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. 1991 Oct;10(10):3073–3078. doi: 10.1002/j.1460-2075.1991.tb07859.x

Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron.

J S Gantt 1, S L Baldauf 1, P J Calie 1, N F Weeden 1, J D Palmer 1
PMCID: PMC453023  PMID: 1915281

Abstract

Most chloroplast and mitochondrial proteins are encoded by nuclear genes that once resided in the organellar genomes. Transfer of most of these genes appears to have occurred soon after the endosymbiotic origin of organelles, and so little is known about the process. Our efforts to understand how chloroplast genes are functionally transferred to the nuclear genome have led us to discover the most recent evolutionary gene transfer yet described. The gene rpl22, encoding chloroplast ribosomal protein CL22, is present in the chloroplast genome of all plants examined except legumes, while a functional copy of rpl22 is located in the nucleus of the legume pea. The nuclear rpl22 gene has acquired two additional domains relative to its chloroplast ancestor: an exon encoding a putative N-terminal transit peptide, followed by an intron which separates this first exon from the evolutionarily conserved, chloroplast-derived portion of the gene. This gene structure suggests that the transferred region may have acquired its transit peptide by a form of exon shuffling. Surprisingly, phylogenetic analysis shows that rpl22 was transferred to the nucleus in a common ancestor of all flowering plants, at least 100 million years preceding its loss from the legume chloroplast lineage.

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Selected References

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

  1. Baldauf S. L., Manhart J. R., Palmer J. D. Different fates of the chloroplast tufA gene following its transfer to the nucleus in green algae. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5317–5321. doi: 10.1073/pnas.87.14.5317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baldauf S. L., Palmer J. D. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990 Mar 15;344(6263):262–265. doi: 10.1038/344262a0. [DOI] [PubMed] [Google Scholar]
  3. Campbell W. H., Gowri G. Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol. 1990 Jan;92(1):1–11. doi: 10.1104/pp.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Christopher D. A., Cushman J. C., Price C. A., Hallick R. B. Organization of ribosomal protein genes rpl23, rpl2, rps19, rpl22 and rps3 on the Euglena gracilis chloroplast genome. Curr Genet. 1988 Sep;14(3):275–285. doi: 10.1007/BF00376748. [DOI] [PubMed] [Google Scholar]
  5. Crepet W. L., Taylor D. W. The diversification of the leguminosae: first fossil evidence of the mimosoideae and papilionoideae. Science. 1985 May 31;228(4703):1087–1089. doi: 10.1126/science.228.4703.1087. [DOI] [PubMed] [Google Scholar]
  6. Dyer M. R., Gay N. J., Powell S. J., Walker J. E. ATP synthase from bovine mitochondria: complementary DNA sequence of the mitochondrial import precursor of the gamma-subunit and the genomic sequence of the mature protein. Biochemistry. 1989 May 2;28(9):3670–3680. doi: 10.1021/bi00435a008. [DOI] [PubMed] [Google Scholar]
  7. Evrard J. L., Kuntz M., Weil J. H. The nucleotide sequence of five ribosomal protein genes from the cyanelles of Cyanophora paradoxa: implications concerning the phylogenetic relationship between cyanelles and chloroplasts. J Mol Evol. 1990 Jan;30(1):16–25. doi: 10.1007/BF02102449. [DOI] [PubMed] [Google Scholar]
  8. Fitch W. M., Margoliash E. Construction of phylogenetic trees. Science. 1967 Jan 20;155(3760):279–284. doi: 10.1126/science.155.3760.279. [DOI] [PubMed] [Google Scholar]
  9. Fukuzawa H., Kohchi T., Sano T., Shirai H., Umesono K., Inokuchi H., Ozeki H., Ohyama K. Structure and organization of Marchantia polymorpha chloroplast genome. III. Gene organization of the large single copy region from rbcL to trnI(CAU). J Mol Biol. 1988 Sep 20;203(2):333–351. doi: 10.1016/0022-2836(88)90003-4. [DOI] [PubMed] [Google Scholar]
  10. Gilbert W. The exon theory of genes. Cold Spring Harb Symp Quant Biol. 1987;52:901–905. doi: 10.1101/sqb.1987.052.01.098. [DOI] [PubMed] [Google Scholar]
  11. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  12. Haas R. C., Korenfeld C., Zhang Z. F., Perryman B., Roman D., Strauss A. W. Isolation and characterization of the gene and cDNA encoding human mitochondrial creatine kinase. J Biol Chem. 1989 Feb 15;264(5):2890–2897. [PubMed] [Google Scholar]
  13. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  14. Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet. 1989 Jun;217(2-3):185–194. doi: 10.1007/BF02464880. [DOI] [PubMed] [Google Scholar]
  15. Jacobsen K., Laursen N. B., Jensen E. O., Marcker A., Poulsen C., Marcker K. A. HMG I-like proteins from leaf and nodule nuclei interact with different AT motifs in soybean nodulin promoters. Plant Cell. 1990 Jan;2(1):85–94. doi: 10.1105/tpc.2.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kao J. S., Wu M. The sequence of the plastid encoded rpl22 protein in marine macroalgae, Gracilaria tenuistipitata. Nucleic Acids Res. 1990 May 25;18(10):3067–3067. doi: 10.1093/nar/18.10.3067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lagacé M., Howell B. W., Burak R., Lusty C. J., Shore G. C. Rat carbamyl-phosphate synthetase I gene. Promoter sequence and tissue-specific transcriptional regulation in vitro. J Biol Chem. 1987 Aug 5;262(22):10415–10418. [PubMed] [Google Scholar]
  18. Madsen L. H., Kreiberg J. D., Gausing K. A small gene family in barley encodes ribosomal proteins homologous to yeast YL17 and L22 from archaebacteria, eubacteria, and chloroplasts. Curr Genet. 1991 May;19(5):417–422. doi: 10.1007/BF00309605. [DOI] [PubMed] [Google Scholar]
  19. McLaughlin W. E., Larrinua I. M. The sequence of the maize plastid encoded rpl 22 locus. Nucleic Acids Res. 1987 May 26;15(10):4356–4356. doi: 10.1093/nar/15.10.4356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Michalowski C. B., Pfanzagl B., Löffelhardt W., Bohnert H. J. The cyanelle S10 spc ribosomal protein gene operon from Cyanophora paradoxa. Mol Gen Genet. 1990 Nov;224(2):222–231. doi: 10.1007/BF00271555. [DOI] [PubMed] [Google Scholar]
  21. Milligan B. G., Hampton J. N., Palmer J. D. Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol. 1989 Jul;6(4):355–368. doi: 10.1093/oxfordjournals.molbev.a040558. [DOI] [PubMed] [Google Scholar]
  22. Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
  23. Ohkubo S., Muto A., Kawauchi Y., Yamao F., Osawa S. The ribosomal protein gene cluster of Mycoplasma capricolum. Mol Gen Genet. 1987 Dec;210(2):314–322. doi: 10.1007/BF00325700. [DOI] [PubMed] [Google Scholar]
  24. Oliver J. L., Marín A., Martínez-Zapater J. M. Chloroplast genes transferred to the nuclear plant genome have adjusted to nuclear base composition and codon usage. Nucleic Acids Res. 1990 Jan 11;18(1):65–73. doi: 10.1093/nar/18.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Palmer J. D. Comparative organization of chloroplast genomes. Annu Rev Genet. 1985;19:325–354. doi: 10.1146/annurev.ge.19.120185.001545. [DOI] [PubMed] [Google Scholar]
  26. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  27. Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Spielmann A., Roux E., von Allmen J. M., Stutz E. The soybean chloroplast genome: complete sequence of the rps19 gene, including flanking parts containing exon 2 of rpl2 (upstream), but rpl22 (downstream). Nucleic Acids Res. 1988 Feb 11;16(3):1199–1199. doi: 10.1093/nar/16.3.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Suiter K. A., Wendel J. F., Case J. S. LINKAGE-1: a PASCAL computer program for the detection and analysis of genetic linkage. J Hered. 1983 May-Jun;74(3):203–204. doi: 10.1093/oxfordjournals.jhered.a109766. [DOI] [PubMed] [Google Scholar]
  30. Takeshima H., Joh T., Tsuzuki T., Shimada K., Matsukado Y. Structural organization of the mouse mitochondrial malate dehydrogenase gene. J Mol Biol. 1988 Mar 5;200(1):1–11. doi: 10.1016/0022-2836(88)90328-2. [DOI] [PubMed] [Google Scholar]
  31. Takiguchi M., Murakami T., Miura S., Mori M. Structure of the rat ornithine carbamoyltransferase gene, a large, X chromosome-linked gene with an atypical promoter. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6136–6140. doi: 10.1073/pnas.84.17.6136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tanaka M., Wakasugi T., Sugita M., Shinozaki K., Sugiura M. Genes for the eight ribosomal proteins are clustered on the chloroplast genome of tobacco (Nicotiana tabacum): similarity to the S10 and spc operons of Escherichia coli. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6030–6034. doi: 10.1073/pnas.83.16.6030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Traut T. W. Do exons code for structural or functional units in proteins? Proc Natl Acad Sci U S A. 1988 May;85(9):2944–2948. doi: 10.1073/pnas.85.9.2944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tsuzuki T., Obaru K., Setoyama C., Shimada K. Structural organization of the mouse mitochondrial aspartate aminotransferase gene. J Mol Biol. 1987 Nov 5;198(1):21–31. doi: 10.1016/0022-2836(87)90454-2. [DOI] [PubMed] [Google Scholar]
  35. Wolfe K. H., Gouy M., Yang Y. W., Sharp P. M., Li W. H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6201–6205. doi: 10.1073/pnas.86.16.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wolfe K. H., Li W. H., Sharp P. M. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9054–9058. doi: 10.1073/pnas.84.24.9054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wolter F. P., Fritz C. C., Willmitzer L., Schell J., Schreier P. H. rbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci U S A. 1988 Feb;85(3):846–850. doi: 10.1073/pnas.85.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zhou D. X., Quigley F., Massenet O., Mache R. Cotranscription of the S10- and spc-like operons in spinach chloroplasts and identification of three of their gene products. Mol Gen Genet. 1989 Apr;216(2-3):439–445. doi: 10.1007/BF00334388. [DOI] [PubMed] [Google Scholar]
  39. Zurawski G., Zurawski S. M. Structure of the Escherichia coli S10 ribosomal protein operon. Nucleic Acids Res. 1985 Jun 25;13(12):4521–4526. doi: 10.1093/nar/13.12.4521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. van den Boogaart P., Samallo J., Agsteribbe E. Similar genes for a mitochondrial ATPase subunit in the nuclear and mitochondrial genomes of Neurospora crassa. Nature. 1982 Jul 8;298(5870):187–189. doi: 10.1038/298187a0. [DOI] [PubMed] [Google Scholar]
  41. von Heijne G. Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 1986 Jun;5(6):1335–1342. doi: 10.1002/j.1460-2075.1986.tb04364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. von Heijne G., Steppuhn J., Herrmann R. G. Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem. 1989 Apr 1;180(3):535–545. doi: 10.1111/j.1432-1033.1989.tb14679.x. [DOI] [PubMed] [Google Scholar]

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