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Plastid DNA insertions in plant nuclear genomes: the sites, abundance and ages, and a predicted promoter analysis

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Abstract

The transfer of plastid DNA sequences into plant nuclear genomes plays an important role in the genomic evolution of plants. The abundance of nuclear-localized plastid DNA (nupDNA) correlates positively with nuclear genome size, but the genetic content of nupDNA remains unknown. In this mini review, we analyzed the number of nuclear-localized plastid gene fragments in known plant genomic data. Our analysis suggests that nupDNAs are abundant in plant nuclear genomes and can include multiple complete copies of protein-coding plastid genes. Mutated nuclear copies of plastid genes contained synonymous and nonsynonymous substitutions. We estimated the age of the nupDNAs based on the time when each integration occurred, which was calculated by comparing the nucleotide substitution rates of the nupDNAs and their respective plastid genes. These data suggest that there are two distinct age distribution patterns for nupDNAs in plants, and Oryza sativa and Zea mays were found to contain a very high proportion of young nupDNAs. Expressed sequence tags and predicted promoters of nupDNAs were identified, revealing that certain nuclear-localized plastid genes may be functional and that some have undergone positive natural selection pressure.

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References

  • Adams KL, Song K, Roessler PG et al (1999) Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc Natl Acad Sci U S A 96:13863–13868

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Adams KL, Qiu YL, Stoutemyer M et al (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci U S A 99:9905–9912

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796

    Article  Google Scholar 

  • Argout X, Salse J, Aury JM et al (2011) The genome of Theobroma cacao. Nat Genet 43:101–108

    Article  CAS  PubMed  Google Scholar 

  • Ayliffe MA, Scott NS, Timmis JN (1998) Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants. Mol Biol Evol 15:738–745

    Article  CAS  PubMed  Google Scholar 

  • Baldauf SL, Palmer JD (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344:262–265

    Article  CAS  PubMed  Google Scholar 

  • Banks JA, Nishiyama T, Hasebe M et al (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bausher MG, Singh ND, Lee SB et al (2006) The complete chloroplast genome sequence of Citrus sinensis (L) Osbeck var’Ridge Pineapple’: organization and phylogenetic relationships to other angiosperms. BMC Plant Biol 6:21

    Article  PubMed Central  PubMed  Google Scholar 

  • Bensasson D, Zhang DX, Hartl DL et al (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321

    Article  PubMed  Google Scholar 

  • Bortiri E, Coleman-Derr D, Lazo GR et al (2008) The complete chloroplast genome sequence of Brachypodium distachyon: sequence comparison and phylogenetic analysis of eight grass plastomes. BMC Res Notes 1:61

    Article  PubMed Central  PubMed  Google Scholar 

  • Daniell H, Wurdack KJ, Kanagaraj A et al (2008) The complete nucleotide sequence of the cassava (Manihot esculenta) chloroplast genome and the evolution of atpF in Malpighiales: RNA editing and multiple losses of a group II intron. Theor Appl Genet 116:723–737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gantt JS, Baldauf SL, Calie PJ et al (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10:3073

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gargano D, Vezzi A, Scotti N et al (2005) The complete nucleotide sequence of potato (Solanum tuberosum cv.Desiree) chloroplast DNA. In: Abstracts Second Solanaceae Genome workshop p. 107

  • Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo X, Castillo-Ramírez S, González V et al (2007) Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genomics 8:228

    Article  PubMed Central  PubMed  Google Scholar 

  • Guo X, Ruan S, Hu W et al (2008) Chloroplast DNA insertions into the nuclear genome of rice: the genes, sites and ages of insertion involved. Funct Integr Genom 8:101–108

    Article  CAS  Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R 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  CAS  PubMed  Google Scholar 

  • Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76

    Article  CAS  PubMed  Google Scholar 

  • Huang CY, Ayliffe MA, Timmis JN (2004) Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco. Proc Natl Acad Sci U S A 101:9710–9715

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang S, Li R, Zhang Z et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Jansen RK, Kaittanis C, Saski C et al (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32

    Article  PubMed Central  PubMed  Google Scholar 

  • Kahlau S, Aspinall S, Gray JC et al (2006) Sequence of the tomato chloroplast DNA and evolutionary comparison of solanaceous plastid genomes. J Mol Evol 63:194–207

    Article  CAS  PubMed  Google Scholar 

  • Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138

    Article  CAS  PubMed  Google Scholar 

  • Maier RM, Neckermann K, Igloi GL et al (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628

    Article  CAS  PubMed  Google Scholar 

  • Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci U S A 100:8612–8614

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin W, Stoebe B, Goremykin V et al (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165

    Article  CAS  PubMed  Google Scholar 

  • Martin W, Rujan T, Richly E et al (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99:12246–12251

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsuo M, Ito Y, Yamauchi R et al (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast–nuclear DNA flux. Plant Cell 17:665–675

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maul JE, Lilly JW, Cui L et al (2002) The Chlamydomonas reinhardtii Plastid Chromosome Islands of Genes in a Sea of Repeats. Plant Cell 14:2659–2679

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Millen RS, Olmstead RG, Adams KL et al (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13:645–658

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ming R, Hou S, Feng Y et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nishiyama T, Fujita T, Shin T et al (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci U S A 100:8007–8012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noutsos C, Richly E, Leister D (2005) Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants. Genome Res 15:616–628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paiva JAP, Prat E, Vautrin S et al (2011) Advancing Eucalyptus genomics: identification and sequencing of lignin biosynthesis genes from deep-coverage BAC libraries. BMC Genomics 12:137

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Pląder W, Yukawa Y, Sugiura M et al (2007) The complete structure of the cucumber (Cucumis sativus L.) chloroplast genome: its composition and comparative analysis. Cell Mol Biol Lett 12:584–594

    PubMed  Google Scholar 

  • Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

  • Prochnik S, Marri PR, Desany B et al (2012) The cassava genome: current progress, future directions. Trop Plant Biol 5:88–94

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rujan T, Martin W (2001) How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends Genet 17:113–120

    Article  CAS  PubMed  Google Scholar 

  • Saski C, Lee SB, Daniell H et al (2005) Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol 59:309–322

    Article  CAS  PubMed  Google Scholar 

  • Saski C, Lee SB, Fjellheim S et al (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor Appl Genet 115:571–590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T et al (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6:283–290

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sheppard AE, Timmis JN (2009) Instability of plastid DNA in the nuclear genome. PLoS Genet 5:e1000323

    Article  PubMed Central  PubMed  Google Scholar 

  • Shrager J, Hauser C, Chang CW et al (2003) Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information. Plant Physiol 131:401–408

    Article  PubMed Central  PubMed  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN et al (2010) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116

    Article  PubMed Central  PubMed  Google Scholar 

  • Smith DR (2009) Unparalleled GC content in the plastid DNA of Selaginella. Plant Mol Biol 71:627–639

    Article  CAS  PubMed  Google Scholar 

  • Smith DR, Crosby K, Lee RW (2011) Plastids and gene transfer: correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genome Biol Evol 3:365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sugiura C, Kobayashi Y, Aoki S et al (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY et al (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Vogel JP, Garvin DF, Mockler TC et al (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  CAS  Google Scholar 

  • Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12:885–893

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu Q, Chen LL, Ruan X et al (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Furihata HY, Kawabe A (2013) Patterns of genomic integration of nuclear chloroplast DNA fragments in plant species. DNA Res 21:127–140

    Article  PubMed Central  PubMed  Google Scholar 

  • Young HA, Lanzatella CL, Sarath G et al (2011a) Chloroplast genome variation in upland and lowland switchgrass. PLoS One 6:e23980

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Young ND, Debellé F, Oldroyd GED et al (2011b) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yuan Q, Hill J, Hsiao J et al (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 Genet Genomics 267:713–720

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Trans-Century Training Program’s Foundation for the Talents by Heilongjiang Provincial Education Department (1251–NCET—004) and the Innovation Team Project by Heilongjiang Provincial Education Department to A. X. Wang, the Returned Oversea Scholar Foundation by Heilongjiang Provincial Education Department (1252HQ011), and the National Science Foundation of China (31301780) to X. L. Chen.

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Authors and Affiliations

  1. Heilongjiang Provincial Key University Laboratory of Agricultural Functional Genes, College of Life Science, Northeast Agricultural University, Harbin, 150030, China

    Hongyu Chen, Zhenzhu Zhang, Chao Gong & Aoxue Wang

  2. Institute of Industrial Crops, Heilongjiang Academy of Agricultural Sciences, Harbin, 150086, China

    Ying Yu

  3. College of Horticulture, Northeast Agricultural University, Harbin, 150030, China

    Xiuling Chen & Jingfu Li

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  1. Hongyu Chen
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  2. Ying Yu
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  3. Xiuling Chen
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  4. Zhenzhu Zhang
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  5. Chao Gong
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  7. Aoxue Wang
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Correspondence to Aoxue Wang.

Supplementary material

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Online Resource 1

Homologs of plastid genes in plant nuclear DNA. (PDF 728 kb)

Online Resource 2

Homologs of intact coding DNA sequences (CDSs) of plastid genes in plant nuclear DNA. (PDF 257 kb)

Online Resource 3

Sequence alignment of predicted plant gene promoter regions. (PDF 384 kb)

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Chen, H., Yu, Y., Chen, X. et al. Plastid DNA insertions in plant nuclear genomes: the sites, abundance and ages, and a predicted promoter analysis. Funct Integr Genomics 15, 131–139 (2015). https://doi.org/10.1007/s10142-014-0422-z

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