Skip to main content
NCBI home page
Comparative and Functional Genomics logoLink to Comparative and Functional Genomics
. 2003 Feb;4(1):31–36. doi: 10.1002/cfg.245

Why Chloroplasts and Mitochondria Contain Genomes

John F Allen 1,✉
PMCID: PMC2447392  PMID: 18629105

Abstract

Chloroplasts and mitochondria originated as bacterial symbionts. The larger, host cells acquired genetic information from their prokaryotic guests by lateral gene transfer. The prokaryotically-derived genes of the eukaryotic cell nucleus now function to encode the great majority of chloroplast and mitochondrial proteins, as well as many proteins of the nucleus and cytosol. Genes are copied and moved between cellular compartments with relative ease, and there is no established obstacle to successful import of any protein precursor from the cytosol. Yet chloroplasts and mitochondria have not abdicated all genes and gene expression to the nucleus and to cytosolic translation. What, then, do chloroplast- and mitochondrially-encoded proteins have in common that confers a selective advantage on the cytoplasmic location of their genes? The proposal advanced here is that co-location of chloroplast and mitochondrial genes with their gene products is required for rapid and direct regulatory coupling. Redox control of gene expression is suggested as the common feature of those chloroplast and mitochondrial proteins that are encoded in situ. Recent evidence is consistent with this hypothesis, and its underlying assumptions and predictions are described.

Full Text

The Full Text of this article is available as a PDF (147.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams K. L., Daley D. O., Qiu Y. L., Whelan J., Palmer J. D. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature. 2000 Nov 16;408(6810):354–357. doi: 10.1038/35042567. [DOI] [PubMed] [Google Scholar]
  2. Allen J. F. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol. 1993 Dec 21;165(4):609–631. doi: 10.1006/jtbi.1993.1210. [DOI] [PubMed] [Google Scholar]
  3. Allen J. F., Pfannschmidt T. Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Philos Trans R Soc Lond B Biol Sci. 2000 Oct 29;355(1402):1351–1359. doi: 10.1098/rstb.2000.0697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Allen J. F., Raven J. A. Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J Mol Evol. 1996 May;42(5):482–492. doi: 10.1007/BF02352278. [DOI] [PubMed] [Google Scholar]
  5. Allen John. Photosynthesis of ATP-electrons, proton pumps, rotors, and poise. Cell. 2002 Aug 9;110(3):273–276. doi: 10.1016/s0092-8674(02)00870-x. [DOI] [PubMed] [Google Scholar]
  6. Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
  7. Berks B. C., Sargent F., Palmer T. The Tat protein export pathway. Mol Microbiol. 2000 Jan;35(2):260–274. doi: 10.1046/j.1365-2958.2000.01719.x. [DOI] [PubMed] [Google Scholar]
  8. Bogorad L. Evolution of organelles and eukaryotic genomes. Science. 1975 May 30;188(4191):891–898. doi: 10.1126/science.1138359. [DOI] [PubMed] [Google Scholar]
  9. Claros M. G., Perea J., Shu Y., Samatey F. A., Popot J. L., Jacq C. Limitations to in vivo import of hydrophobic proteins into yeast mitochondria. The case of a cytoplasmically synthesized apocytochrome b. Eur J Biochem. 1995 Mar 15;228(3):762–771. [PubMed] [Google Scholar]
  10. Doolittle W. F. Phylogenetic classification and the universal tree. Science. 1999 Jun 25;284(5423):2124–2129. doi: 10.1126/science.284.5423.2124. [DOI] [PubMed] [Google Scholar]
  11. Embley T. M., Martin W. A hydrogen-producing mitochondrion. Nature. 1998 Dec 10;396(6711):517–519. doi: 10.1038/24994. [DOI] [PubMed] [Google Scholar]
  12. Escobar Galvis M. L., Allen J. F., Hâkansson G. Protein synthesis by isolated pea mitochondria is dependent on the activity of respiratory complex II. Curr Genet. 1998 May;33(5):320–329. doi: 10.1007/s002940050343. [DOI] [PubMed] [Google Scholar]
  13. Gabriel K., Buchanan S. K., Lithgow T. The alpha and the beta: protein translocation across mitochondrial and plastid outer membranes. Trends Biochem Sci. 2001 Jan;26(1):36–40. doi: 10.1016/s0968-0004(00)01684-4. [DOI] [PubMed] [Google Scholar]
  14. Gatenby A. A., Ellis R. J. Chaperone function: the assembly of ribulose bisphosphate carboxylase-oxygenase. Annu Rev Cell Biol. 1990;6:125–149. doi: 10.1146/annurev.cb.06.110190.001013. [DOI] [PubMed] [Google Scholar]
  15. Gray M. W., Burger G., Lang B. F. Mitochondrial evolution. Science. 1999 Mar 5;283(5407):1476–1481. doi: 10.1126/science.283.5407.1476. [DOI] [PubMed] [Google Scholar]
  16. Gray M. W. Mitochondrial genes on the move. Nature. 2000 Nov 16;408(6810):302-3, 305. doi: 10.1038/35042663. [DOI] [PubMed] [Google Scholar]
  17. Henze K., Martin W. How do mitochondrial genes get into the nucleus? Trends Genet. 2001 Jul;17(7):383–387. doi: 10.1016/s0168-9525(01)02312-5. [DOI] [PubMed] [Google Scholar]
  18. Jackson-Constan D., Akita M., Keegstra K. Molecular chaperones involved in chloroplast protein import. Biochim Biophys Acta. 2001 Dec 12;1541(1-2):102–113. doi: 10.1016/s0167-4889(01)00148-3. [DOI] [PubMed] [Google Scholar]
  19. Koehler C. M., Merchant S., Schatz G. How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem Sci. 1999 Nov;24(11):428–432. doi: 10.1016/s0968-0004(99)01462-0. [DOI] [PubMed] [Google Scholar]
  20. Konstantinov Y. M., Lutsenko G. N., Podsosonny V. A. Genetic functions of isolated maize mitochondria under model changes of redox conditions. Biochem Mol Biol Int. 1995 Jun;36(2):319–326. [PubMed] [Google Scholar]
  21. Mahler H. R., Raff R. A. The evolutionary origin of the mitochondrion: a nonsymbiotic model. Int Rev Cytol. 1975;43:1–124. doi: 10.1016/s0074-7696(08)60067-4. [DOI] [PubMed] [Google Scholar]
  22. Martin W., Hoffmeister M., Rotte C., Henze K. An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem. 2001 Nov;382(11):1521–1539. doi: 10.1515/BC.2001.187. [DOI] [PubMed] [Google Scholar]
  23. Martin W., Stoebe B., Goremykin V., Hapsmann S., Hasegawa M., Kowallik K. V. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 1998 May 14;393(6681):162–165. doi: 10.1038/30234. [DOI] [PubMed] [Google Scholar]
  24. Martin W, Herrmann RG. Gene transfer from organelles to the nucleus: how much, what happens, and Why? . Plant Physiol. 1998 Sep;118(1):9–17. doi: 10.1104/pp.118.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. doi: 10.1098/rspb.1999.0792. [DOI] [PMC free article] [Google Scholar]
  26. Palmer J. D. Organelle genomes: going, going, gone! Science. 1997 Feb 7;275(5301):790–791. doi: 10.1126/science.275.5301.790. [DOI] [PubMed] [Google Scholar]
  27. Pfanner Nikolaus, Wiedemann Nils. Mitochondrial protein import: two membranes, three translocases. Curr Opin Cell Biol. 2002 Aug;14(4):400–411. doi: 10.1016/s0955-0674(02)00355-1. [DOI] [PubMed] [Google Scholar]
  28. Pfannschmidt T., Nilsson A., Tullberg A., Link G., Allen J. F. Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life. 1999 Sep;48(3):271–276. doi: 10.1080/713803507. [DOI] [PubMed] [Google Scholar]
  29. Popot J. L., de Vitry C. On the microassembly of integral membrane proteins. Annu Rev Biophys Biophys Chem. 1990;19:369–403. doi: 10.1146/annurev.bb.19.060190.002101. [DOI] [PubMed] [Google Scholar]
  30. Race H. L., Herrmann R. G., Martin W. Why have organelles retained genomes? Trends Genet. 1999 Sep;15(9):364–370. doi: 10.1016/s0168-9525(99)01766-7. [DOI] [PubMed] [Google Scholar]
  31. Robinson C., Bolhuis A. Protein targeting by the twin-arginine translocation pathway. Nat Rev Mol Cell Biol. 2001 May;2(5):350–356. doi: 10.1038/35073038. [DOI] [PubMed] [Google Scholar]
  32. Saccone C., Gissi C., Lanave C., Larizza A., Pesole G., Reyes A. Evolution of the mitochondrial genetic system: an overview. Gene. 2000 Dec 30;261(1):153–159. doi: 10.1016/s0378-1119(00)00484-4. [DOI] [PubMed] [Google Scholar]
  33. Salzberg S. L., White O., Peterson J., Eisen J. A. Microbial genes in the human genome: lateral transfer or gene loss? Science. 2001 May 17;292(5523):1903–1906. doi: 10.1126/science.1061036. [DOI] [PubMed] [Google Scholar]
  34. Sargent Frank, Berks Ben C., Palmer Tracy. Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch Microbiol. 2002 May 22;178(2):77–84. doi: 10.1007/s00203-002-0434-2. [DOI] [PubMed] [Google Scholar]
  35. Schatz G. Protein transport. The doors to organelles. Nature. 1998 Oct 1;395(6701):439–440. doi: 10.1038/26620. [DOI] [PubMed] [Google Scholar]
  36. Schemidt R. A., Qu J., Williams J. R., Brusilow W. S. Effects of carbon source on expression of F0 genes and on the stoichiometry of the c subunit in the F1F0 ATPase of Escherichia coli. J Bacteriol. 1998 Jun;180(12):3205–3208. doi: 10.1128/jb.180.12.3205-3208.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stupar R. M., Lilly J. W., Town C. D., Cheng Z., Kaul S., Buell C. R., Jiang J. Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A. 2001 Apr 17;98(9):5099–5103. doi: 10.1073/pnas.091110398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tovar J., Fischer A., Clark C. G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol. 1999 Jun;32(5):1013–1021. doi: 10.1046/j.1365-2958.1999.01414.x. [DOI] [PubMed] [Google Scholar]
  39. Tullberg A., Alexciev K., Pfannschmidt T., Allen J. F. Photosynthetic electron flow regulates transcription of the psaB gene in pea (Pisum sativum L.) chloroplasts through the redox state of the plastoquinone pool. Plant Cell Physiol. 2000 Sep;41(9):1045–1054. doi: 10.1093/pcp/pcd031. [DOI] [PubMed] [Google Scholar]
  40. Westphal S., Soll J., Vothknecht U. C. A vesicle transport system inside chloroplasts. FEBS Lett. 2001 Oct 12;506(3):257–261. doi: 10.1016/s0014-5793(01)02931-3. [DOI] [PubMed] [Google Scholar]
  41. Wilson R. J., Denny P. W., Preiser P. R., Rangachari K., Roberts K., Roy A., Whyte A., Strath M., Moore D. J., Moore P. W. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol. 1996 Aug 16;261(2):155–172. doi: 10.1006/jmbi.1996.0449. [DOI] [PubMed] [Google Scholar]
  42. Wilson S. B., Davidson G. S., Thomson L. M., Pearson C. K. Redox control of RNA synthesis in potato mitochondria. Eur J Biochem. 1996 Nov 15;242(1):81–85. doi: 10.1111/j.1432-1033.1996.0081r.x. [DOI] [PubMed] [Google Scholar]
  43. van der Giezen Mark, Slotboom Dirk Jan, Horner David S., Dyal Patricia L., Harding Marilyn, Xue Gang-Ping, Embley T. Martin, Kunji Edmund R. S. Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 2002 Feb 15;21(4):572–579. doi: 10.1093/emboj/21.4.572. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Comparative and Functional Genomics are provided here courtesy of Wiley

RESOURCES