonic chick lens. Exp Eye Res 30:361–370
Sibley CG, Ahlquist JE (1985) The relationships of some groups of African birds, based on comparisons of the genetic material, DNA. In: Schuchmann (ed) Proceedings of the International Symposium on African Vertebrates. Zoologisches Forschungsinstitut und Museum Alexander Koenig. Bonn, pp 115–161
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517
Spriggs MK, Olmsted RA, Vankatesan S, Coligan JE, Collins PC (1986) Fusion glycoprotein of human parainfluenza virus type 3: nucleotide sequence of the gene, direct identification of the cleavage-activation site, and comparison with other paramyxoviruses. Virology 152:241–251.
Tréton JA, Jones RE, King CR, Piatigorsky J (1984) Evidence against γ-crystallin DNA or RNA sequences in the chicken. Exp Eye Res 39:513–522
Wawrousek EF, Nickerson JM, Piatigorsky J (1986) Two δ-crystallin polypeptides are derived from a cloned δ1-crystallin cDNA. FEBS Lett 205:235–240
Williams LA, Piatigorsky J (1979a) Comparative and evolutionary aspects of δ-crystallin in the vertebrate lens. Eur J Biochem 100:349–357
Williams LA, Piatigorsky J (1979b) Heterogeneity of δ-crystallins of the embryonic mallard lens. Correlation between subunit compositions and isoelectric points. Biochemistry 18:1438–1442
Williams LA, Ding L, Horwitz J, Piatigorsky J (1985) τ-Crystallin from the turtle lens: purification and partial characterization. Exp Eye Res 40:741–749
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639
Wistow G, Slingsby C, Blundell T, Driessen H, de Jong W, Bloemendal H (1981) Eye-lens proteins: the three-dimensional structure of β-crystallin predicted from monomeric γ-crystallin. FEBS Lett 133:9–16
Yasuda K, Kondoh H, Okada TS, Nakajima N, Shimura Y (1982a) Organization of δ-crystallin genes in the chicken. Nucleic Acids Res 10:2879–2891
Yasuda K, Kondoh H, Okaaki K, Shimura Y, Okada TS (1982b) Organization and structure of α- and δ-crystallin genes and their expression in cells by microinjection. Fifth International congress of Eye Research, Eindhoven, The Netherlands, p 38
Yasuda K, Nakajima N, Isobe T, Okada TS, Shimura Y (1984) The nucleotide sequence of a complete chicken δ-crystallin cDNA. EMBO J 3:1397–1402
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Piatigorsky, J., Norman, B. & Jones, R.E. Conservation of δ-crystallin gene structure between ducks and chickens. J Mol Evol 25, 308–317 (1987). https://doi.org/10.1007/BF02603115
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DOI: https://doi.org/10.1007/BF02603115