Abstract
The importance of photosynthesis as a mode of energy production has put plastid genomes of plants under a constant purifying selection. This has shaped the characteristic features of plastid genomes across the entire spectrum of photosynthetic plants and has led to a highly uniform and conserved plastid genome with respect to structure, size, gene order, intron and editing site positions and coding capacity. Parasitic species that have dropped photosynthesis as the main energy provider share striking deviations from the plastid genome norm: multiple rearrangements within the circular chromosome, pseudogenization and gene deletions, promoter losses, intron losses as well as the extensive loss of mRNA editing competence have been reported. The collective loss of larger sets of functionally related genes like those for the plastid NADH–dehydrogenase complex and concomitant losses of RNA polymerase genes together with their target promoters point to “domino effects” where an initial loss might have triggered others. An example, which will be discussed in more detail, is the concomitant loss of the intron maturase gene matK and all introns that are supposedly subject to MatK-dependent splicing in two Cuscuta species.
Similar content being viewed by others
Abbreviations
- IR:
-
Inverted repeat
- LSC:
-
Large single copy region
- NEP:
-
Nuclear-endoded RNA polymerase
- PEP:
-
Plastid-encoded RNA polymerase
- ptDNA:
-
Plastid DNA
- SSC:
-
Small single copy region
References
Allen JF (2003) The function of genomes in bioenergetic organelles. Philos Trans R Soc Lond B Biol Sci 358:19–37
Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88
Barbrook AC, Howe CJ, Purton S (2006) Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci 11:101–108
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 218:135–142
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 219:541–546
Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Bock R (ed) Cell and molecular biology of plastids. Topics in current genetics, vol 19. Springer, Berlin, pp 29–62
Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM (2007) Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 3: e148, pp 1401–1413
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 320:37–77
Bungard RA (2004) Photosynthetic evolution in parasitic plants: insight from the chloroplast genome. Bio Essays 26:235–247
Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46
Cai Z, Guisinger M, Kim HG, Ruck E, Blazier JC, McMurtry V, Kuehl JV, Boore J, Jansen RK (2008) Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. J Mol Evol 67:696–704
Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH, Cheng CH, Lin CY, Liu SM, Chaw SM (2006) The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol 23:279–291
Blazier JC, Guisinger MM, Jansen RK (2011) Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol Biol 76:263–272
Daniell H, Wurdack KJ, Kanagaraj A, Lee SB, Saski C, Jansen RK (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
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 4:12
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
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 7:45
Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, Hall N, Ren Q, Paulsen IT, Pain A, Berriman M, Wilson RJ, Sato S, Ralph SA, Mann DJ, Xiong Z, Shallom SJ, Weidman J, Jiang L, Lynn J, Weaver B, Shoaibi A, Domingo AR, Wasawo D, Crabtree J, Wortman JR, Haas B, Angiuoli SV, Creasy TH, Lu C, Suh B, Silva JC, Utterback TR, Feldblyum TV, Pertea M, Allen J, Nierman WC, Taracha EL, Salzberg SL, White OR, Fitzhugh HA, Morzaria S, Venter JC, Fraser CM, Nene V (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309:134–137
Gockel G, Hachtel W (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347–351
Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66:34–44
Greiner S, Wang X, Herrmann RG, Rauwolf U, Mayer K, Haberer G, Meurer J (2008) The complete nucleotide sequences of the 5 genetically distinct plastid genomes of Oenothera, subsection Oenothera: II, a microevolutionary view using bioinformatics and formal genetic data. Mol Biol Evol 25:2019–2030
Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2008) Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA 105:18424–18429
Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2011) Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Mol Biol Evol 28:583–600
Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119
Hess W, Müller A, Nagy F, Börner T (1994) Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol Gen Genet 242:305–312
Hibberd JM, Bungard RA, Press MC, Jeschke WD, Scholes JD, Quick WP (1998) Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205:506–513
Horvath EM, Peter SO, Joet T, Rumeau D, Cournac L, Horvath GV, Kavanagh TA, Schafer C, Peltier G, Medgyesy P (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol 123:1337–1350
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 158:121–133
Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374
Jansen RK, Wojciechowski MF, Sanniyasi E, Lee SB, Daniell H (2008) Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Mol Phylogenet Evol 48:1204–1217
Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121
Krause K (2010) Plastid genome variation and selective constraint in species of the parasitic plant genus Cuscuta. In: Urbano KV (ed) Advances in genetics research, vol 2, chap 15. Nova Science Publishers Inc, New York, pp 1–15
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, chap 4. Springer, Berlin, in press
Krause K, Berg S, Krupinska K (2003) Plastid transcription in the holoparasitic plant genus Cuscuta: parallel loss of the rrn16 PEP-promoter and of the rpoA and rpoB genes coding for the plastid-encoded RNA polymerase. Planta 216:815–823
Krause K, Kilbienski I, Mulisch M, Rodiger A, Schafer A, Krupinska K (2005) DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 579:3707–3712
Lane CE, Archibald JM (2008) The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol Evol 23:268–275
Liere K, Weihe A, Borner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168:1345–1360
Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Borner T, Tillich M (2008) Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol 6:36
Marechal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186:299–317
Marechal A, Parent JS, Veronneau-Lafortune F, Joyeux A, Lang BF, Brisson N (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc Natl Acad Sci USA 106:14693–14698
Martin M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiol Biochem 48:636–645
McCoy SR, Kuehl JV, Boore JL, Raubeson LA (2008) The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol 8:130
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 7:57
McNeal JR, Kuehl JV, Boore JL, Leebens-Mack J, dePamphilis CW (2009) Parallel loss of plastid introns and their maturase in the genus Cuscuta. PLoS One 4:e5982
Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30
Panda MM, Choudhury NK (1992) Effect of irradiance and nutrients on chlorophyll and carotenoid content and Hill reaction activity in Cuscuta reflexa. Photosyntetica 26:585–592
Revill MJ, Stanley S, Hibberd JM (2005) Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. J Exp Bot 56:2477–2486
Reyes-Prieto A, Bhattacharya D (2007) Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within Plantae. Mol Biol Evol 24:2358–2361
Sato S (2011) The apicomplexan plastid and its evolution. Cell Mol Life Sci 68:1285–1296
Schmitz-Linneweber C, Barkan A (2007) RNA splicing and RNA editing in chloroplasts In: Bock R (ed) Cell and molecular biology plastids. Topics in Current Genetics, vol 19. Springer, Berlin, Heidelberg, pp 213–248
Schmitz-Linneweber C, Maier RM, Alcaraz JP, Cottet A, Herrmann RG, Mache R (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Mol Biol 45:307–315
Sherman TD, Pettigrew WT, Vaughn KC (1999) Structural and immunological characterization of the Cuscuta pentagona L. chloroplast. Plant Cell Physiol 40:592–603
Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (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
Tillich M, Krause K (2010) The ins and outs of editing and splicing of plastid RNAs: lessons from parasitic plants. Nat Biotechnol 27:256–266
Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43:708–715
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 25:1566–1575
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 210:701–707
van der Kooij TA, Krupinska K, Krause K (2005) Tocochromanol content and composition in different species of the parasitic flowering plant genus Cuscuta. J Plant Physiol 162:777–781
Westwood JH, Yoder JI, Timko MP, de Pamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235
Wicke S, Schneeweiss GM, Depamphilis CW, Muller KF, Quandt D (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297
Wickett NJ, Fan Y, Lewis PO, Goffinet B (2008a) Distribution and evolution of pseudogenes, gene losses, and a gene rearrangement in the plastid genome of the nonphotosynthetic liverwort, Aneura mirabilis (Metzgeriales, Jungermanniopsida). J Mol Evol 67:111–122
Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, DePamphilis CW, Boore JL, Goffinet B (2008b) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25:393–401
Wilson RJ, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, Whyte A, Strath M, Moore DJ, Moore PW, Williamson DH (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261:155–172
Wolf PG, Der JP, Duffy AM, Davidson JB, Grusz AL, Pryer KM (2011) The evolution of chloroplast genes and genomes in ferns. Plant Mol Biol 76:251–261
Wolfe KH, Morden CW, Ems SC, Palmer JD (1992a) Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: loss or accelerated sequence evolution of tRNA and ribosomal protein genes. J Mol Evol 35:304–317
Wolfe KH, Morden CW, Palmer JD (1992b) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652
Yue F, Cui L, de Pamphilis CW, Moret BM, Tang J (2008) Gene rearrangement analysis and ancestral order inference from chloroplast genomes with inverted repeat. BMC Genomics 9(Suppl 1):S25
Zoschke R, Nakamura M, Liere K, Sugiura M, Borner T, Schmitz-Linneweber C (2010) An organellar maturase associates with multiple group II introns. Proc Natl Acad Sci USA 107:3245–3250
Acknowledgments
The constructive suggestions made by Prof. Karsten Fischer (University of Tromsø) regarding the text and concept of the manuscript are highly appreciated. The author is aware that in many cases, only a selection of relevant publications were cited and wishes to apologize to all authors whose original papers could not be referred to due to space limitations.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Krause, K. Piecing together the puzzle of parasitic plant plastome evolution. Planta 234, 647–656 (2011). https://doi.org/10.1007/s00425-011-1494-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-011-1494-9