• Hoekstra, R. F. Evolutionary origin and consequences of uniparental mitochondrial inheritance. Hum. Reprod. 15, 102–111 (2000).

    Article 

    Google Scholar
     

  • Greiner, S., Sobanski, J. & Bock, R. Why are most organelle genomes transmitted maternally? BioEssays 37, 80–94 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Birky, C. W. Jr., Maruyama, T. & Fuerst, P. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513–527 (1983).

    Article 

    Google Scholar
     

  • Birky, C. W. Jr. Uniparental inheritance of organelle genes. Curr. Biol. 18, R692–R695 (2008).

    Article 
    CAS 

    Google Scholar
     

  • Havird, J. C., Hall, M. D. & Dowling, D. K. The evolution of sex: a new hypothesis based on mitochondrial mutational erosion. BioEssays 37, 951–958 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Muller, H. J. The relation of recombination to mutational advance. Mutat. Res. 1, 2–9 (1964).

    Article 

    Google Scholar
     

  • Blanchard, J. L. & Lynch, M. Organellar genes – why do they end up in the nucleus? Trends Genet. 16, 315–320 (2000).

    Article 
    CAS 

    Google Scholar
     

  • Khakhlova, O. & Bock, R. Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J. 46, 85–94 (2006).

    Article 
    CAS 

    Google Scholar
     

  • Smith, J. M. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).

    Article 
    CAS 

    Google Scholar
     

  • Wolfe, K. H., Li, W.-H. & Sharp, P. M. Rates of nucleotide substitutions vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl Acad. Sci. USA 84, 9054–9058 (1987).

    Article 
    CAS 

    Google Scholar
     

  • Drouin, G., Daoud, H. & Xia, J. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol. Phylogenet. Evol. 49, 827–831 (2008).

    Article 
    CAS 

    Google Scholar
     

  • Wu, Z., Waneka, G., Broz, A. K., King, C. R. & Sloan, D. B. MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes. Proc. Natl Acad. Sci. USA 117, 16448–16455 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Cho, Y., Mower, J. P., Qiu, Y.-L. & Palmer, J. D. Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc. Natl Acad. Sci. USA 101, 17741–17746 (2004).

    Article 
    CAS 

    Google Scholar
     

  • Guisinger, M. M., Kuehl, J. V., Boore, J. L. & Jansen, R. K. Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc. Natl Acad. Sci. USA 105, 18424–18429 (2008).

    Article 
    CAS 

    Google Scholar
     

  • Parkinson, C. L. et al. Multiple major increases and decreases in mitochondrial substitution rates in the plant family Geraniaceae. BMC Evol. Biol. 5, 73 (2005).

    Article 

    Google Scholar
     

  • Sloan, D. B. et al. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10, e1001241 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Medgyesy, P., Fejes, E. & Maliga, P. Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc. Natl Acad. Sci. USA 82, 6960–6964 (1985).

    Article 
    CAS 

    Google Scholar
     

  • Thanh, N. D. & Medgyesy, P. Limited chloroplast gene transfer via recombination overcomes plastome-genome incompatibility between Nicotiana tabacum and Solanum tuberosum. Plant Mol. Biol. 12, 87–93 (1989).

    Article 
    CAS 

    Google Scholar
     

  • Baldev, A. et al. Recombination between chloroplast genomes of Trachystoma ballii and Brassica juncea following protoplast fusion. Mol. Gen. Genet. 260, 357–361 (1998).

    Article 
    CAS 

    Google Scholar
     

  • Barnard-Kubow, K. B., McCoy, M. A. & Galloway, L. F. Biparental chloroplast inheritance leads to rescue from cytonuclear incompatibility. New Phytol. 213, 1466–1476 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Tsitrone, A., Kirkpatrick, M. & Levin, D. A. A model for chloroplast capture. Evolution 57, 1776–1782 (2003).


    Google Scholar
     

  • Acosta, M. C. & Premoli, A. C. Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol. Phylogenet. Evol. 54, 235–242 (2010).

    Article 

    Google Scholar
     

  • Roux, F. et al. Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field. Proc. Natl Acad. Sci. USA 113, 3687–3692 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Bock, D. G., Andrew, R. L. & Rieseberg, L. H. On the adaptive value of cytoplasmic genomes in plants. Mol. Ecol. 23, 4899–4911 (2014).

    Article 

    Google Scholar
     

  • Zouros, E., Oberhauser Ball, A., Saavedra, C. & Freeman, K. R. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl Acad. Sci. USA 91, 7463–7467 (1994).

    Article 
    CAS 

    Google Scholar
     

  • Shi, L., Zhu, T., Mogensen, H. L. & Smith, S. E. Paternal plastid inheritance in alfalfa: plastid nucleoid number within generative cells correlates poorly with plastid number and male plastid transmission strength. Curr. Genet. 19, 399–401 (1991).

    Article 

    Google Scholar
     

  • Metzlaff, M., Börner, T. & Hagemann, R. Variations of chloroplast DNAs in the genus Pelargonium and their biparental inheritance. Theor. Appl. Genet. 60, 37–41 (1981).

    Article 
    CAS 

    Google Scholar
     

  • Szmidt, A. E., Alden, T. & Hällgren, J.-E. Paternal inheritance of chloroplast DNA in Larix. Plant Mol. Biol. 9, 59–64 (1987).

    Article 
    CAS 

    Google Scholar
     

  • Mogensen, H. L. The hows and whys of cytoplasmic inheritance in seed plants. Am. J. Bot. 83, 383–404 (1996).

    Article 

    Google Scholar
     

  • Matsushima, R., Hu, Y., Toyoda, K., Sakamoto, S. & Sakamoto, W. The model plant Medicago truncatula exhibits biparental plastid inheritance. Plant Cell Physiol. 49, 81–91 (2008).

    Article 
    CAS 

    Google Scholar
     

  • Ruf, S., Karcher, D. & Bock, R. Determining the transgene containment level provided by chloroplast transformation. Proc. Natl Acad. Sci. USA 104, 6998–7002 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Azhagiri, A. K. & Maliga, P. Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants. Plant J. 52, 817–823 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Hagemann, R. & Schröder, M.-B. The cytological basis of the plastid inheritance in angiosperms. Protoplasma 152, 57–64 (1989).

    Article 

    Google Scholar
     

  • Zhang, Q., Liu, Y. & Sodmergen, S. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 44, 941–951 (2003).

    Article 
    CAS 

    Google Scholar
     

  • Zhou, Q. et al. Mitochondrial endonuclease G mediates breakdown of paternal mitochondria upon fertilization. Science 353, 394–399 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Tilney-Bassett, R. A. E. Nuclear control of chloroplast inheritance in higher plants. J. Heredity 85, 347–354 (1994).

    Article 

    Google Scholar
     

  • Svab, Z. & Maliga, P. Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc. Natl Acad. Sci. USA 104, 7003–7008 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Corriveau, J. L., Goff, L. J. & Coleman, A. W. Plastid DNA is not detectable in the male gametes and pollen tubes of an angiosperm (Antirrhinum majus) that is maternal for plastid inheritance. Curr. Genet. 17, 439–444 (1990).

    Article 
    CAS 

    Google Scholar
     

  • Svab, Z. & Maliga, P. Mutation proximal to the tRNA binding region of the Nicotiana plastid 16S rRNA confers resistance to spectinomycin. Mol. Gen. Genet. 228, 316–319 (1991).

    Article 
    CAS 

    Google Scholar
     

  • Ahlert, D., Ruf, S. & Bock, R. Plastid protein synthesis is required for plant development in tobacco. Proc. Natl Acad. Sci. USA 100, 15730–15735 (2003).

    Article 
    CAS 

    Google Scholar
     

  • Matsushima, R. et al. A conserved, Mg2+-dependent exonuclease degrades organelle DNA during Arabidopsis pollen development. Plant Cell 23, 1608–1624 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Takami, T. et al. Organelle DNA degradation contributes to the efficient use of phosphate in seed plants. Nat. Plants 4, 1044–1055 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Greiner, S. & Bock, R. Tuning a ménage à trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35, 354–365 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Zupok, A. et al. A photosynthesis operon in the chloroplast genome drives speciation in evening primroses. Plant Cell 33, 2583–2601 (2021).

    Article 

    Google Scholar
     

  • De Storme, N., Copenhaver, G. P. & Geelen, D. Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol. 160, 1808–1826 (2012).

    Article 

    Google Scholar
     

  • Birky, C. W. Jr. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc. Natl Acad. Sci. USA 92, 11331–11338 (1995).

    Article 
    CAS 

    Google Scholar
     

  • Wada, M. & Suetsugu, N. Plant organelle positioning. Curr. Opin. Plant Biol. 7, 626–631 (2004).

    Article 
    CAS 

    Google Scholar
     

  • Wada, M. & Kong, S.-G. Actin-mediated movement of chloroplasts. J. Cell Sci. 131, 210310 (2018).

    Article 

    Google Scholar
     

  • Wang, X., Sheng, X., Tian, X., Zhang, Y. & Li, Y. Organelle movement and apical accumulation of secretory vesicles in pollen tubes of Arabidopsis thaliana depend on class XI myosins. Plant J. 104, 1685–1697 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Moison, M. et al. Cytoplasmic phylogeny and evidence of cyto-nuclear co-adaptation in Arabidopsis thaliana. Plant J. 63, 728–738 (2010).

    Article 
    CAS 

    Google Scholar
     

  • Boussardon, C. et al. Novel cytonuclear combinations modify Arabidopsis thaliana seed physiology and vigor. Front. Plant Sci. 10, 32 (2019).

    Article 

    Google Scholar
     

  • Jaramillo-Correa, J. P. & Bousquet, J. Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171, 1951–1962 (2005).

    Article 
    CAS 

    Google Scholar
     

  • Apitz, J., Weihe, A., Pohlheim, F. & Börner, T. Biparental inheritance of organelles in Pelargonium: evidence for intergenomic recombination of mitochondrial DNA. Planta 237, 509–515 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Alwadani, K. G., Janes, J. K. & Andrew, R. L. Chloroplast genome analysis of box-ironbark Eucalyptus. Mol. Phylogenet. Evol. 136, 76–86 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Menczel, L., Morgan, A., Brown, S. & Maliga, P. Fusion-mediated combination of Ogura-type cytoplasmic male sterility with Brassica napus plastids using X-irradiated CMS protoplasts. Plant Cell Rep. 6, 98–101 (1987).

    Article 
    CAS 

    Google Scholar
     

  • Chung, S.-M., Gordon, V. S. & Staub, J. E. Sequencing cucumber (Cucumis sativus L.) chloroplast genomes identifies differences between chilling-tolerant and -susceptible cucumber lines. Genome 50, 215–225 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Hertle, A. P., Haberl, B. & Bock, R. Horizontal genome transfer by cell-to-cell travel of whole organelles. Sci. Adv. 7, eabd8215 (2021).

  • Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue culture. Physiol. Plant. 15, 473–497 (1962).

    Article 
    CAS 

    Google Scholar
     

  • Bock, R. Transgenic plastids in basic research and plant biotechnology. J. Mol. Biol. 312, 425–438 (2001).

    Article 
    CAS 

    Google Scholar
     

  • Bock, R. Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu. Rev. Plant Biol. 66, 211–241 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Edwards, K. D. et al. A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genomics 18, 448 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Concordet, J.-P. & Haeussler, M. CRISPOR: intuitive guide selection for CRISPR/Cas9 genome editing experiments and screens. Nucleic Acids Res. 46, W242–W245 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Ruf, S. et al. High-efficiency generation of fertile transplastomic Arabidopsis plants. Nat. Plants 5, 282–289 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Coutu, C. et al. pORE: a modular binary vector series suited for both monocot and dicot plant transformation. Transgenic Res. 16, 771–781 (2007).

    Article 
    CAS 

    Google Scholar
     

  • Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 343, 343–345 (2009).

    Article 

    Google Scholar
     

  • Lampropoulos, A. et al. GreenGate – a novel, versatile, and efficient cloning system for plant transgenesis. PLoS ONE 8, e83043 (2013).

    Article 

    Google Scholar
     

  • Doyle, J. J. & Doyle, J. L. Isolation of plant DNA from fresh tissue. Focus 12, 13–15 (1990).


    Google Scholar
     

  • Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408 (2001).

    Article 
    CAS 

    Google Scholar
     

  • Dunn, P. K. & Smyth, G. K. in Generalized Linear Models With Examples in R (eds. DeVeaux, R., Fienberg, S.E & Olkin, I.) Ch. 9–10 (Springer, 2018).

  • Bozdogan, H. Model selection and Akaike’s Information Criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345–370 (1987).

    Article 

    Google Scholar
     

  • Burnham, K. P. & Anderson, D. R. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Meth. Res. 33, 261–304 (2004).

    Article 

    Google Scholar
     

  • Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S. 4th edn (Springer, 2002).

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