Abstract
We have characterized several Vicia faba genes encoding methionine residue-free group B subunits of the 11S or legumin storage proteins. The respective gene subfamily consists of 10 to 15 members, six of them having been studied by DNA sequence analysis. Four functional genes (LeB2, LeB4, LeB6, LeB7) are highly homologous in their coding region and 0.3 kb of their 3′ flanking sequences. On the other hand, two pseudogenes (ψLeB1, ψLeB5) have accumulated a large number of mutations including an identical 0.7 kb internal deletion; they are both flanked by a repetitive element. Analysis of sequence changes show that transitions are nearly double as frequent as transversions. CpG is the most infrequent dinucleotide whereas TpA is significantly underrepresented in exon sequences. End points of deletions are correlated with short direct repeats and preferentially found in the two introns. Our studies indicate that the Vicia faba legumin B gene subfamily contains a group of expressed, highly homologous genes as well as more diverged pseudogenes.
Similar content being viewed by others
References
Albertini A, Hofer M, Calos M, Miller J: On the formation of spontaneous deletions: The importance of short sequence homologies in the generation of large deletions. Cell 24: 319–328 (1982).
Bäumlein H, Wobus U, Pustell J, Kafatos FC: The legumin gene family: structure of a B type gene of Vicia faba and a possible legumin gene specific element. Nucleic Acids Res 6: 2707–2720 (1986).
Bäumlein H, Müller A, Schiemann J, Helbing D, Manteuffel R, Wobus U: A legumin B gene of Vicia faba is experessed in developing seeds of transgenic tobacco. Biol Zentralblatt 106: 569–575 (1987).
Boudraa M, Perrin P: CpG and TpA frequencies in the plant system. Nucleic Acids Res 14: 5729–5737 (1987).
Bown D, Levasseur M, Croy RRD, Boulter D, Gatehouse JA: Sequence of a pseudogene in the legumin gene family of pea (Pisum sativum L.). Nucleic Acids Res 13: 4527–4238 (1985).
Brown GG, Lee JS, Brisson N, Verma DPS: The evolution of a plant globin gene family. J Mol Evol 21: 19–32 (1984).
Casey R, Domoney C and Ellis N: Legume storage proteins and their genes. Oxford Surv Plant Mol Cell Biol 3: 1–95 (1986).
Chlan CA, Pyle JB, Legocki AB, DureIII L: Developmental biochemistry of cottonseed embryogenesis and germination. XVIII. cDNA and amino acid sequences of members of the storage protein families. Plant Mol Biol 7: 475–489 (1986).
Cho T-J, Davies CS, Nielsen NC: Inheritance and organization of glycinin genes in soybean. Plant Cell 1: 329–337 (1989).
Croy RRD, Evans IM, Yarwood JN, Harris N, Gatehouse JA, Shirsat AH, Kang A, Ellis JR, Thompson A, Boulter D: Expression of pea legumin sequences in pea, Nicotiana and yeast. Biochem Physiol Pfl 183: 183–197 (1988).
Dasgupta U, Weston-Hafer K, Berg D: Local DNA sequence control of deletion formation in Escherichia coli plasmid pBR322. Genetics 115: 41–49 (1986).
DenDunnen J, Moormann R, Lubsen N, Schoenmakers J: Concerted and divergent evolution within the rat gamma-crystallin gene family. J Mol Biol 189: 37–46 (1986).
Derbyshire E, Wright DJ, Boulter D: Legumin and vicilin, storage proteins of legume seeds. Phytochemistry 15: 3–24 (1976).
Domoney C, Casey R: Measurement of gene number for seed storage proteins in Pisum. Nucleic Acids Res 13: 687–699 (1985).
Domoney C, Ellis THN, Davies DR: Organization and mapping of legumin genes in Pisum. Mol Gen Genet 202: 280–285 (1986).
Doyle JJ, Schuler MA, Godette WD, Zenger V, Beachy RN: The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris. J Biol Chem 261: 9228–9238 (1986).
Efstratiadis A, Posakony JW, Maniatis T, Lawn RM, O'Conell C, Spitz Ra, Riel JK, Forget BJ, Weissmann SM, Slightom JL, Blechl AE, Smithies O, Baralle F, Shoulders CC, Proudfoot NJ: The structure and evolution of the human α-globin gene family. Cell 21: 653–668 (1980).
Glickman B, Ripley L: Structural intermediates of deletion mutagenesis: a role for palindromic DNA. Proc Natl Acad Sci USA 81: 512–516 (1984).
Grandbastian M, Berry-Lowe S, Shirley B, Meagher R: Two soybean ribulose-1, 5-biphosphate carboxylase small subunit genes share extensive homology even in distant flanking sequence. Plant Mol Biol 7: 451–465 (1986).
Harada JH, Barker SJ, Goldberg RB: Soybean α-conglycinin genes are clustered in several DNA regions and are regulated by transcriptional and posttranscriptional processes. Plant Cell 1: 415–425 (1989).
Heim U: Struktur und Evolution der Legumin B-Gen-familie von Vicia faba. Dissertation, AdW der DDR, Fob Biologie/Medizin (1988).
Hood L, Kronenberg M, Hunkapiller T: T cell antigen receptors and the immunoglobulin supergene family. Cell 40: 225–229 (1985).
Horstmann C: Specific subunit pairs of legumin from Vicia faba. Phytochemistry 22: 1861–1866 (1983).
Jeffreys AJ, Harris S: Processes of gene duplication. Nature 296: 9–10 (1982).
Jones CW, Kafatos FC: Accepted mutations in a gene family: Evolutionary diversification of duplicated DNA. J Mol Evol 19: 87–103 (1982).
Kimura M: Estimation of evolutionary distance between homologous nucleotide sequences. Proc Natl Acad Sci USA 78: 454–458 (1981).
Krawinkel U, Zoebelein G, Bothwell A: Palindromic sequences are associated with sites of DNA breakage during gene conversion. Nucleic Acids Res 14: 3871–3882 (1986).
Lehrmann MA, Goldstein JL, Russell DW, Brown MS: Duplication of seven exons in LDL receptor gene caused by Alu-Alu recombination in a subject with familial hypercholesterolemia. Cell 48: 827–835 (1987).
Maeda N, Smithies O: The evolution of multigene families: human haptoglobin genes. Ann Rev Genet 20: 81–108 (1987).
Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
McClelland M: The frequency and distribution of methylable DNA sequences in leguminous plant protein coding genes. J Mol Evol 19: 346–354 (1983).
Müntz K, Horstmann C, Schlesier B: Seed proteins and their genetics in Vicia faba. L. Biol Zentralblatt 105: 107–120 (1986).
Nalbantoglu J, Hartley D, Phear G, Tear G, Meuth M: Spontaneous deletion formation at the aprt locus of hamster cells: the presence of short sequence homologies and dyad symmetries at deletion termini. EMBO J 5: 1199–1204 (1986).
Nalbantoglu J, Phear G, Meuth M: DNA sequence analysis of spontaneous mutations at the aprt locus of hamster cells. Mol Cell Biol 4: 1445–1449 (1987).
Nielsen NC, Dickinson CD, Co T-J, Thanh VH, Scallon BJ, Fischer RL, Sims TL, Drews GN, Golberg RB: Characterization of the glycinin gene family in soybean. Plant Cell 1: 313–328 (1989).
Pang PP, Pruitt RE, Meyerowitz EM: Molecular cloning, genome organization, expression and evolution of 12S seed storage protein genes of Arabidopsis thaliana. Plant Mol Biol 11: 805–820 (1988).
Pustell J, Kafatos FC: A convenient and adaptable microcomputer environment for DNA and protein sequence manipulation and analysis. Nucl Acids Res 14: 479–488 (1986).
Rafalsky JA: Structure of wheat gamma-gliadin genes. Gene 43: 221–229 (1986).
Salser W: Globin mRNA sequences: analysis of base pairing and evolutionary implications. Cold Spring Harbor Symp Quant Biol 42: 985–1002 (1977).
Shen S, Slightom JL, Smithies O: A history of the human fetal globin gene duplication. Cell 26: 191–203 (1981).
Spena A, Viotti A, Pirrotta V: Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction patterns. J Mol Biol 169: 799–811 (1983).
Takaiwa F, Kikuchi S, Oono K: A rice glutelin gene family — A major type of glutelin mRNAs can be divided into two classes. Mol Gen Genet 208: 15–22 (1987).
Walsh JB: Sequence-dependent gene conversion: can duplicated genes diverge fast enough to escape conversion. Genetics 117: 543–557 (1987).
Wobus U, Bäumlein H, Bassüner R, Heim U, Jung R, Müntz K, Panitz R, Saalbach G, Weschke W: Molecular characterization of Vicia faba storage protein specific DNA. Kulturpflanze (Bln.) 32: 5117–5126 (1984).
Wobus U, Bäumlein H, Bassüner R, Heim U, Jung R, Müntz K, Saalbach G, Weschke W: Characteristics of two types of legumin genes in the field bean (Vicia faba L. var. minor) genome as revealed by cDNA analysis. FEBS Lett 201: 74–80 (1986).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Heim, U., Schubert, R., Bäumlein, H. et al. The legumin gene family: structure and evolutionary implications of Vicia faba B-type genes and pseudogenes. Plant Mol Biol 13, 653–663 (1989). https://doi.org/10.1007/BF00016020
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00016020