Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus
Open accessAbstract
We used DNA sequencing and gel blot surveys to assess the integrity of the chloroplast gene infA, which codes for translation initiation factor 1, in >300 diverse angiosperms. Whereas most angiosperms appear to contain an intact chloroplast infA gene, the gene has repeatedly become defunct in approximately 24 separate lineages of angiosperms, including almost all rosid species. In four species in which chloroplast infA is defunct, transferred and expressed copies of the gene were found in the nucleus, complete with putative chloroplast transit peptide sequences. The transit peptide sequences of the nuclear infA genes from soybean and Arabidopsis were shown to be functional by their ability to target green fluorescent protein to chloroplasts in vivo. Phylogenetic analysis of infA sequences and assessment of transit peptide homology indicate that the four nuclear infA genes are probably derived from four independent gene transfers from chloroplast to nuclear DNA during angiosperm evolution. Considering this and the many separate losses of infA from chloroplast DNA, the gene has probably been transferred many more times, making infA by far the most mobile chloroplast gene known in plants.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many gene transfers to the nucleus have occurred during plastid evolution.
“Previous work has shown that many gene transfers to the nucleus have occurred during plastid evolution (19, 20)”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Martin, W., & Schnarrenberger, C. (1997) · Current Genetics · doi:10.1007/s002940050241 · Cited by 254 · see citing works
Flagged first, then by citations
Research works printed but not linked: 12
- Downie, S.R., and Palmer, J.D. (1992). Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In Molecular Systematics of Plants, P.S. Soltis, D.E. Soltis, and J.J. Doyle, eds (New York: Chapman and Hall), pp. 14-35.
- Gyllensten, U. (1989). Direct sequencing of in vitro amplified DNA. In PCR Technology, H.A. Erlich, ed (New York: Stockton Press), pp. 45-60.
- Herrmann, R.G. (1997). Eukaryotism, towards a new interpretation. In Eukaryotism and Symbiosis, H.E.A. Schenk, R.G. Herrmann, K.W. Jeon, N.E. Muller, and W. Schwemmler, eds (Vienna: Springer), pp. 73-118.
- Kubo, N., Harada, K., Hirai, A., and Kadowaki, K. (1999). A single nuclear transcript encoding mitochondrial RPS14 and SDHB of rice is processed by alternative splicing: Common use of the same mitochondrial targeting signal for different proteins. Proc. Natl. Acad. Sci. USA 96, 9207-9211.
- Laroche, J., Li, P., Maggia, L., and Bousquet, J. (1997). Molecular evolution of angiosperm mitochondrial introns and exons. Proc. Natl. Acad. Sci. USA 94, 5722-5727.
- Makalowski, W., and Boguski, M.S. (1998). Evolutionary parame- ters of the transcribed mammalian genome: An analysis of 2,820 orthologous rodent and human sequences. Proc. Natl. Acad. Sci. USA 95, 9407-9412.
- Palmer, J.D., and Delwiche, C.F. (1998). The origin and evolution of plastids and their genomes. In Molecular Systematics of Plants. II. DNA Sequencing, D.E. Soltis, P.S. Soltis, and J.J. Doyle, eds (Boston: Kluwer Academic Publishing), pp. 375-409.
- Palmer, J.D., Adams, K.L., Cho, Y., Parkinson, C.L., Qiu, Y.L., and Song, K. (2000). Dynamic evolution of plant mitochondrial genomes: Mobile genes and introns and highly variable mutation rates. Proc. Natl. Acad. Sci. USA 97, 6960-6966.
- Pearson, W.R., and Lipman, D.J. (1988). Improved tools for biolog- ical sequence comparison. Proc. Natl. Acad. Sci. USA 85, 2444- 2448.
- Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., and Sugiura, M. (1994). Loss of all ndh genes as deter- mined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc. Natl. Acad. Sci. USA 91, 9794-9798.
- Wolfe, K.H., Li, W.H., and Sharp, P.M. (1987). Rates of nucle- otide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84, 9054-9058.
- Wolfe, K.H., Morden, C.W., and Palmer, J.D. (1992a). Function and evolution of a minimal plastid genome from a nonphoto- synthetic parasitic plant. Proc. Natl. Acad. Sci. USA 89, 10648-10652.
Cited by
Sorted by citations
Horizontal gene transfer in eukaryotic evolution
Keeling, P. J., & Palmer, J. D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2386 · Cited by 1,355 · see citing works
Self-citationMartin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M., & Penny, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182432999 · Cited by 1,178 · see citing works
- Authors
- Millen, R. S., Olmstead, R. G., Adams, K. L., Palmer, J. D., Lao, N. T., Heggie, L., Kavanagh, T. A., Hibberd, J. M., Gray, J. C., Morden, C. W., Calie, P. J., Jermiin, L. S., & Wolfe, K. H.
- Affiliations
- University of Colorado Boulder (US)
- University of Washington (US)
- Indiana University Bloomington (US)
- Trinity College Dublin (IE)
- University of Cambridge (GB)
- University of Hawaiʻi at Mānoa (US)
- Eastern Kentucky University (US)
- The University of Sydney (AU)
- ORCID
- Venue
- The Plant Cell
- Publisher
- Oxford University Press (OUP)
- Published
- 2001-03
- Volume
- 13
- Issue
- 3
- Pages
- 645-658
- ISSN
- 1040-4651 (ISSN-L)
- 1532-298X
- PMC
- PMC135507
- OpenAlex
- W2110188639
- Cited by
- 503
- References
- 2
- Citations by year
- 2026: 16 · 2025: 41 · 2024: 49 · 2023: 39 · 2022: 45 · 2021: 38 · 2020: 31 · 2019: 22 · 2018: 25 · 2017: 21 · 2016: 22 · 2015: 12 · 2014: 16 · 2013: 13 · 2012: 9
- FWCI
- 3.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Plant Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (GM-35087, R01GM035087)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
- Keywords
- chloroplast DNA, flowering plants, gene loss, nuclear translocation, chloroplast transit peptide, soybean, Arabidopsis, gene mobility
- MeSH terms
- Amino Acid Sequence, Cell Nucleus, DNA Transposable Elements, Indicators and Reagents, Introns, Luminescent Proteins, Molecular Sequence Data, Nuclear Proteins, Phylogeny, Plant Proteins, Glycine max, Transcription Factors, DNA Probes, Arabidopsis, Sequence Homology, Amino Acid, Sequence Analysis, DNA, Solanum lycopersicum, DNA, Chloroplast, Evolution, Molecular, Artificial Gene Fusion, Magnoliopsida, Rosales, Sequence Analysis, Protein, Green Fluorescent Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
