Skip to main content
Log in

Chloroplast DNA insertions into the nuclear genome of rice: the genes, sites and ages of insertion involved

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Rice (Oryza sativa) is one of three predominant grain crops, and its nuclear and organelle genomes have been sequenced. Following genome analysis revealed many exchanges of DNA sequences between the nuclear and organelle genomes. In this study, a total of 45 chloroplast DNA insertions more than 2 kb in length were detected in rice nuclear genome. A homologous recombination mechanism is expected for those chloroplast insertions with high similarity between their flanking sequences. Only five chloroplast insertions with high sequence similarity between two flanking sequences from an insertion were found in the 45 insertions, suggesting that rice might follow the non-homologous end-joining (NHEJ) repair of double-stranded breaks mechanism, which is suggested to be common to all eukaryotes. Our studies indicate that the most chloroplast insertions occurred at a nuclear region characterized by a sharp change of repetitive sequence density. One potential explanation is that regions such as this might be susceptible target sites or “hotspots” of DNA damage. Our results also suggest that the insertion of retrotransposon elements or non-chloroplast DNA into chloroplast DNA insertions may contribute significantly to their fragmentation process. Moreover, based on chloroplast insertions in nuclear genomes of two subspecies (indica and japonica) of cultivated rice, our results strongly suggest that they diverged during 0.06–0.22 million years ago.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Delcher AL, Phillippy A, Carlton J, Salzberg SL (2002) Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30:2478–2483

    Article  PubMed  Google Scholar 

  • Feng Q et al (2002) Sequence and analysis of rice chromosome 4. Nature 420:316–320

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28

    Article  CAS  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcl. Proc Natl Acad Sci USA 93:10274–10279

    Article  PubMed  CAS  Google Scholar 

  • Ge S, Sang T, Lu B, Hong D (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci USA 96:14400–14405

    Article  PubMed  CAS  Google Scholar 

  • Goff SA et al (2002) A draft sequence of the rice genome (Oryza sativa L ssp japonica). Science 296:92–114

    Article  PubMed  CAS  Google Scholar 

  • Hannenhalli S, Pevzner PA (1995) Transforming men into mice (polynomial algorithm for genomic distance problem). Proceedings of the 36th Annual IEEE Symposium on Foundations of Computer Science. IEEE, Milwaukee, Wisconsin, pp 581–592

  • Hiratsuka J et al (1989) 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 217:185–194

    Article  PubMed  CAS  Google Scholar 

  • Huang C et al (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76

    Article  PubMed  CAS  Google Scholar 

  • Huang CY, Grunheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138:1723–1733

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  PubMed  CAS  Google Scholar 

  • Leister D (2005) Origin, evolution and genetic effects of nuclear insertions of organelle DNA. Trends Genet 21:655–663

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410

    Article  PubMed  CAS  Google Scholar 

  • Mishmar D et al (2004) Mitochondrial DNA-like sequences in the nucleus (NUMTs): insights into our African origins and the mechanism of foreign DNA integration. Hum Mutat 23:125–133

    Article  PubMed  CAS  Google Scholar 

  • Muse SV (2000) Examining rates and patterns of nucleotide substitution in plants. Plant Mol Biol 42:25–43

    Article  PubMed  CAS  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Hubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Gen Genomics 268:434–445

    Article  CAS  Google Scholar 

  • Pevzner P, Tesler G (2003) Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Res 13:37–45

    Article  PubMed  CAS  Google Scholar 

  • Ricchetti M et al (1999) Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402:96–100

    Article  PubMed  CAS  Google Scholar 

  • Sall T, Jakobsson M, Lind-hallden C, Hallden C (2003) Chloroplast DNA indicates a single origin of the allotetraploid Arabidopsis suecica. J Evol Biol 16:1019–1029

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316

    Article  PubMed  CAS  Google Scholar 

  • Shahmuradov IA, Akbarova YY, Solovyev VV, Aliye JA (2003) Abundance of plastid DNA insertions in nuclear genomes of rice and Arabidopsis. Plant Mol Biol 52:923–934

    Article  PubMed  CAS  Google Scholar 

  • Stegemann S et al (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100:8828–8833

    Article  PubMed  CAS  Google Scholar 

  • Tang J et al (2004) A comparison of rice chloroplast genomes. Plant Physiol 135:412–420

    Article  PubMed  CAS  Google Scholar 

  • The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity, and evolution of rice chromosome 10. Science 300:1566–1569

    Article  Google Scholar 

  • Tian X, Zheng J, Hu S, Yu J (2006) The rice mitochondrial genomes and their variations. Plant Physiol 140:401–410

    Article  PubMed  CAS  Google Scholar 

  • Vaughan DA, Morishima H, Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6:139–146

    Article  PubMed  CAS  Google Scholar 

  • Vitte C, Ishii T, Lamy F, Brar D, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol Gen Genomics 272:504–511

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (1999) Phylogenetic Analysis by Maximum Likelihood (PAML) (University College, London, UK), http://abacusgeneuclacuk/software/pamlhtml

  • Yu X, Gabriel A (1999) Patching broken chromosomes with extranuclear cellular DNA. Mol Cell 4:873–881

    Article  PubMed  CAS  Google Scholar 

  • Yu J et al (2002) A draft sequence of the rice genome (Oryza sativa L ssp indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Yu J et al (2005) The genome of Oryza sativa: a history of duplication. PloS Biol 3(2):e38

    Article  PubMed  Google Scholar 

  • Yuan Q, Hill J, Hsiao J, Moffat K, Ouyang S, Cheng Z, Jiang J, Buell CR (2002) Genome sequencing of a 239-kb region of rice chromosome 10 L reveals a high frequency of gene duplication and a large chloroplast DNA insertion. Mol Gen Genomics 267:713–720

    Article  CAS  Google Scholar 

  • Zhu Q, Ge S (2005) Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 167:249–265

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Jianzhi Zhang (University of Michigan) for his critical reading of the manuscript. This work was supported by National Natural Science Foundation of China (30270810) and National High Technology Research and Development Program of China (2006AA10A102).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Longjiang Fan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 142 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, X., Ruan, S., Hu, W. et al. Chloroplast DNA insertions into the nuclear genome of rice: the genes, sites and ages of insertion involved. Funct Integr Genomics 8, 101–108 (2008). https://doi.org/10.1007/s10142-007-0067-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-007-0067-2

Keywords

Navigation