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Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases

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Abstract

We have compared the nucleotide and protein sequences of the three maize catalase genes with other plant catalases to reconstruct the evolutionary relationship among these catalases. These sequences were also compared with other eukaryotic and prokaryotic catalases. Phylogenies based on distances and parsimony analysis show that all plant catalases derive from a common ancestral catalase gene and can be divided into three distinct groups. The first, and major, group includes maizeCatl, barleyCat1, riceCatB and most of the dicot catalases. The second group is an apparent dicot-specific catalase group encompassing the tobaccoCat2 and tomatoCat. The third is a monocot-specific catalase class including the maize Cat3, barley Cat2, and riceCatA. The maize Cat2 gene is loosely related to the first group. The distinctive features of monocot-specific catalases are their extreme high codon bias at the third position and low degree of sequence similarity to other plant catalases. Similarities in the intron positions for several plant catalase genes support the conclusion of derivation from a common ancestral gene. The similar intron position between bean catalases and human catalase implies that the animal and plant catalases might have derived from a common progenitor gene sequence.

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Abbreviations

CAT:

catalase protein and isozymes

Cat :

catalase genes and transcripts

References

  • Abler ML, Scandalios JG (1993) Isolation and characterization of a genomic sequence encoding the maizeCat3 catalase gene. Plant Mol Biol 22:1031–1038

    Article  CAS  PubMed  Google Scholar 

  • Acevedo A, Scandalios JG (1991) Catalase and superoxide dismutase gene expression and distribution during stem development in maize. Dev Genet 12:423–430

    Article  CAS  Google Scholar 

  • Bell GI, Najarian RC, Mullenbach GT, Hallewell RA (1986) cDNA sequences coding for human kidney catalase. Nucleic Acids Res 14:5561–5562

    CAS  PubMed  Google Scholar 

  • Bethards LA, Skadsen RW, Scandalios JG (1987) Isolation and characterization of a cDNA clone for theCat2 gene in maize and its homology with other catalases. Proc Natl Acad Sci USA 84:6830–6834

    CAS  PubMed  Google Scholar 

  • Bibb MJ, Findlay PR, Johnson MW (1984) The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene 30:157–166

    Article  CAS  PubMed  Google Scholar 

  • Boldt R, Scandalios JG (1995) Circadian regulation of theCat3 catalase gene in maize (Zea mays L.): entrainment of the circadian rhythm ofCat3 by different light treatments. Plant J 7:989–999

    Article  CAS  Google Scholar 

  • Campbell WH, Gowri G (1990) Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol 92:1–11

    CAS  Google Scholar 

  • Cohen G, Rapatz W, Ruis H (1988) Sequence of theSaccharomyces cerevisiae CTAI gene and amino acid sequence of catalase A derived from it. Eur J Biochem 176:159–163

    CAS  PubMed  Google Scholar 

  • Deisseroth A, Dounce AL (1970) Catalase: physical and chemical properties, mechanism of catalysis, and physiological role. Physiol Rev 50:319–375

    CAS  PubMed  Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    CAS  PubMed  Google Scholar 

  • Dibb NJ, Newman AJ (1989) Evidence that introns arose at protosplice sites. EMBO J 8:2015–2021

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogency Inference Package): version 3.5c. University of Washington, Seattle

    Google Scholar 

  • Fowler T, Rey MW, VahaVahe P, Power SD, Berka RM (1993) TheCatR gene encoding a catalase fromAspergillus niger: primary structure and elevated expression through increased gene copy number and use of a strong promoter. Mol Microbiol 9:989–998

    CAS  PubMed  Google Scholar 

  • Gilbert W (1987) The exon theory of genes. Cold Spring Harb Symp Quart Biol 52:901–905

    CAS  Google Scholar 

  • Gilbert W, Glynias M (1993) On the ancient nature of introns. Gene 135:137–144

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Ruzsa S, Skadsen RW, Scandalios JG (1991) Comparison of theCat2 complementary DNA sequences of a normal catalase activity line (W64A) and a high catalase activity line (R6-67) of maize. Plant Physiol 96:1379–1381

    CAS  Google Scholar 

  • Guan L, Scandalios JG (1993) Characterization of the catalase antioxidant defense geneCatl of maize, and its developmentally regulated expression in transgenic tobacco. Plant J 3:527–536

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Scandalios JG (1995) Developmentally related responses of maize catalase genes to salicylic acid. Proc Natl Acad Sci USA 92:5930–5934

    CAS  PubMed  Google Scholar 

  • Guan L, Polidoros AN, Scandalios JG (1996) Isolation, characterization and expression of the maize Catz catalase gene. Plant Molec Biol (in press)

  • Hartig A, Ruis H (1986) Nucleotide sequence of theSaccharomyces cerevisiae CTTI gene and deduced amino acid sequence of yeast catalase T. Eur J Biochem 160:487–490

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Higo H (1995) Cloning and characterization of three catalase genes from rice. Plant Physiol Suppl 108:74

    Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    CAS  PubMed  Google Scholar 

  • Isin SH, Allen RD (1991) Isolation and characterization of a pea catalase cDNA. Plant Mol Biol 17:1263–1265

    Article  CAS  PubMed  Google Scholar 

  • Kagawa Y, Nojima H, Nukiwa N, Ishizuka M, Nakajima T, Yasuhara T, Tanaka T, Oshima T (1984) High guanine plus cytosine content in the third letter of codons of an extreme thermophile. J Biol Chem 259:2956–2960

    CAS  PubMed  Google Scholar 

  • Kuhsel MG, Strickland R, Palmer JK (1990) An ancient group-I intron shared by eubacteria and chloroplasts. Science 250:1570–1573

    CAS  PubMed  Google Scholar 

  • Lloyd AT, Sharp PM (1992) Evolution of codon usage patterns: the extent and nature of divergence betweenCandida albicans andSaccharomyces cerevisiae. Nucleic Acids Res 20:5289–5295

    CAS  PubMed  Google Scholar 

  • Mori H, Higo K, Higo H, Minobe Y, Matsui H, Chiba S (1992) Nucleotide and derived amino acid sequence of a catalase cDNA isolated from rice immature seeds. Plant Mot Biol 18:973–976

    CAS  Google Scholar 

  • Morita S, Tasaka M, Fujisawa H, Ushimaru T, Tsuji H (1994) A cDNA clone encoding a rice catalase isozyme. Plant Physiol 105:1015–1016

    Article  CAS  PubMed  Google Scholar 

  • Moriyama EN, Hard DL (1993) Codon usage bias and base composition of nuclear genes in Drosophila. Genetics 134:847–858

    CAS  PubMed  Google Scholar 

  • Murry EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic acids Res 17:477–498

    Google Scholar 

  • Murthy MRN, Reid TJ, Sicignano A, Tanaka N, Rossmann MG (1981) Structure of beef liver catalase. J Mol Biol 152:465–499

    Article  CAS  PubMed  Google Scholar 

  • Nakashima H, Yamamoto M, Goto K, Osumi T, Hashimoto T, Endo, H (1990) Isolation and characterization of the rat catalase-encoding gene. Gene 89:279–288

    Article  Google Scholar 

  • Newgard CB, Nakano K, Hwang PK, Fetterick RJ (1986) Sequence analysis of the cDNA encoding human liver glycogen phosphorylase reveals tissue-specific codon usage. Proc Natl Acad Sci USA 83:8132–8136

    CAS  PubMed  Google Scholar 

  • Ni W, Turley RB, Trelease TN (1990) Characterization of a cDNA encoding cottonseed catalase. Biochim Biophys Acta 1049:219–222

    CAS  PubMed  Google Scholar 

  • Ni W, Trelease TN (1991) Post-translational regulation of catalase isozyme expression in cotton seeds. Plant Cell 3:737–744

    Article  CAS  PubMed  Google Scholar 

  • Orr EC, Bewley GC, Orr WC (1990) cDNA and deduced amino acid sequence of Drosophila catalase. Nucleic Acids Res 18:3663

    CAS  PubMed  Google Scholar 

  • Quan F, Korneluk RG, Tropak MG, Gravel RA (1986) Isolation and characterization of the human catalase gene. Nucleic Acids Res 14:5321–5335

    CAS  PubMed  Google Scholar 

  • Redinbaugh MG, Wadsworth GJ, Scandalios JG (1988) Characterization of catalase transcripts and their differential expression in maize. Biochim Biophys Acta 951:104–116

    CAS  PubMed  Google Scholar 

  • Redinbaugh MG, Sabre M, Scandalios JG (1990) Expression of the maizeCat3 catalase gene is under the influence of a circadian rhythm. Proc Natl Acad Sci USA 87:6853–6857

    CAS  PubMed  Google Scholar 

  • Roupakias DG, McMillin DE, Scandalios JG (1980) Chromosomal location of the catalase structural genes inZea mays, using B-A translocations. Theor Appl Genet 58:211–218

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sakajo S, Nkamura K, Asahi T (1987) Molecular cloning and nucleotide sequence of full-length cDNA for sweet potato catalase mRNA. Eur J Biochem 165:437–442

    Article  CAS  PubMed  Google Scholar 

  • Scandalios JG (1965) Subunit dissociation and recombination of catalase isozymes. Proc Natl Acad Sci USA 53:1035–1040

    CAS  PubMed  Google Scholar 

  • Scandalios JG (1974) Subcellular localization of catalase variants coded by two genetic loci during maize development. J Hered 65:28–32

    CAS  Google Scholar 

  • Scandalios JG (1994) Regulation and properties of plant catalases. In: Foyer CH, Mullineaux PM (eds) Causes of photoxidative stress & amelioration of defense system in plants. CRC Press, Boca Raton, pp 275–315

    Google Scholar 

  • Scandalios JG, Tong WF, Roupakias DG (1980)Cat3, a third gene locus coding for a tissue-specific catalase in maize: Genetics, intracellular location, and some biochemical properties. Mol Gen Genet 179:33–41

    Article  CAS  Google Scholar 

  • Scandalios JG, Tsaftaris AS, Chandlee JM, Skadsen RW (1984) Expression of the developmentally regulated catalase (Cat) genes in maize. Dev Genet 4:281–293

    CAS  Google Scholar 

  • Schroeder WA, Shelton JR, Shelton JB, Robberson B, Apell G, Fang RS, Ventura JB (1982) The complete amino acid sequence of bovine liver catalase and the partial sequence of bovine erythrocyte catalase. Arch Biochem Biophys 214:397–421

    CAS  PubMed  Google Scholar 

  • Skadsen RW, Scandalios JG (1987) Translational control of photo-induced expression of theCat2 catalase gene during leaf development in maize. Proc Natl Acad Sci USA 84:2785–2789

    CAS  PubMed  Google Scholar 

  • Suzuki M, Ario T, Hattori T, Nakamura K, Asahi T (1994) Isolation and characterization of two tightly linked catalase genes from castor bean that are differentially regulated. Plant Mol Biol 25:507–516

    Article  CAS  PubMed  Google Scholar 

  • Wadsworth GJ, Scandalios JG (1989) Differential expression of the maize catalase genes during kernel development: the role of steady-state mRNA levels. Dev Genet 10:04–310

    Article  Google Scholar 

  • Willekens H, Villarroel R, Inze D, Van Montagu M, Van camp, W (1994a) Molecular identification of catalases fromNicotiana plumbaginifolia. FEBS Lett 352:79–83

    Article  CAS  Google Scholar 

  • Willekens H, Langebartels C, Tire C, Van Montagu M, Inze D, Van Camp W (1994b) Differential expression of catalase genes inNicotiana plumbaginifolia. Proc Natl Acad Sci USA 91:0450–10454

    Google Scholar 

  • Williamson JD, Scandalios JG (1992) Differential response of maize catalases to abscisic acid:Vpl transcriptional activator is not required for ABA-regulatedCatl expression. Proc Natl Acad Sci USA 89:8842–8846

    CAS  PubMed  Google Scholar 

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  1. Department of Genetics, North Carolina State University, Box 7614, 27695-7614, Raleigh, NC, USA

    Lingqiang Guan & John G. Scandalios

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  1. Lingqiang Guan
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  2. John G. Scandalios
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Correspondence to: J.G. Scandalios

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Guan, L., Scandalios, J.G. Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. J Mol Evol 42, 570–579 (1996). https://doi.org/10.1007/BF02352287

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  • DOI: https://doi.org/10.1007/BF02352287

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