Abstract
We used the chloroplast gene rbcL as a model to study the frequency and relative timing of transfer of chloroplast sequences to the mitochondrial genome. Southern blot survey of 20 mitochondrial DNAs confirmed three previously reported groups of plants containing rbcL in their mitochondrion, while PCR studies identified a new mitochondrial rbcL. Published and newly determined mitochondrial and chloroplast rbcL sequences were used to reconstruct rbcL phylogeny. The results imply five or six separate interorganellar transfers of rbcL among the angiosperms examined, and hundreds of successful transfers across all flowering plants. By taxonomic criteria, the crucifer transfer is the most ancient, two separate transfers within the grass family are of intermediate ancestry, and the morning-glory transfer is most recent. All five mitochondrial copies of rbcL examined exhibit insertion and/or deletion events that disrupt the reading frame (three are grossly truncated); and all are elevated in the proportion of nonsynonymous substitutions, providing clear evidence that these sequences are pseudogenes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Duvall MR, Morton BR (1996) Molecular phylogenetics of Poaceae: an expanded analysis of rbcL sequence data. Mol Phylogenet Evol 5:352–358
Eyre-Walker A, Gaut BS (1997) Correlated substitution rates among plant genomes. Mol Biol Evol 14:455–460
Folkerts O, Hanson MR (1989) Three copies of a single recombination repeat occur on the 443 kb mastercircle of the Petunia hybrida 3704 mitochondrial genome. Nucleic Acids Res 17:7345–7357
Gaut BS (1998) Molecular clocks and nucleotide substitution rates higher plants. Evol Biol 30:93–120
Gaut BS, Muse SV, Clark W, Clegg MT (1992) Relative substitution at the rbcL locus in monocotyledonous plants. J Mol Evol 35:292–303
Gray MW (1983) The bacterial ancestry of plastids and mitochondria. Bioscience 33:693–699
Källersjö M, Farris JS, Chase MW, Bremer B, Fay MF, Humphries CJ, Petersen G, Seberg O, Bremer K (1998) Simultaneous parsimony jackknife analysis of 2538 rbcL DNA sequences reveals support for major clades of green plants, land plants, seed plants and flowering plants. Plant Syst Evol 213:259–287
Kanno A, Nakazono M, Hirai A, Kameya T (1997) Maintenance of chloroplast-derived sequences in the mitochondrial DNA of Gramineae. Curr Genet 32:413–419
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and branching order in Hominoidea. J Mol Evol 229:170–179
Kolodner R, Tewari KK (1972) Physiochemical characterization of mitochondrial DNA from pea leaves. Proc Natl Acad Sci USA 69:1830–1834
Kubo T, Yanai Y, Kinoshita T, Mikami T (1995) The chloroplast trnP-trnW-petG gene cluster in the mitochondrial genomes of Beta vulgaris, B. trigyna and B. webbiana: evolutionary aspects. Curr Genet 27:285–289
Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA) Nucleic Acids Res 28:2571–2576
Lonsdale DM (1989) The plant mitochondrial genome. In: Marcus A. (ed) The biochemistry of plants, vol 15. Academic Press, New York, pp 229–295
Lonsdale DM, Hodge TP, Howe CJ, Stern DB (1983) Maize mitochondrial DNA contains a sequence homologous to the ribulose-1,5-bisphosphate carboxylase large subunit gene of chloroplast DNA. Cell 34:1007–1014
Maeda N, Kitano K, Fukui T, Ezaki S, Atomi H, Miki K, Imanaka T (1999) Ribulose bisphosphate carboxylase/oxygenase from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 is composed solely of large subunits and forms a pentagonal structure. J Mol Biol 293:57–66
Marienfeld J, Unseld M, Brennicke A (1999) The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci 4:495–502
Moon E, Kao T-H, Wu R (1987) Rice chloroplast DNA molecules are heterogeneous as revealed by DNA sequences of a cluster of genes. Nucleic Acids Res 15:611–630
Nakazono M, Hirai A (1993) Identification of the entire set of transferred chloroplast DNA sequences in the mitochondrial genome of rice. Mol Gen Genet 236:341–346
Nugent JM, Palmer JD (1988) Location, identity, amount and serial entry of chloroplast DNA sequences in crucifer mitochondrial DNAs. Curr Genet 14:501–509
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced for the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. J Mol Biol 223:1–7
Olmstead RG, Michaels HJ, Scott KM, Palmer JD (1992) Monophyly of the Asteridae and identification of their major lineages inferred from DNA sequences of rbcL. Ann Mo Bot Gard 79:249–265
Palmer JD (1992) Comparison of chloroplast and mitochondrial genome evolution in plants. In: Herrmann RG (ed) Cell organelles. Springer, Berlin Heidelberg New York, pp 99–133
Palmer JD, Shields CR (1984) Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307:437–440
Qiu Y-L, Chase MW, Les DH, Parks CR (1993) Molecular phylogenetics of the Magnoliidae: cladistic analyses of nucleotide sequences of the plastid gene rbcL. Ann Mo Bot Gard 80:587–606
Rodman J, Price RA, Karol K, Conti E, Sytsma KJ, Palmer JD (1993) Nucleotide sequences of the rbcL gene indicate monophyly of mustard oil plants. Ann Mo Bot Gard 80:686–699
Schuster W, Brennicke A (1988) Interorganellar sequence transfer: plant mitochondrial DNA is nuclear, is plastid, is mitochondrial. Plant Sci 54:1–10
Sennblad B, Endress ME, Bremer B (1998) Morphology and molecular data in phylogenetic fraternity: the tribe Wrightieae (Apocynaceae) revisited. Am J Bot 85:1143–1158
Siculella L, Palmer JD (1988) Physical and gene organization of mitochondrial DNA in fertile and male sterile sunflower. CMS-associated alterations in structure and transcription of the atpA gene. Nucleic Acids Res 16:3787–3799
Siemeister G, Hachtel W (1990) Structure and expression of a gene encoding the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL) in the colourless euglenoid flagellae Asasia longa. Plant Mol Biol 14:825–833
Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from a combined data set of 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461
Stern DB (1987) DNA transposition between plant organellar genomes. J Cell Sci Suppl 7:145–154
Stern DB, Lonsdale DM (1982) Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature 299:698–702
Stern DB, Palmer JD (1984) Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants. Proc Natl Acad Sci USA 81:1946–1950
Stern DB, Palmer JD (1986) Tripartite mitochondrial genome of spinach: physical structure, mitochondrial gene mapping, and location of transposed chloroplast DNA sequences. Nucleic Acids Res 14:5651–5666
Swofford DL (2002) PAUP* 4.0 beta 10. *Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, Mass.
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Turmel M, Otis C, Lemieux C (2002) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275–11280
Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nature Genetics 15:57–61
Watanabe N, Nakazono M, Kanno A, Tsutsumi N, Hirai A (1994) Evolutionary variations in DNA sequences transferred from chloroplast genomes to mitochondrial genomes in the Gramineae. Curr Genet 26:512–518
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 15:555–556
Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43
Yang Z, Kumar S, Nei M (1995) A new method of inference of ancestral nucleotide and amino-acid sequences. Genetics 141:1641–1650
Acknowledgements
We thank Kathy Scott, Colleen Dixon, and Laura McInerney for technical assistance, Robert Price for providing cpDNA rbcL sequences, Maureen Hanson, Kathleen Newton, and Barbara Sears for providing mtDNA samples, David Lonsdale for providing the maize mitochondrial clone pLSH20, Gerard Zurawski for providing sequencing primers, Elizabeth Kellogg for comments on Poaceae relationships, and Lawrence Bogorad and Steven Rodermel for encouragement. This work was supported, in part, by National Institutes of Health grant GM-35087 to J.D.P.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F.-A. Wollman
Rights and permissions
About this article
Cite this article
Cummings, M.P., Nugent, J.M., Olmstead, R.G. et al. Phylogenetic analysis reveals five independent transfers of the chloroplast gene rbcL to the mitochondrial genome in angiosperms. Curr Genet 43, 131–138 (2003). https://doi.org/10.1007/s00294-003-0378-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-003-0378-3