Another first for the Apiaceae: evidence for mitochondrial DNA transfer into the plastid genome

Year 2014, Volume: 44 Issue: 2, 131 - 144, 11.08.2015

Stephen R. Downie1, Rhiannon M. Peery1 Robert K. Jansen2,3 Stephen R. Downie Rhiannon M Peery Robert K Jansen

Abstract

Another first for the Apiaceae: evidence for mitochondrial DNA transfer into the plastid genome

Abstract

The complete plastid genome (plastome) sequences of Anthriscus cerefolium, Crithmum maritimum, Hydrocotyle verticillata, Petroselinum crispum, and Tiedemannia filiformis subsp. greenmanii have recently been determined. With the exceptions of Crithmum and Petroselinum, which each demonstrate major shifts of their LSC-IRB (JLB) and LSC-IRA (JLA) junctions, all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structure, organization, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to Jsimilarity to any other region of their plastid genomes and BLAST searches of the Petroselinum insert resulted in multiple significant hits to angiosperm mitochondrial genome sequences. We highlight results of this recent work on the comparative analysis of whole plastid genomes from the Apiales, present the circular plastome gene map of Petroselinum crispum (parsley), review the literature indicating other instances of mitochondrial DNA transfer into Apiaceae plastomes as evidenced by complete mitochondrial DNA sequencing of Daucus carota, and describe our ongoing research on the elucidation of mechanisms creating the many large IR junction shifts characteristic of the family

Keywords

Intracellular DNA transfer, plastome, mitochondrial DNA, inverted repeat

References

• Bach, I. C., A. Olesen, and P. W. Simon. (2002). PCR-based markers to differentiate the mitochondrial genomes of petaloid and male fertile carrot (Daucus carota L.). Euphytica 127: 353–365.
• Bock, R. (2010). The give-and-take of DNA: horizontal gene transfer in plants. Trends in Plant Science 15: 11–22.
• Bock, R. and J. N. Timmis. (2008). Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30: 556–566.
• Constance, L. (1971). History and classification of Umbelliferae (Apiaceae). Pp. 1-8 In The Biology and Chemistry of the Umbelliferae. Edited by V. H. Heywood. Academic Press, New York.
• Cutler, H. G. (1992). An historical perspective of ancient poisons. Pp. 1-13 In Phytochemical Resources for Medicine and Agriculture. Edited by H. N. Nigg and D. Seigler. Plenum Press, New York.
• Downie, S. R. and J. D. Palmer. (1992). Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. Pp. 14–35 in Molecular Systematics of Plants, eds. P. S. Soltis, D. E. Soltis, and J. J. Doyle. New York: Chapman and Hall.
• Downie, S. R. and R. K. Jansen (2015). A comparative analysis of whole plastid genomes from the Apiales: expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions. Systematic Botany 40: 336-351.
• Downie, S. R., M. F. Watson, K. Spalik, and D. S. Katz-Downie. (2000). Molecular systematics of Old World Apioideae (Apiaceae): relationships among some members of tribe Peucedaneae sensu lato, the placement of several island-endemic species, and resolution within the apioid superclade. Canadian Journal of Botany 78: 506-528.
• Downie, S. R., G. M. Plunkett, M. F. Watson, K. Spalik, D. S. Katz-Downie, C. M. ValiejoRoman, E. I. Terentieva, A. V. Troitsky, B.-Y. Lee, J. Lahham, and A. El-Oqlah. (2001). Tribes and clades within Apiaceae subfamily Apioideae: the contribution of molecular data. Edinburgh Journal of Botany 58: 301–330.
• Goulding, S. E., R. G. Olmstead, C. W. Morden, and K. H. Wolfe. (1996). Ebb and flow of the chloroplast inverted repeat. Molecular and General Genetics 252: 195–206. Goremykin, V. V., F. Salamini, R. Velasco, and R. Viola. (2009). Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Molecular Biology and Evolution 26: 99–110.
• S. R. DOWNIE, R. M. PEERY, R. K. JANSEN 143 Heywood, V. H. (1971). The Biology and Chemistry of the Umbelliferae. Academic Press, New York. Iorizzo M., D. Grzebelus, D. Senalik, M. Szklarczyk, D. Spooner, and P. Simon. (2012)
• a. Against the traffic: the first evidence for mitochondrial DNA transfer into the plastid genome. Mobile Genetic Elements 2: 261–266.
• Iorizzo, M., D. Senalik, M. Szklarczyk, D. Grzebelus, D. Spooner, and P. Simon. (2012)b. De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biology 12: 61.
• Jansen R. K. and T. A. Ruhlman. (2012). Plastid genomes of seed plants. Pp. 103–126 in Genomics of chloroplasts and mitochondria, advances in photosynthesis and respiration, eds. R. Bock and V. Knoop. Dordrecht: Springer.
• Karimi, M. H., P. Ebadi, and Z. Amirghofran. (2012). Parsley and immunomodulation. Expert Review of Clinical Immunology 8: 295-297.
• Kim, K.-J. and H.-L. Lee. (2004). Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Research 11: 247–261.
• Kleine, T., U. G. Maier, and D. Leister. (2009). DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annual Review of Plant Biology 60: 115–138.
• Ku, C., W.-C. Chung, L.-L. Chen, and C.-H. Kuo. (2013). The complete plastid genome sequence of Madagascar periwinkle Catharanthus roseus (L.) G. Don: plastid genome evolution, molecular marker identification, and phylogenetic implications in asterids. PLoS ONE 8: e68518.
• Lohse, M., O. Drechsel, and R. Bock. (2007). OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics 52: 267–274.
• Morison, R. (1672). Plantarum Umbelliferarum Distributio Nova. Oxford. Palmer, J. D. (1985). Comparative organization of chloroplast genomes. Annual Review of Genetics 19: 325–354.
• Park S., T. A. Ruhlman, J. S. M. Sabir, M. H Z. Mutwakil, M.N. Baeshen, M. J. Sabir, N. A. Baeshen, and R. K. Jansen. (2014). Complete sequences of organelle genomes from the medicinal plant Rhazya stricta (Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids. BMC Genomics 15:405.
• Peery, R., J. V. Kuehl, J. L. Boore, and L. Raubeson. (2006). Comparisons of three Apiaceae chloroplast genomes—coriander, dill and fennel. Abstract, Botany 2006 Meeting.
• Peery, R., S. R. Downie, J. V. Kuehl, J. L. Boore, and L. Raubeson. (2007). Chloroplast genome evolution in Apiaceae. Abstract, Botany 2007 Meeting.
• Peery, R., S. R. Downie, R. K. Jansen, and L. A. Raubeson. (2011). Apiaceae organellar genomes. XVIII International Botanical Congress Abstract Book, p. 481.
• Another first for the Apiaceae: evidence for mitochondrial DNA transfer into 144 the plastid genome
• Plunkett, G. M. and S. R. Downie. (2000). Expansion and contraction of the chloroplast inverted repeat in Apiaceae subfamily Apioideae. Systematic Botany 25: 648-667. Reduron, J.-P. (1989). La représentation végétale au travers des Ombellifères. Bulletin de la Société Industrielle de Mulhouse.
• Richardson, A. O. and J. D. Palmer. (2007). Horizontal gene transfer in plants. Journal of Experimental Botany 58: 1–9.
• Rokas, A. and P. W. H. Holland. (2000). Rare genomic changes as a tool for phylogenetics. Trends in Ecology and Evolution 15: 454-459.
• Ruberto, G., M. T. Baratta, S. G. Deans, and H. J. D. Dorman. (2000). Antioxidant and antimicrobial activity of Foeniculum vulgare and Crithmum maritimum essential oils. Planta Medica 66: 687-693.
• Ruhlman T. A. and R. K. Jansen. (2014). The plastid genomes of flowering plants. Pp. 3–38 in Chloroplast Biotechnology: Methods and Protocols, ed. P. Maliga. New York: Springer.
• Ruhlman, T., S.-B. Lee, R. K. Jansen, J. B. Hostetler, L. J. Tallon, C. D. Town, and H. Daniell. (2006). Complete plastid genome sequence of Daucus carota: implications for biotechnology and phylogeny of angiosperms. BMC Genomics 7: 222. Simon, P. W., R. E. Freeman, J. V. Vieira, L. S. Boiteux, M. Briard, T. Nothnagel, B.
• Michalik, and Y.-S. Kwon. (2008). Carrot. Pp. 327–357 in Vegetables II. Handbook of Plant Breeding, Vol. 2. New York: Springer.
• Smith, D. R. (2011). Extending the limited transfer window hypothesis to inter-organelle DNA migration. Genome Biology and Evolution 3: 743–748. Smith, D. R. (2014). Mitochondrion-to-plastid DNA transfer: it happens. New Phytologist 202: 736-738.
• Straub, S. C. K., R. C. Cronn, C. Edwards, M. Fishbein, and A. Liston. (2013). Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biology and Evolution 5: 1872–1885.
• Watson, M. F., G. M. Plunkett, S. R. Downie, and P. P. Lowry II. (2001). Introduction. Evolution, biogeography and systematics of the Apiales (Araliaceae and Apiaceae). Edinburgh Journal of Botany 58: 179-181.
• Wicke, S., G. M. Schneeweiss, C. W. dePamphilis, K. F. Müller, and D. Quandt. (2011). The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Molecular Biology 76: 273–297.