The complete plastid genome sequence and the photosynthetic activity of the putative mycoheterotrophic orchid Limodorum abortivum

In: Israel Journal of Plant Sciences

The sparsely distributed Limodorum abortivum is a European-Mediterranean orchid species, which grows on decomposing plant material. Although some chlorophyll-pigmentation is observed in the degenerated scales-shaped leaf and stems regions of the plant, its photosynthetic capacity is assumed to be insufficient to support the full energy requirements of an adult plant. In Israel, L. abortivum shows a patchy distribution patterns in the Galilee, Golan, Carmel and Judean regions. To gain more insights into the physiology and photosynthetic activity of L. abortivum, we analyzed the organellar morphologies, photosynthetic activities the chloroplast-DNA sequence by Illumina-HTS. Microscopic analyses indicated to the presence of mature chloroplasts with well-organized grana-thylakoids in the leaves and stems of L. abortivum. However, the numbers of chloroplasts per cell and the grana ultrastructure density within the organelles were notably lower than those of model plant species and fully photosynthetically-active orchids. The cpDNA of L. abortivum (154,954 bp) encodes 60 proteins, 34 tRNAs and 4 rRNAs. The coding-regions of 24 genes are interrupted by 26 group-II intron-sequences. While many genes related to photosynthesis (RuBisCo, PSI, PSII and cytochrome b 6 /f subunits) have remained intact in the cpDNA, the majority of the NADH-dehydrogenase (ndh) subunits were either lost or became nonfunctional (i.e. pseudogenized). In agreement with previous reports, the photosynthetic-rates of adult Limodorum plants were found to be very low, further indicating that carbon-assimilation activity is insufficient to support the energy requirements of an adult plant, and may suggest that L. abortivum have adopted nutritional strategies similar to that of mycoheterotrophic orchid species.

  • Allen J.F. , de Paula W.B.M. , Puthiyaveetil S. , Nield J. (2011). A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Sci. 16: 645–655.

    • Search Google Scholar
    • Export Citation
  • Altschul S.F. , Gish W. , Miller W. , Myers E.W. , Lipman D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    • Search Google Scholar
    • Export Citation
  • Arnon D.I. (1949). Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol. 24: 1–15.

  • Asaf S. , Waqas M. , Khan A.L. , Khan M.A. , Kang S.-M. , Imran Q.M. , Shahzad R. , Bilal S. , Yun B.-W. , Lee I.-J. (2017). The complete chloroplast genome of wild rice (Oryza minuta) and its comparison to related species. Front. Plant Sci. 8: 1–15.

    • Search Google Scholar
    • Export Citation
  • Atwood J.T. (1995). Phylogeny and classification of the orchid family. Robert L. Dressler. Q. Rev. Biol. 70: 84–84.

  • Barkan A. (2011). Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 155: 1520–1532.

    • Search Google Scholar
    • Export Citation
  • Barkan A. , Rojas M. , Fujii S. , Yap A. , Chong Y. , Bond C. , Small I. (2012). A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8: e1002910.

    • Search Google Scholar
    • Export Citation
  • Barkan A. , Small I. (2014). Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65: 415–442.

  • Bazos I. , Yannitsaros A. (2005). Floristic reports from the island of Lesvos (Greece) I. Dicotyledones: Aceraceae to Guttiferae. Edinb. J. Bot. 61: 49–86.

    • Search Google Scholar
    • Export Citation
  • Brown G.G. , Colas des Francs-Small C. , Ostersetzer-Biran O. (2014). Group II intron splicing factors in plant mitochondria. Front. Plant Sci. 5: 35.

    • Search Google Scholar
    • Export Citation
  • Bungard R.A. (2004). Photosynthetic evolution in parasitic plants: insight from the chloroplast genome. BioEssays 26: 235–247.

  • Buttler K.P. (1986). Orchideen. Die wildwachsenden Arten undUnterarten Europas, Vorderasiens und Nordafrikas . Munchen: MosaikVerlag GmbH (in German).

    • Search Google Scholar
    • Export Citation
  • Cameron K.M. , Chase M.W. , Whitten W.M. , Kores P.J. , Jarrell D.C. , Albert V.A. , Yukawa T. , Hills H.G. , Goldman D.H. (1999). A phylogenetic analysis of the Orchidaceae: evidence from rbcL nucleotide sequences. Am. J. Bot. 86: 208–224.

    • Search Google Scholar
    • Export Citation
  • Casano L.M. , Lascano H.R. , Martin M. , Sabater B. (2004). Topology of the plastid Ndh complex and its NDH-F subunit in thylakoid membranes. Biochem. J. 382: 145–155.

    • Search Google Scholar
    • Export Citation
  • Chang C.C. , Lin H.C. , Lin I.P. , Chow T.Y. , Chen H.H. , Chen W.H. , Cheng C.H. , Lin C.Y. , Liu S.M. , Chang C.C. , Chaw S.M. (2006). The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mo.l Biol . Evol. 23: 279–291.

    • Search Google Scholar
    • Export Citation
  • Chase M.W. , Cameron K.M. , Freudenstein J.V. , Pridgeon A.M. , Salazar G. , van den Berg C. , Schuiteman A. (2015). An updated classification of Orchidaceae. Botanical Journal of the Linnean Society 177: 151–174.

    • Search Google Scholar
    • Export Citation
  • Colas des Francs-Small C. , Small I. (2014). Surrogate mutants for studying mitochondrially encoded functions. Biochimie 100: 234–242.

    • Search Google Scholar
    • Export Citation
  • Danin A. , Fragman-Sapir O. (2016). Flora of Israel Online. http://flora.org.il/en/plants/.

  • Delannoy E. , Fujii S. , Colas des Francs-Small C. , Brundrett M. , Small I. (2011). Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol. Biol. Evol. 28: 2077–2086.

    • Search Google Scholar
    • Export Citation
  • Dressler R. , Rasmussen H. (1996). Terrestrial Orchids: From Seed to Mycotrophic Plant . New York: Cambridge University Press.

  • Feng Y.L. , Wicke S. , Li J.W. , Han Y. , Lin C.S. , Li D.Z. , Zhou T.T. , Huang W.C. , Huang L.Q. , Jin X.H. (2016). Lineage-specific reductions of plastid genomes in an orchid tribe with partially and fully mycoheterotrophic species. Genome Biol. Evol. 8: 2164–2175.

    • Search Google Scholar
    • Export Citation
  • Finazzi G. , Johnson G.N. , Dall’Osto L. , Joliot P. , Wollman F.A. , Bassi R. (2004). A zeaxanthin-independent non-photochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl. Acad. Sci. U. S. A. 101: 17322–17322.

    • Search Google Scholar
    • Export Citation
  • Funk H.T. , Berg S. , Krupinska K. , Maier U.G. , Krause K. (2007a). Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol . 7: 1–12.

    • Search Google Scholar
    • Export Citation
  • Funk H.T. , Berg S. , Krupinska K. , Maier U.G. , Krause K. (2007b). Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol . 7: 45–48.

    • Search Google Scholar
    • Export Citation
  • Gebauer G. , Meyer M. (2003). 15N and 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol. 160: 209–223.

    • Search Google Scholar
    • Export Citation
  • Germain A. , Hotto A.M. , Barkan A. , Stern D.B. (2013). RNA processing and decay in plastids. Wiley Interdiscip. Rev. RNA 4: 295–316.

    • Search Google Scholar
    • Export Citation
  • Girlanda M. , Selosse M. A. Cafasso , D. Brilli , F. Delfine , S. Fabbian , R. Ghignone , S. Pinelli , P. Segreto , R. Loreto , F. Cozzolino , S., Perotto S. (2005). Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Mol. Ecol. 15: 491–504.

    • Search Google Scholar
    • Export Citation
  • Gornicki P. , Faris J. , King I. , Podkowinski J. , Gill B. , Haselkorn R. (1997). Plastid-localized acetyl-CoA carboxylase of bread wheat is encoded by a single gene on each of the three ancestral chromosome sets. Proc. Natl. Acad. Sci. U.S.A. 94: 14179–14184.

    • Search Google Scholar
    • Export Citation
  • Grewe F. , Edger P.P. , Keren I. , Sultan L. , Pires J.C. , Ostersetzer-Biran O. , Mower J.P. (2014). Comparative analysis of 11 Brassicales mitochondrial genomes and the mitochondrial transcriptome of Brassica oleracea. Mitochondrion 19, Part B: 135–143.

    • Search Google Scholar
    • Export Citation
  • Griffon E. (1898). L’assimilation chlorophyllienne chez les Orchidées terrestres et en particulier chez le Limodorum abortivum. Comptes Rendus de l’Académie des Sciences Paris (Physiologie Végétale) 127: 973–976.

    • Search Google Scholar
    • Export Citation
  • Gualberto J.M. , Lamattina L. , Bonnard G. , Weil J.H. , Grienenberger J.M. (1989). RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341: 660–662.

    • Search Google Scholar
    • Export Citation
  • Gualberto J.M. , Mileshina D. , Wallet C. , Niazi A.K. , Weber-Lotfi F. , Dietrich A. (2014). The plant mitochondrial genome: dynamics and maintenance. Biochimie 100: 107–120.

    • Search Google Scholar
    • Export Citation
  • Hammani K. , Giege P. (2014). RNA metabolism in plant mitochondria. Trends Plant Sci. 19: 380–389.

  • Hartzell S. , Bartlett M. , Yin J. , Porporato A. (2018). Similarities in the evolution of plants and cars. PLOS ONE 13: e0198044.

  • Hausner G. , Olson R. , Simon D. , Johnson I. , Sanders E.R. , Karol K.G. , McCourt R.M. , Zimmerly S. (2006). Origin and evolution of the chloroplast trnK (matK) Intron: a model for evolution of Group II Intron RNA structures. Mol. Biol. Evol. 23: 380–391.

    • Search Google Scholar
    • Export Citation
  • Hiratsuka J. , Shimada H. , Whittier R. , Ishibashi T. , Sakamoto M. , Mori M. , Kondo C. , Honji Y. , Sun C.R. , Meng B.Y. , 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.

    • Search Google Scholar
    • Export Citation
  • Holt N.E. , Fleming G.R. , Niyogi K.K. (2004). Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43: 8281–8289.

    • Search Google Scholar
    • Export Citation
  • Hong C.P. , Park J. , Lee Y. , Lee M. , Park S.G. , Uhm Y. , Lee J. , Kim C.-K. (2017). accD nuclear transfer of Platycodon grandiflorum and the plastid of early Campanulaceae. BMC Genomics 18: 607.

    • Search Google Scholar
    • Export Citation
  • Hull E. , Kitchener H.H.K. (1885). Mount Seir, Sinai and Western Palestine: Being a Narrative of a Scientific Expedition. London: Publication for the Committee of the Palestine Exploration Fund by Alexander P. Watt.

    • Search Google Scholar
    • Export Citation
  • Karcher D. , Bock R. (1998). Site-selective inhibition of plastid RNA editing by heatshock and antibiotics: a role for plastid translation in RNA editing. Nucleic Acids Res. 26: 1185–1190.

    • Search Google Scholar
    • Export Citation
  • Katoh K. , Rozewicki J. , Yamada K.D. (2017). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinformatics: bbx108–bbx108.

    • Search Google Scholar
    • Export Citation
  • Keren I. , Bezawork-Geleta A. , Kolton M. , Maayan I. , Belausov E. , Levy M. , Mett A. , Gidoni D. , Shaya F. , Ostersetzer-Biran O. (2009). AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15: 2299–2311.

    • Search Google Scholar
    • Export Citation
  • Konishi T. , Shinohara K. , Yamada K. , Sasaki Y. (1996). Acetyl-CoA carboxylase in higher plants: most plants other than gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. Plant Cell Physiol. 37: 117–122.

    • Search Google Scholar
    • Export Citation
  • Leake J.R. (1994). The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol. 127: 171–216.

  • Lichtenthaler H.K. , Wellbrum A.R. (1983). Determinations of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11: 591–592.

    • Search Google Scholar
    • Export Citation
  • Lin C.-S. , Chen J.J.W. , Huang Y.-T. , Chan M.-T. , Daniell H. , Chang W.-J. , Hsu C.-T. , Liao D.-C. , Wu F.-H. , Lin S.-Y. , Liao C.-F. , Deyholos M.K. , Wong G.K.-S. , Albert V.A. , Chou M.-L. , Chen C.-Y. , Shih M.-C. (2015). The location and translocation of ndh genes of chloroplast origin in the Orchidaceae family. Sci Rep. 5: 9040.

    • Search Google Scholar
    • Export Citation
  • Logacheva M.D. , Schelkunov M.I. , Penin A.A. (2011). Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol. Evol. 3: 1296–1303.

    • Search Google Scholar
    • Export Citation
  • Lohse M. , Drechsel O. , Bock R. (2007). OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr. Genet. 52: 267–274.

    • Search Google Scholar
    • Export Citation
  • Lohse M. , Drechsel O. , Kahlau S. , Bock R. (2013). OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 41: 1–7.

    • Search Google Scholar
    • Export Citation
  • Maayan I. , Shaya F. , Ratner K. , Mani Y. , Lavee S. , Avidan B. , Shahak Y. , Ostersetzer-Biran O. (2008). Photosynthetic activity during olive (Olea europaea) leaf development correlates with plastid biogenesis and Rubisco levels. Physio.l Plant 134: 547–558.

    • Search Google Scholar
    • Export Citation
  • Maier R.M. , Neckermann K. , Igloi G.L. , Kössel H. (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.

    • Search Google Scholar
    • Export Citation
  • Maxwell K. , Johnson G.N. (2000). Chlorophyll fluorescence – a practical guide. J. Exp. Bot. 51: 659–668.

  • Merckx V. , Bidartondo M.I. , Hynson N.A. (2009). Myco-heterotrophy: when fungi host plants. Ann. Bot. 104: 1255–1261.

  • Mohr G. , Perlman P.S. , Lambowitz A.M. (1993). Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucleic Acids Res. 21: 4991–4997.

    • Search Google Scholar
    • Export Citation
  • Moran R. , Porath D. (1980), Chlorophyll determination in intact tissues using N,N-dimethylformamide. Plant Physiol . 65: 478–479.

  • Muller P. , Li X.-P. , Niyogi K.K. (2001). Non-photochemical quenching. A response to excess light energy. Plant Physiol . 125: 1558–1566.

    • Search Google Scholar
    • Export Citation
  • Müller P. , Li X.-P. , Niyogi K.K. (2001). Non-photochemical quenching. A response to excess light energy. Plant Physiol . 125: 1558–1566.

    • Search Google Scholar
    • Export Citation
  • Polunin O. (1989). Guía fotográfica de las flores silvestres de España y de Europa. Barcelona: Omega.

  • Porra R.J. , Thompson W.A. , Kriedemann P.E. (1989). Determ ination of accurate extin ction coefficients and sim ultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975L: 384–394.

    • Search Google Scholar
    • Export Citation
  • Prikryl J. , Rojas M. , Schuster G. , Barkan A. (2011). Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl. Acad. Sci. U.S.A. 108: 415–420.

    • Search Google Scholar
    • Export Citation
  • Revill M.J.W. , Stanley S. , Hibberd J.M. (2005). Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. J. Exp. Bot. 56: 2477–2486.

    • Search Google Scholar
    • Export Citation
  • Roy M. , Gonneau C. , Rocheteau A. , Berveiller D. , Thomas J.-C. , Damesin C. , Selosse M.-A. (2013). Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ . Ecol. Monogr. 83: 95–117.

    • Search Google Scholar
    • Export Citation
  • Sato S. , Nakamura Y. , Kaneko T. , Asamizu E. , Tabata S. (1999). Complete structure of the chloroplast genome of Arabidopsis thaliana . DNA Res. 6: 283–290.

    • Search Google Scholar
    • Export Citation
  • Schelkunov M.I. , Shtratnikova V.Y. , Nuraliev M.S. , Selosse M.-A. , Penin A.A. , Logacheva M.D. (2015). Exploring the limits for reduction of plastid genomes: a case study of the mycoheterotrophic orchids Epipogium aphyllum and Epipogium roseum . Genome Biol. Evol. 7: 1179–1191.

    • Search Google Scholar
    • Export Citation
  • Schmitz-Linneweber C. , Lampe M.-K. , Sultan L.D. , Ostersetzer-Biran O. (2015). Organellar maturases: a window into the evolution of the spliceosome. BBA-BIOENERGETICS 1847: 798–808.

    • Search Google Scholar
    • Export Citation
  • Schreiber U. (2004). Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G.C. , Govindjee, eds, Chlorophyll a Fluorescence: A Signature of Photosynthesis. Dordrecht: Springer, pp. 279–319.

    • Search Google Scholar
    • Export Citation
  • Shevtsov S. , Nevo-Dinur K. , Faigon L. , Sultan L.D. , Zmudjak M. , Markovits M. , Ostersetzer-Biran O. (2018). Control of organelle gene expression by the mitochondrial transcription termination factor mTERF22 in Arabidopsis thaliana plants. PLoS One 13: e0201631.

    • Search Google Scholar
    • Export Citation
  • Shikanai T. (2006). RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol. Life Sci. 63: 698–708.

    • Search Google Scholar
    • Export Citation
  • Shin H.W. , Lee N.S. (2018). Understanding plastome evolution in Hemiparasitic Santalales: complete chloroplast genomes of three species, Dendrotrophe varians, Helixanthera parasitica, and Macrosolen cochinchinensis . PLoS One 13: e0200293.

    • Search Google Scholar
    • Export Citation
  • Shinozaki K. , Ohme M. , Tanaka M. , Wakasugi T. , Hayashida N. , Matsubayashi T. , Zaita N. , Chunwongse J. , Obokata J. , Yamaguchi-Shinozaki K. , Ohto C. , Torazawa K. , Meng B.Y. , Sugita M. , Deno H. , Kamogashira T. , Yamada K. , Kusuda J. , Takaiwa F. , Kato A. , Tohdoh N. , Shimada H. , Sugiura M. (1986). The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5: 2043–2049.

    • Search Google Scholar
    • Export Citation
  • Song Y. , Yu W.-B. , Tan Y. , Liu B. , Yao X. , Jin J. , Padmanaba M. , Yang J.-B. , Corlett R.T. (2017). Evolutionary comparisons of the chloroplast genome in Lauraceae and insights into loss events in the Magnoliids. Genome Biol. Evol. 9: 2354–2364.

    • Search Google Scholar
    • Export Citation
  • Stadermann K.B. , Holtgrawe D. , Weisshaar B. (2016). Chloroplast genome sequence of Arabidopsis thaliana accession Landsberg erecta, assembled from single-molecule, real-time sequencing data. Genome Announc. 4: 1–2.

    • Search Google Scholar
    • Export Citation
  • Stern D.B. , Goldschmidt-Clermont M. , Hanson M.R. (2010). Chloroplast RNA metabolism. Ann. Rev. Plant Biol. 61: 125–155.

  • Stöckel M. , Meyer C. , Gebauer G. (2011). The degree of mycoheterotrophic carbon gain in green, variegated and vegetative albino individuals of Cephalanthera damasonium is related to leaf chlorophyll concentrations. New Phytol. 189: 790–796.

    • Search Google Scholar
    • Export Citation
  • Sugiura M. (1989). The chloroplast chromosomes in land plants. Annu. Rev. Cell Biol. 5: 51–70.

  • Vogel J. , Hubschmann T. , Borner T. , Hess W.R. (1997). Splicing and intron-internal RNA editing of trnK-matK transcripts in barley plastids: support for MatK as an essential splice factor. J. Mol. Biol. 270: 179.

    • Search Google Scholar
    • Export Citation
  • Wicke S. , Müller K.F. , de Pamphilis C.W. , Quandt D. , Wickett N.J. , Zhang Y. , Renner S.S. , Schneeweiss G.M. (2013). Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell 25: 3711–3725.

    • Search Google Scholar
    • Export Citation
  • Wickett N.J. , Zhang Y. , Hansen S.K. , Roper J.M. , Kuehl J.V. , Plock S.A. , Wolf P.G. , dePamphilis C.W. , Boore J.L. , Goffinet B. (2008). Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis . Mol. Biol. Evol. 25: 393–401.

    • Search Google Scholar
    • Export Citation
  • Wolfe K.H. , Morden C.W. , Palmer J.D. (1992). Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. PNAS 89: 10648–10652.

    • Search Google Scholar
    • Export Citation
  • Zerbino D.R. , Birney E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821–829.

    • Search Google Scholar
    • Export Citation
  • Zhu S. , Niu Z. , Yan W. , Xue Q. , Ding X. (2016). The complete chloroplast genome sequence of Anoectochilus emeiensis. Mitochondrial DNA. Part A, DNA Mapping, Dequencing, and Analysis 27: 3565–3566.

    • Search Google Scholar
    • Export Citation
  • Zmasek C.M. , Eddy S.R. (2001). ATV: display and manipulation of annotated phylogenetic trees. Bioinformatics 17: 383–384.

  • Zmudjak M. , Ostersetzer-Biran O. (2017). RNA metabolism and transcript regulation. In: Logan D.C. , ed., Annual Plant Reviews , Volume 50 , pp. 261–309. Wiley-Blackwell.

    • Search Google Scholar
    • Export Citation
  • Zoschke R. , Nakamura M. , Liere K. , Sugiura M. , Börner T. , Schmitz-Linneweber C. (2010). An organellar maturase associates with multiple group II introns. PNAS 107: 3245–3250.

    • Search Google Scholar
    • Export Citation
  • Zoschke R. , Ostersetzer-Biran O. , Börner T. , Schmitz-Linneweber C. (2009). Analysis of the regulation of MatK gene expression. Endocytobiosis Cell Res. 19: 127–135.

    • Search Google Scholar
    • Export Citation

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 138 138 14
Full Text Views 57 57 7
PDF Downloads 25 25 1