Reduced Genomes from Parasitic Plant Plastids: Templates for Minimal Plastomes?

  • Kirsten KrauseEmail author
  • Lars B. Scharff
Part of the Progress in Botany book series (BOTANY, volume 75)


Plastids are the characteristic cell organelles of plants. While movement, loss, and replacement of whole plastids have occurred in single-celled algae and some parasites derived thereof, land plants have shown more moderate twists in plastid evolution. Here, the most poignant deviations are the reduction in size and coding capacity of plastid genomes as a consequence of a heterotrophic lifestyle in haustorial parasites and mycoheterotrophic plants, which will be broadly summarized in this article as “parasitic plants”. While the loss of photosynthesis genes can be easily explained with the vanishing of a photoautotrophic lifestyle, other gene losses are more difficult to reconcile with persisting regulatory and metabolic functions of the reduced plastids. An assessment of plastid gene essentiality using tobacco plastome mutants revealed that the catalog of losses even includes genes for the gene expression apparatus that are essential for cell viability under heterotrophic conditions. We will discuss whether these genes really are dispensable and to what degree minimal parasitic plant plastomes could be blueprints for artificial plastid genomes.


Endosymbiosis Evolution Parasitic plants Plastids Transcription Translation 



A. Tooming-Klunderud (Norwegian High-Throughput Sequencing Centre, University of Oslo, Norway) is thanked for 454 sequence generation of Cuscuta ESTs. Dr. R. Schwacke (Tromsø, Norway) and J. Hollmann (University of Kiel, Germany) are thanked for helping with bioinformatic evaluation of transcriptome data. We thank Prof. I. Dörr and Dr. T. van der Kooij for sharing their electron micrographs of Cuscuta.


  1. Ahlert D, Ruf S, Bock R (2003) Plastid protein synthesis is required for plant development in tobacco. Proc Natl Acad Sci 100:15730–15735PubMedCrossRefGoogle Scholar
  2. Alkatib S, Scharff LB, Rogalski M, Fleischmann TT, Matthes A, Schöttler MA, Ruf S, Bock R (2012a) The contributions of wobbling and superwobbling to the reading of the genetic code. PLoS Genet 8:e1003076PubMedCrossRefGoogle Scholar
  3. Alkatib S, Fleischmann TT, Scharff LB, Bock R (2012b) Evolutionary constraints on the plastid tRNA set decoding methionine and isoleucine. Nucleic Acids Res 40:6713–6724PubMedCrossRefGoogle Scholar
  4. Allison L (2000) The role of sigma factors in plastid transcription. Biochimie 82:537–548PubMedCrossRefGoogle Scholar
  5. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515PubMedCrossRefGoogle Scholar
  6. Baba K, Schmidt J, Espinosa-Ruiz A, Villarejo A, Shiina T, Gardestrom P, Sane AP, Bhalerao RP (2004) Organellar gene transcription and early seedling development are affected in the rpoT;2 mutant of Arabidopsis. Plant J 38:38–48PubMedCrossRefGoogle Scholar
  7. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2Google Scholar
  8. Barbrook AC, Howe CJ, Purton S (2006) Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci 11:101–108PubMedCrossRefGoogle Scholar
  9. Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155:1520–1532PubMedCrossRefGoogle Scholar
  10. Barkman TJ, McNeal JR, Lim SH, Coat G, Croom HB, Young ND, Depamphilis CW (2007) Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 7:248PubMedCrossRefGoogle Scholar
  11. Barrett CF, Davis JI (2012) The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. Am J Bot 99:1513–1523PubMedCrossRefGoogle Scholar
  12. Berg S, Krupinska K, Krause K (2003) Plastids of three Cuscuta species differing in plastid coding capacity have a common parasite-specific RNA composition. Planta 218:135–142PubMedCrossRefGoogle Scholar
  13. Berg S, Krause K, Krupinska K (2004) The rbcL genes of two Cuscuta species, C. gronovii and C. subinclusa, are transcribed by the nuclear-encoded plastid RNA polymerase (NEP). Planta 219:541–546PubMedCrossRefGoogle Scholar
  14. Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352PubMedCrossRefGoogle Scholar
  15. Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Bock R (ed) Cell and molecular biology of plastids, vol 19, Topics in current genetics. Springer, Berlin, pp 29–62CrossRefGoogle Scholar
  16. Borza T, Popescu CE, Lee RW (2005) Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot Cell 4:253–261PubMedCrossRefGoogle Scholar
  17. Bubunenko MG, Schmidt J, Subramanian AR (1994) Protein substitution in chloroplast ribosome evolution: a eukaryotic cytosolic protein has replaced its organelle homologue (L23) in spinach. J Mol Biol 240:28–41PubMedCrossRefGoogle Scholar
  18. Bubunenko M, Korepanov A, Court DL, Jagannathan I, Dickinson D, Chaudhuri BR, Garber MB, Culver GM (2006) 30S ribosomal subunits can be assembled in vivo without primary binding ribosomal protein S15. RNA 12:1229–1239PubMedCrossRefGoogle Scholar
  19. Bundrett M (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  20. Cahoon AB, Stern DB (2001) Plastid transcription: a menage a trois? Trends Plant Sci 6:45–46CrossRefGoogle Scholar
  21. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366PubMedCrossRefGoogle Scholar
  22. Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354PubMedGoogle Scholar
  23. Corneille S, Lutz K, Svab Z, Maliga P (2001) Efficient elimination of selectable marker genes from the plastid genome by the CRE-lox site-specific recombination system. Plant J 27:171–178PubMedCrossRefGoogle Scholar
  24. Crick FHC (1966) Codon—anticodon pairing: the wobble hypothesis. J Mol Biol 19:548–555PubMedCrossRefGoogle Scholar
  25. Dawson JH, Musselman LI, Wolswinkel P, Dörr I (1994) Biology and control of Cuscuta. Rev Weed Sci 6:265–317Google Scholar
  26. de Koning AP, Keeling PJ (2004) Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga. Eukaryot Cell 3:1198–1205PubMedCrossRefGoogle Scholar
  27. de Koning AP, Keeling PJ (2006) The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol 4:12PubMedCrossRefGoogle Scholar
  28. 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 28:2077–2086PubMedCrossRefGoogle Scholar
  29. Demarsy E, Buhr F, Lambert E, Lerbs-Mache S (2012) Characterization of the plastid-specific germination and seedling establishment transcriptional programme. J Exp Bot 63:925–939PubMedCrossRefGoogle Scholar
  30. DeSantis-Maciossek G, Kofer W, Bock A, Schoch S, Maier RM, Wanner G, Rüdiger W, Koop HU, Herrmann RG (1999) Targeted disruption of the plastid RNA polymerase genes rpoA, B and C1: molecular biology, biochemistry and ultrastructure. Plant J 18:477–489CrossRefGoogle Scholar
  31. Duchêne A-M, Pujol C, Maréchal-Drouard L (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55:1–18PubMedCrossRefGoogle Scholar
  32. Favory JJ, Kobayshi M, Tanaka K, Peltier G, Kreis M, Valay JG, Lerbs-Mache S (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res 33:5991–5999PubMedCrossRefGoogle Scholar
  33. Fleischmann TT, Scharff LB, Alkatib S, Hasdorf S, Schöttler MA, Bock R (2011) Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23:3137–3155PubMedCrossRefGoogle Scholar
  34. Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:45PubMedCrossRefGoogle Scholar
  35. Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10:3073–3078PubMedGoogle Scholar
  36. Gibson DG, Benders GA, Andrews-Pfannkoch C, Denisova EA, Baden-Tillson H, Zaveri J, Stockwell TB, Brownley A, Thomas DW, Algire MA, Merryman C, Young L, Noskov VN, Glass JI, Venter JC, Hutchison CA III, Smith HO (2008) Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science 319:1215–1220PubMedCrossRefGoogle Scholar
  37. Gockel G, Hachtel W (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347–351PubMedCrossRefGoogle Scholar
  38. Hajdukiewicz P, Allison L, Maliga P (1997) The two RNA-polymerases encoded by the nuclear and plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 13:4041–4048CrossRefGoogle Scholar
  39. Hallick RB, Lipper C, Richards OC, Rutter WJ (1976) Isolation of a transcriptionally active chromosome from chloroplasts of Euglena gracilis. Biochemistry 15:3039–3045PubMedCrossRefGoogle Scholar
  40. Han CD, Coe EH Jr, Martienssen RA (1992) Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize. EMBO J 11:4037–4046PubMedGoogle Scholar
  41. Hess W, Börner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59PubMedCrossRefGoogle Scholar
  42. Hess WR, Hoch B, Zeltz P, Hubschmann T, Kossel H, Borner T (1994) Inefficient rpl2 splicing in barley mutants with ribosome-deficient plastids. Plant Cell 6:1455–1465PubMedGoogle Scholar
  43. Hibberd JM, Bungard RA, Press MC, Jeschke WD, Scholes JD, Quick WP (1998) Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205:506–513CrossRefGoogle Scholar
  44. Howe CJ, Purton S (2007) The little genome of apicomplexan plastids: its raison d’etre and a possible explanation for the “delayed death” phenomenon. Protist 158:121–133PubMedCrossRefGoogle Scholar
  45. Hricova A, Quesada V, Micol JL (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiol 141:942–956PubMedCrossRefGoogle Scholar
  46. Igloi G, Kössel H (1992) The transcriptional apparatus of chloroplasts. Crit Rev Plant Sci 10:525–558CrossRefGoogle Scholar
  47. Ingelsson B, Vener AV (2012) Phosphoproteomics of Arabidopsis chloroplasts reveals involvement of the STN7 kinase in phosphorylation of nucleoid protein pTAC16. FEBS Lett 586:1265–1271PubMedCrossRefGoogle Scholar
  48. Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Kato K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J 42:133–144PubMedCrossRefGoogle Scholar
  49. Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107:10949–10954PubMedCrossRefGoogle Scholar
  50. Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 365:729–748PubMedCrossRefGoogle Scholar
  51. Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121PubMedCrossRefGoogle Scholar
  52. Krause K (2011) Piecing together the puzzle of parasitic plant plastome evolution. Planta 234:647–656PubMedCrossRefGoogle Scholar
  53. Krause K (2012) Plastid genomes of parasitic plants: a trail of reductions and losses. In: Bullerwell C (ed) Organelle genetics: evolution of organelle genomes and gene expression. Springer, BerlinGoogle Scholar
  54. Krause K, Krupinska K (2000) Molecular and functional properties of highly purified transcriptionally active chromosomes from spinach chloroplasts. Physiol Plant 109:188–195CrossRefGoogle Scholar
  55. Krause K, Maier RM, Kofer W, Krupinska K, Herrmann RG (2000) Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet 263:1022–1030PubMedCrossRefGoogle Scholar
  56. Lane CE, Archibald JM (2008) The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol Evol 23:268–275PubMedCrossRefGoogle Scholar
  57. Leake JR (1994) The biology of myco-heterotrophic (“saprophytic”) plants. New Phytol 127:171–216CrossRefGoogle Scholar
  58. Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31:171–188PubMedCrossRefGoogle Scholar
  59. Legen J, Wanner G, Herrmann RG, Small I, Schmitz-Linneweber C (2007) Plastid tRNA genes trnC-GCA and trnN-GUU are essential for plant cell development. Plant J 51:751–762PubMedCrossRefGoogle Scholar
  60. Leister D, Kleine T (2011) Role of intercompartmental DNA transfer in producing genetic diversity. Int Rev Cell Mol Biol 291:73–114PubMedCrossRefGoogle Scholar
  61. Liere K, Weihe A, Borner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168:1345–1360PubMedCrossRefGoogle Scholar
  62. Lim L, McFadden GI (2010) The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci 365:749–763PubMedCrossRefGoogle Scholar
  63. Logacheva MD, Schelkunov MI, Penin AA (2011) Sequencing and analysis of plastid genome in mycoheterotrophic orchid Neottia nidus-avis. Genome Biol Evol 3:1296–1303PubMedCrossRefGoogle Scholar
  64. Loschelder H, Schweer J, Link B, Link G (2006) Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiol 142:642–650PubMedCrossRefGoogle Scholar
  65. Lung B, Zemann A, Madej MJ, Schuelke M, Techritz S, Ruf S, Bock R, Hüttenhofer A (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res 34:3842–3852PubMedCrossRefGoogle Scholar
  66. Maeder C, Draper DE (2005) A small protein unique to bacteria organizes rRNA tertiary structure over an extensive region of the 50 S ribosomal subunit. J Mol Biol 354:436–446PubMedCrossRefGoogle Scholar
  67. Maguire BA, Wild DG (1997) The roles of proteins L28 and L33 in the assembly and function of Escherichia coli ribosomes in vivo. Mol Microbiol 23:237–245PubMedCrossRefGoogle Scholar
  68. Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, Watkins KP, Barkan A, van Wijk KJ (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 158:156–189PubMedCrossRefGoogle Scholar
  69. Matsuzaki M, Kuroiwa H, Kuroiwa T, Kita K, Nozaki H (2008) A cryptic algal group unveiled: a plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Mol Biol Evol 25:1167–1179PubMedCrossRefGoogle Scholar
  70. McNeal JR, Kuehl JV, Boore JL, de Pamphilis CW (2007) Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biol 7:57PubMedCrossRefGoogle Scholar
  71. Melonek J, Matros A, Trösch M, Mock H-P, Krupinska K (2012) The core of chloroplast nucleoids contains architectural SWIB-domain proteins. Plant Cell 24(7):3060–3073PubMedCrossRefGoogle Scholar
  72. Merckx V, Freudenstein JV (2010) Evolution of mycoheterotrophy in plants: a phylogenetic perspective. New Phytol 185:605–609PubMedCrossRefGoogle Scholar
  73. Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313PubMedCrossRefGoogle Scholar
  74. Myouga F, Akiyama K, Motohashi R, Kuromori T, Ito T, Iizumi H, Ryusui R, Sakurai T, Shinozaki K (2010) The Chloroplast Function Database: a large-scale collection of Arabidopsis Ds/Spm- or T-DNA-tagged homozygous lines for nuclear-encoded chloroplast proteins, and their systematic phenotype analysis. Plant J 61:529–542PubMedCrossRefGoogle Scholar
  75. Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140PubMedCrossRefGoogle Scholar
  76. Nickrent DL, Ouyang Y, Duff RJ, dePhamphilis CW (1997) Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Mol Biol 34:717–729PubMedCrossRefGoogle Scholar
  77. Peled-Zehavi H, Danon A (2007) Translation and translational regulation in chloroplasts. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 249–281CrossRefGoogle Scholar
  78. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, -6, and −12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197PubMedCrossRefGoogle Scholar
  79. Pombert J-F, Keeling PJ (2010) The mitochondrial genome of the entomoparasitic green alga helicosporidium. PLoS One 5:e8954PubMedCrossRefGoogle Scholar
  80. Privat I, Hakimi MA, Buhot L, Favory JJ, Mache-Lerbs S (2003) Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol Biol 51:385–399PubMedCrossRefGoogle Scholar
  81. Revill MJ, Stanley S, Hibberd JM (2005) Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. J Exp Bot 56:2477–2486PubMedCrossRefGoogle Scholar
  82. Reyes-Prieto A, Bhattacharya D (2007) Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within Plantae. Mol Biol Evol 24:2358–2361PubMedCrossRefGoogle Scholar
  83. Rogalski M, Ruf S, Bock R (2006) Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res 34:4537–4545PubMedCrossRefGoogle Scholar
  84. Rogalski M, Karcher D, Bock R (2008a) Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 15:192–198PubMedCrossRefGoogle Scholar
  85. Rogalski M, Schottler MA, Thiele W, Schulze WX, Bock R (2008b) Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 20(8):2221–2237, tpc.108.060392PubMedCrossRefGoogle Scholar
  86. Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF (2007) Plastid genes in a non-photosynthetic dinoflagellate. Protist 158:105–117PubMedCrossRefGoogle Scholar
  87. Schneider A (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80:1033–1053PubMedCrossRefGoogle Scholar
  88. Schroter Y, Steiner S, Matthai K, Pfannschmidt T (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics 10:2191–2204PubMedCrossRefGoogle Scholar
  89. Schwacke R, Fischer K, Ketelsen B, Krupinska K, Krause K (2007) Comparative survey of plastid and mitochondrial targeting properties of transcription factors in Arabidopsis and rice. Mol Genet Genomics 277:631–646PubMedCrossRefGoogle Scholar
  90. Schweer J, Turkeri H, Link B, Link G (2010) AtSIG6, a plastid sigma factor from Arabidopsis, reveals functional impact of cpCK2 phosphorylation. Plant J 62:192–202PubMedCrossRefGoogle Scholar
  91. Sharma MR, Wilson DN, Datta PP, Barat C, Schluenzen F, Fucini P, Agrawal RK (2007) Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc Natl Acad Sci USA 104(49):19315–19320PubMedCrossRefGoogle Scholar
  92. Steiner S, Schroter Y, Pfalz J, Pfannschmidt T (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157:1043–1055PubMedCrossRefGoogle Scholar
  93. Tartar A, Boucias DG (2004) The non-photosynthetic, pathogenic green alga Helicosporidium sp. has retained a modified, functional plastid genome. FEMS Microbiol Lett 233:153–157PubMedCrossRefGoogle Scholar
  94. Tiller N, Weingartner M, Thiele W, Maximova E, Schottler MA, Bock R (2012) The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. Plant J 69:302–316PubMedCrossRefGoogle Scholar
  95. Ueda M, Fujimoto M, Arimura S, Murata J, Tsutsumi N, Kadowaki K (2007) Loss of the rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene 402:51–56PubMedCrossRefGoogle Scholar
  96. Ueda M, Nishikawa T, Fujimoto M, Takanashi H, Arimura S, Tsutsumi N, Kadowaki K (2008) Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol Biol Evol 25:1566–1575PubMedCrossRefGoogle Scholar
  97. van der Kooij TA, Krause K, Dorr I, Krupinska K (2000) Molecular, functional and ultrastructural characterisation of plastids from six species of the parasitic flowering plant genus Cuscuta. Planta 210:701–707PubMedCrossRefGoogle Scholar
  98. Wagner R, Pfannschmidt T (2006) Eukaryotic transcription factors in plastids – bioinformatic assessment and implications for the evolution of gene expression machineries in plants. Gene 381:62–70PubMedCrossRefGoogle Scholar
  99. Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, DePamphilis CW, Boore JL, Goffinet B (2008) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25:393–401PubMedCrossRefGoogle Scholar
  100. Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652PubMedCrossRefGoogle Scholar
  101. Yao J, Roy-Chowdhury S, Allison LA (2003) AtSig5 is an essential nucleus-encoded Arabidopsis sigma-like factor. Plant Physiol 132:739–747PubMedCrossRefGoogle Scholar
  102. Zghidi W, Merendino L, Cottet A, Mache R, Lerbs-Mache S (2007) Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids. Nucleic Acids Res 35:455–464PubMedCrossRefGoogle Scholar
  103. Zhelyazkova P, Sharma CM, Forstner KU, Liere K, Vogel J, Borner T (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24:123–136PubMedCrossRefGoogle Scholar
  104. Zubko MK, Day A (1998) Stable albinism induced without mutagenesis: a model for ribosome-free plastid inheritance. Plant J 15:265–271PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department for Arctic and Marine BiologyUniversity of TromsøTromsøNorway
  2. 2.Max-Plank Institute for Molecular Plant PhysiologyPotsdam-GolmGermany

Personalised recommendations