Skip to main content
Log in

Structure and evolution of the largest chloroplast gene (ORF2280): internal plasticity and multiple gene loss during angiosperm evolution

  • Original Articles
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

We have determined the nucleotide sequence of the Pelargonium x hortorum ORF2280 homolog, the largest gene in the plastid genome of most land plants, and compared it to published homologs from Nicotiana tabacum, Epifagus virginiana, Spinacia oleracea, and Marchantia polymorpha. Multiple alignment of protein sequences requires an extraordinary number of gaps, indicating a very high frequency of insertion/deletion events during the evolution of the protein; however, the overall predicted size of the protein varies relatively little among the five species. At 2 109 codons, the Pelargonium gene is smaller than other land plant ORF2280 homologs and exhibits a rate of nucleotide substitution several times higher relative to Nicotiana, Epifagus, and Spinacia. Southern-blot and restriction-mapping studies were carried out to uncover length variation in ORF2280 homologs from 279 species (representing 111 families) of angiosperms. In many independent angiosperm lineages, this gene has sustained deletions ranging in size from 200 bp to almost 6 kb. Based on the severity of deletions, we postulate that the chloroplast homolog of ORF2280 has become nonfunctional in at least four independent lineages of angiosperms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baldauf SL, Palmer JD (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344: 262–265

    Google Scholar 

  • Baldauf SL, Manhart JR, Palmer JD (1990) Different fates of the chloroplast tufA gene following its transfer to the nucleus in green algae. Proc Natl Acad Sci USA 87: 5317–5321

    Google Scholar 

  • Birky CM Jr, Walsh JB (1992) Biased gene conversion, copy number, and apparent mutation rate differences within chloroplast and bacterial genomes. Genetics 130: 677–683

    Google Scholar 

  • Blasko K, Kaplan SA, Higgins KG, Wolfson R, Sears BB (1988) Variation in copy number of a 24-base pair tandem repeat in the chloroplast DNA of Oenothera hookeri strain Johansen. Curr Genet 14: 287–292

    Google Scholar 

  • Bömmer D, Haberhausen G, Zetsche K (1993) A large deletion in the plastid DNA of the holoparasitic flowering plant Cuscuta reflexa concerning two ribosomal proteins (rpl2, rpl23), one transfer RNA (trnl) and an ORF2280 homologue. Curr Genet 24: 171–176

    Google Scholar 

  • Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu Y-L, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedrén M, Gaut BS, Jansen RK, Kim K-J, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang Q-Y, Plunkett GM, Soltis PS, Swensen SM, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn GH Jr., Graham SW, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Missouri Bot Gard 80: 528–580

    Google Scholar 

  • Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Downie SR, Palmer JD (1992 a) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York

    Google Scholar 

  • Downie SR, Palmer JD (1992 b) Restriction site mapping of the chloroplast DNA inverted repeat: a molecular phylogeny of the Asteridae. Ann Missouri Bot Gard 79: 266–283

    Google Scholar 

  • Downie SR, Palmer JD (1994) A chloroplast DNA phylogeny of the Caryophyllales based on structural and inverted repeat restriction site variation. Syst Bot 19(2): (in press)

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation for small quantities of fresh tissue. Phytochem Bull 19: 11–15

    Google Scholar 

  • Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10: 3073–3078

    Google Scholar 

  • Glick RE, Sears BB (1993) Large unidentified open reading frame in plastid DNA (ORF2280) is expressed in chloroplasts. Plant Mol Biol 21: 99–108

    Google Scholar 

  • Herdenberger F, Weil J-H, Steinmetz A (1988) Organization and nucleotide sequence of the broad bean chloroplast genes trnL-UAG, ndhF and two unidentified open reading frames. Curr Genet 14: 609–615

    Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237–244

    Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-O, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNAs accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194

    Google Scholar 

  • Igloi GL, Meinke A, Döry I, Kössel H (1990) Nucleotide sequence of the maize chloroplast rpoB/C 1/C 2 operon: comparison between the derived protein primary structures from various organisms with respect to functional domains. Mol Gen Genet 221: 379–394

    Google Scholar 

  • Manos PS, Nixon KC, Doyle JJ (1993) Cladistic analysis of restriction site variation within the chloroplast DNA inverted repeat region of selected Hamamelididae. Syst Bot 18: 551–562

    Google Scholar 

  • Nimzyk R, Schöndorf T, Hachtel W (1993) In-frame length mutations associated with short tandem repeats are located in unassigned open reading frames of Oenothera chloroplast DNA. Curr Genet 23: 265–270

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene onganization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574

    Google Scholar 

  • Palmer JD (1986) Isolation and structural analysis of chloroplast DNA. Methods Enzymol 118: 167–186

    Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids, vol 7A. Academic Press, San Diego, California, pp 5–53

    Google Scholar 

  • Palmer JD, Stein DB (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10: 823–833

    Google Scholar 

  • Palmer JD, Nugent JM, Herbon LA (1987) Unusual structure of geranium chloroplast DNA: a triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc Natl Acad Sci USA 84: 769–773

    Google Scholar 

  • Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart JR (1988) Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75: 1180–1206

    Google Scholar 

  • Price RA, Palmer JD (1993) Phylogenetic relationships of the Geraniaceae and Geraniales from rbcL sequence comparisons. Ann Missouri Bot Grad 80: 661–671

    Google Scholar 

  • Price RA, Calie PJ, Downie SR, Logsdon JM Jr, Palmer D (1990) Chloroplast DNA variation in the Geraniaceae. In: Vorster P (ed) Proc Inter Geraniaceae symposium. Stellenbosch, South Africa

  • Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255: 1697–1699

    Google Scholar 

  • Richards CM, Hinman SB, Boyer CD, Hardison RC (1991) Survey of plastid RNA abundance during tomato fruit ripening: the amounts of RNA from the ORF2280 region increase in chromoplasts. Plant Mol Biol 17: 1179–1188

    Google Scholar 

  • Shimada H, Sugiura M (1991) Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes. Nucleic Acids Res 19: 983–995

    Google Scholar 

  • Shimada H, Fukuta M, Ishikawa M, Sugiura M (1990) Rice chloroplast RNA polymerase genes: the absence of an intron in rpoC1 and the presence of an extra sequence in rpoC2. Mol Gen Genet 221: 395–402

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Todoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2047

    Google Scholar 

  • Smith AG, Wilson RM, Kaethner TM, Willey DL, Gray JC (1991) Pea chloroplast genes encoding a 4-kDA polypeptide of photosystem I and a putative enzyme of C1 metabolism. Curr Genet 19: 403–410

    Google Scholar 

  • Sugiura M, Shinozaki K, Zaita N, Kususa M, Kumano M (1986) Clone bank of the tobaco (Nicotiana tabacum) chloroplast genome as a set of overlapping restriction endonuclease fragments: mapping of eleven ribosomal protein genes. Plant Sci 44: 211–216

    Google Scholar 

  • Takhtajan AL (1980) Outline of the classification of flowering plants (Magnoliophyta). Bot Rev 46: 225–359

    Google Scholar 

  • Thorne RF (1992) Classification and geography of the flowering plants. Bot Rev 58: 225–348

    Google Scholar 

  • Weglöhner W, Subramanian AR (1991) A heptapeptide repeat contributes to the unusual length of chloroplast ribosomal protein S18. FEBS Lett 279: 193–197

    Google Scholar 

  • Wolfe KH (1994) Similarity of plastid ORF2280 to the CDC48 family: a proteolytic ATPase?. Curr Genet 25: 379–383

    Google Scholar 

  • Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitutions vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84: 9054–9058

    Google Scholar 

  • Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989) Date of the monocot-dieot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86: 6201–6205

    Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1991) Ins and outs of plastid genome evolution. Curr Opin Genet Dey 1: 523–529

    Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1992 a) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89: 10648–10652

    Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1992 b) Small single-copy region of plastid DNA in the non-photosynthetic angiosperm Epifagus virginiana contains only two genes. Differences among dicots, monocots and bryophytes in gene organization at a nonbioenergetic locus. J Mol Biol 223: 95–104

    Google Scholar 

  • Wolfe KH, Morden CW, Ems SE, Palmer JD (1992 c) Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: loss or accelerated sequence evolution of tRNAs and ribosomal protein genes. J Mol Evol 35: 304–317

    Google Scholar 

  • Zhou D-X, Massenet O, Quigley F, Marion MJ, Moneger F, Huber P, Mache R (1988) Characterization of a large inversion in the spinach chloroplast genome relative to Marchantia: a possible transposon-mediated origin. Curr Genet 13: 433–439

    Google Scholar 

  • Zurawski G, Clegg MT (1987) Evolution of higher-plant chloroplast DNA-encoded genes implications for structure-function and phylogenetic studies. Annu Rev Plant Physiol 38: 391–418

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by B. B. Sears

Rights and permissions

Reprints and permissions

About this article

Cite this article

Downie, S.R., Katz-Downie, D.S., Wolfe, K.H. et al. Structure and evolution of the largest chloroplast gene (ORF2280): internal plasticity and multiple gene loss during angiosperm evolution. Curr Genet 25, 367–378 (1994). https://doi.org/10.1007/BF00351492

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00351492

Key words

Navigation