Abstract
Nuclear protein coding sequences from gymnosperms are currently scarce. We have determined 4 kb of nuclear protein coding sequences from gymnosperms and have collected and analyzed >60 kb of nuclear sequences from gymnosperms and nonspermatophytes in order to better understand processes influencing genome evolution in plants. We show that conifers possess both biased and nonbiased genes with respect to GC content, as found in monocots, suggesting that the common ancestor of conifers and monocots may have possessed both biased and nonbiased genes. The lack of biased genes in dicots is suggested to be a derived character for this lineage. We present a simple but speculative model of land-plant genome evolution which considers changes in GC bias and CpG frequency, respectively, as independent processes and which can account for several puzzling aspects of observed nucleotide frequencies in plant genes.
Similar content being viewed by others
Abbreviations
- GC:
-
guanosine plus cytosine
- GapC:
-
glycolytic glyceraldehyde-3-phosphate dehydrogenase, EC 1.2.1.12
- GapA:
-
Calvin cycle glyceraldehyde-3-phosphate dehydrogenase, EC 1.2.1.13
- O/E:
-
ratio of observed-to-expected dinucleotide frequencies
References
Belanger FC, Hepburn AG (1990) The evolution of CpNpG methylation in plants. J Mol Evol 30:26–35
Bernardi G (1989) The isochore organization of the human genome. Annu Rev Genet 23:637–661
Bernardi G (1993) The vertebrate genome: Isochores and evolution. Mol Biol Evol 10:186–204
Bird AP (1986) CpG-rich islands and the function of DNA methylation. Nature 321:209–213
Bohr VA, Smith CA, Okamoto DS, Hanawalt PC (1985) DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40:359–369
Bootsma D, Hoeijmakers JHJ (1993) Engagement with transcription. Nature 363:114–115
Brinkmann H, Martinez P, Quigley F, Martin W, Cerff R (1987) Endosymbiontic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. J Mol Evol 26:320–328
Brinkmann H, Cerff R, Salomon M, Soll J (1989) Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Mol Biol 13:81–94
Campbell WH, Gowri G (1990) Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol 92:1–11
Cerff R (1979) Quaternary structure of higher plant glyceraldehyde-3-phosphate dehydrogenases. Eur J Biochem 94:243–247
Cerff R, Kloppstech K (1982) Structural diversity and differential light control of mRNAs coding for angiosperm glyceraldehyde-3-phosphate dehydrogenases. Proc Natl Acad Sci USA 79:7624–7628
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Downes CS, Anderson JR, Johnson RT (1993) Fine tuning of DNA repair in trancribed genes: mechanisms, prevalence and consequences. Bioessays 15:209–216
Drouin G, Dover GA (1990) Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phylogeny of angiosperm actin genes. J Mol Evol 31:132–150
Fliegmann J, Schröder G, Schanz S, Britsch L, Schröder J (1992) Molecular analysis of chalcone and dihydropinosylvin synthase from Scots pine (Pious sylvestris), and differential regulation of these and related enzyme activities in stressed plants. Plant Mol Biol 18:489–503
Gardiner-Garden M, Frommer M (1992) Significant CpG-rich regions in angiosperm genes. J Mol Evol 14:231–245
Gardiner-Garden M, Sved JA, Frommer M (1992) Methylation sites in angiosperm genes. J Mol Evol 34:219–230
Gruenbaum Y, Naveh-Many T, Cedar H, Razin A (1981) Sequence specificity of methylation in higher plant DNA. Nature 292: 860–862
Hepburn A, Belanger F, Mattheis J (1987) DNA methylation in plants. Dev Genet 8:475–493
Hoeijmakers JHJ (1993) Nucleotide excision repair I: from E. coli to yeast. Trends Genet 9:173–177
Hutchison KW, Harvie PD, Singer PB, Brunner AF, Greenwood MS (1990) Nucleotide sequence of the small subunit of ribulose-1,5-bisphosphate carboxylase from the conifer Larix laricina. Plant Mol Biol 14:281–284
Jansson S, Gusafsson P (1990) Type I and Type II genes for the chlorophyll a/b-binding protein in the gymnosperm Pinus sylvestris (Scots pine): cDNA cloning and sequence analysis. Plant Mol Biol 14:287–296
Jansson S, Gustafsson P (1991) Evolutionary conservation of the chlorophyll a/b-binding proteins: cDNAs encoding Type I, 11, and III LHC I polypeptides from the gymnosperm Scots pine. Mol Gen Genet 229:67–76
Karpinski S, Wingsle G, Olsson O, Hällgren JE (1992) Characterization of cDNA encoding CuZn-superoxide dismutases in Scots pine. Plant Mol Biol 18:545–555
Kenny JR, Dancik BP, Florence LZ, Nargang FE (1988) Nucleotide sequence of the carboxy-terminal portion of a lodgepole pine actin gene. Can J For Res 18:1595–1602
Kersarnach R, Brinkmann H, Liaud M-F, Zhang D-X, Martin W, Cerff R (1994) Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature 367:387–389
Kinlaw CS, Harry DE, Sederoff RR (1990) Isolation and characterization of alcohol dehydrogenase cDNAs from Pinus radiata. Can J For Res 20:1343–1350
Kojima K, Yamamoto N, Sasaki S (1992) Structure of the pine (Pinus thunbergii) chlorophyll a/b-binding protein gene expressed in the absence of light. Plant Mol Biol 19:405–410
Leal I, Misre S (1993) Molecular cloning and characterisation of a legumin-like storage protein cDNA of douglas fir seeds. Plant Mol Biol 21:709–715
Leech MJ, Martin CM, Wang TL (1993) Regulation of myb-related genes in the moss Physcomitrella patens. Plant J 3:51–61
Long Z, Wang SY, Nelson N (1989) Cloning and nucleotide sequence analysis of genes coding for the major chlorophyll-binding protein of the moss Physcomitrella patens and the halotolerant alga Dunaliella salina. Gene 76:299–312
Martin W, Cerff R (1986) Prokaryotic features of a nucleus encoded enzyme: cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem 159:323–331
Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48
Martin W, Lagrange T, Li Y-F, Bisanz-Seyer C, Mache R (1990) Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach. Carr Genet 18:553–556
Martin W, Lydiate D, Brinkmann H, Forkmann G, Saedler H, Cerff R (1993a)Molecular phylogenies in angiosperm evolution. Mol Biol Evol 10:140–163
Martin W, Nock S, Meyer-Gauen G, Häger K-P, Jensen U, Cerff R (1993b) A method for isolation of cDNA-quality mRNA from immature seeds of a gymnosperm rich in polyphenolics. Plant Mol Biol 22:555–556
Martin W, Brinkmann H, Savonna C, Cerff R (1993c) Evidence for a chimeric nature of nuclear genomes: Eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692–9696
Martinez P, Martin W, Cerff R (1989) Structure, evolution and anaerobic regulation of a nuclear gene encoding cytosolic matrix dehydrogenase from maize. J Mol Biol 208:551–565
Matassi G, Montero LM, Salinas J, Bernardi G (1989) The isochore organisation and compositional distribution of homologous coding sequences in the nuclear genome of plants. Nucleic Acids Res 17:5273–5290
Matassi G, Melis R, Mecaya G, Bernardi G (1991) Compositional bimodality of the nuclear genome of tobacco. Nucleic Acids Res 19:3561–3567
Matsuoka M (1990) Classification and characterization of cDNA that encodes the light-harvesting chlorophyll a/b binding protein of photosystem II from rice. Plant Cell Physiol 31:519–526
Matsuoka M, Kano-Murakami Y, Tanaka Y, Ozeki Y, Yamamoto N (1988) Classification and nucleotide sequence of cDNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase from rice. Plant Cell Physiol 29:1015–1022
Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560
McElroy D, Rothenberg M, Wu R (1990) Structural characterization of a rice action gene. Plant Mol Biol 14:163–171
McGrath JM, Pichersky E (1991) 5-methylcytosine content in homosporous ferns. Abstract 1822, Third International Congress of ISPMB, Tucson
Mellon I, Hanawalt PC (1989) Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed strand. Nature 342:95–97
Minami E, Ozeki Y, Matsuoka M, Koizuka N, Tanaka Y (1989) Structure and some characterization of the gene for phenylalanine ammonia-lyase from rice plants. Eur J Biochem 185:19–25
Montero LM, Salinas J, Matassi G, Bernardi G (1990) Gene distribution and isochore organisation in the nuclear genome of plants. Nucleic Acids Res 18:1857–1867
Newton CH, Flinn BS, Sutton BCS (1992) Vicilin-like seed storage proteins in the gymnosperm interior spruce (Picea glaucalengelmanii). Plant Mol Biol 20:315–322
Niesbach-Klösgen U, Barzen E, Bernhardt J, Rohde W, Schwarz-Sommer Zs, Reif HJ, Wienand U, Saedler H (1987) Chalcone synthase genes in plants: a tool to study evolutionary relationships. J Mol Evol 26:213–225
O'Neill SD, Tong Y, Spörlein B, Forkmann G, Yoder JI (1990) Molecular genetic analysis of chalcone synthase in Lycopersicon esculentum and an anthocyanin-deficient mutant. Mol Gen Genet 224:279–288
Perl-Treves R, Nacmias B, Aviv D, Zeelon EP, Galun E (1988) Isolation of two cDNA clones from tomato containing two different superoxide dismutase sequences. Plant Mol Biol 11:609–623
Pichersky E, Bernatzky R, Tanksley SD, Breidenbach B, Kausch AP, Cashmore AR (1985) Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll al/b-binding proteins in Lycopersicon esculentum (tomato). Gene 40:247–258
Pichersky E, Hoffman NE, Malik VS, Bernatzky R, Tanksley SD, Szabo L, Cashmore AR (1987) The tomato Cab-4 and Cab-5 genes encode a second type of CAB polypeptides localized in photosystem II. Plant Mot Biol 9:109–120
Pichersky E, Soltis D, Soltis P (1990) Defective chlorophyll a/b-binding protein genes in the genome of a homosporous fern. Proc Natl Acad Sci USA 87:195–199
Pichersky E.Subramaniam R, White MJ, Reid J, Aebersold R, Green BR (1991) Chlorophyll a/b binding polypeptides of CP29, the internal chlorophyll a/b complex of PSIL Characterization of the tomato gene encoding the 26 kDa (type I) polypeptide, and evidence for a second CP29 polypeptide. Mol Gen Genet 227:277–284
Quigley F, Martin W, Cerff R (1988) Intron conservation across the prokaryote-eukaryote boundry: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci USA 85:2672–2676
Quigley F, Brinkmann H, Martin W, Cerff R (1989) Strong functional GC-pressure in a light regulated maize gene encoding chloroplast GAPA: implications for the evolution of GAPA pseudogenes. J Mol Evol 29:412–421
Rohde W, Dörr S, Salamini F, Becker D (1991) Structure of a chalcone synthase gene from Hordeum vulgare. Plant Mol Biol 16: 1103–1106
Sakamoto A, Ohsuga H, Tanaka K (1992) Nucleotide sequences of two cDNA clones encoding different Cu/Zn-superoxide dismutases expressed in developing rice seed (Oryza sativa L.). Plant Mol Biol 19:323–327
Salinas J, Matassi G, Montero LM, Bernardi G (1988) Compositional compartmentalization and compositional pattern in the nuclear genomes of plants. Nucleic Acids Res 16:4269–4285
Schaeffer L, Roy R, Humbert S, Moncollin V, Vermeulen W, Hoeijmakers JHJ, Chambon P, Egly J-M (1993) DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 260:58–63
Schultz R, Steinmüller K, Klaas M, Forreiter C, Rasmussen S, Hiller C, Apel K (1989) Nucleotide sequence of a cDNA coding for the NADPH-protochlorophyllide oxidoreductase (PCR) of barley (Hordeum vulgare L.) and its expression in Escherichia coli. Mol Gen Genet 217:355–361
Schwarz-Sommer Z, Gierl A, Klösgen RB, Wienand U, Petersen PA, Saedler H (1984) The Spm (En) transposable element controls the excision of a 2-kb DNA insert at the wx m-8 allele of Zea mays. EMBO J 3:1021–1028
Schwekendiek A, Pfeffer G, Kindl H (1992) Pine stilbene synthase cDNA, a tool for probing environmental stress. FEBS Lett 301:41–44
Selby CP, Sancar A (1993) Molecular mechanism of transcription repair coupling. Science 260:53–58
Shih M-C, Lazar G, Goodman HM (1986) Evidence in favor of the symbiotic origin of chloroplasts: primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases. Cell 47:73–80
Sørensen AB, Lauridsen BF, Gausing K (1992) Barley (Hordeum vulgare) gene for CP29, a core chlorophyll a/b binding protein of photosystem II. Plant Physiol 98:1538–1540
Spano AJ, He Z, Michel H, Hunt DF, Timko MP (1992a) Molecular cloning, nuclear gene structure and developmental expression of NADPH-protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18:967–972
Spano AJ, He Z, Timko MP (1992b) NADPH:protochlorophyllide oxidoreductases in white pine (Pinus strobus) and loblolly pine (P. taeda). Mol Gen Genet 236:86–95
Stepien PP, Margossian SP, Landsman D, Butow RA (1992) The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc Natl Acad Sci USA 89:6813–6817
Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657
Sugita M, Manzara T, Pichersky E, Cashmore A, Gruissem W (1987) Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato. Mol Gen Genet 209:247–256
Sund»s A, Tandre K, Holmstedt E, Engström P (1992) Differential gene expression during germination and after the induction of adventitious bud formation in Norway spruce embryos. Plant Mol Biol 18:713–724
Sweder KS, Hanawalt PC (1992) Preferred repair of cyclobutane pyrimidine dinners in the transcribed strand of a gene in yeast chromosomes and plasmids is dependent on transcription. Proc Natl Acad Sci USA 89:10696–10700
Thüümmler F, Dufner M, Kreisl PP, Dittrich P (1992) Molecular cloning of a novel phytochrome gene of the moss Ceratodon purpureus which encodes a putative light-regulated protein kinase. Plant Mol Biol 20:1003–1017
Van Der Straeten D, Rodrigues-Pousada RA, Gielen J, Van Montagu M (1991) Tomato alcohol dehydrogenase: Expression during fruit ripening and under hypoxic conditions. FEBS Lett 295:39–42
Whetten RW, Sederoff RR (1992) Phenylalanine ammonia-lyase from loblolly pine: Purification of the enzyme and isolation of complementary DNA clones. Plant Physiol 98:380–386
Wolfe KH, Sharp P, Li W-H (1989) Mutation rates differ among regions of the mammalian genome. Nature 337:283–285
Xie Y, Wu R (1989) Rice alcohol dehydrogenase genes: anaerobic induction, organ specific expression and characterization of cDNA clones. Plant Mol Biol 13:53–68
Yamamoto N, Kano-Murakami Y, Matsuoka M, Ohashi Y, Tanaka Y (1988a) Nucleotide sequence of a full length cDNA clone of ribulose bisphosphate carboxylase small subunit gene from green dark-grown pine (Pinus tunbergii) seedling. Nucleic Acids Res 16:11830
Yamamoto N, Matsuoka M, Kano-Murakimi Y, Tanaka Y, Ohashi Y (1988b) Nucleotide sequence of a full length cDNA clone of light harvesting chlorophyll a/b binding protein gene from dark-grown pine (Pinus thunbergii) seedlings. Nucleic Acids Res 16:11829
Author information
Authors and Affiliations
Additional information
Correspondence to: W. Martin
Rights and permissions
About this article
Cite this article
Jansson, S., Meyer-Gauen, G., Cerff, R. et al. Nucleotide distribution in gymnosperm nuclear sequences suggests a model for GC-content change in land-plant nuclear genomes. J Mol Evol 39, 34–46 (1994). https://doi.org/10.1007/BF00178247
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00178247