Evolution of Chloroplast Transcript Processing in and Its Chromerid Algal Relatives
It is well understood that apicomplexan parasites, such as the malaria pathogen Plasmodium, are descended from free-living algae, and maintain a vestigial chloroplast that has secondarily lost all genes of photosynthetic function. Recently, two fully photosynthetic relatives of parasitic apicomplexans have been identified, the ‘chromerid’ algae Chromera velia and Vitrella brassicaformis, which retain photosynthesis genes within their chloroplasts. Elucidating the processes governing gene expression in chromerid chloroplasts might provide valuable insights into the origins of parasitism in the apicomplexans. We have characterised chloroplast transcript processing pathways in C. velia, V. brassicaformis and P. falciparum with a focus on the addition of an unusual, 3′ poly(U) tail. We demonstrate that poly(U) tails in chromerids are preferentially added to transcripts that encode proteins that are directly involved in photosynthetic electron transfer, over transcripts for proteins that are not involved in photosynthesis. To our knowledge, this represents the first chloroplast transcript processing pathway to be associated with a particular functional category of genes. In contrast, Plasmodium chloroplast transcripts are not polyuridylylated. We additionally present evidence that poly(U) tail addition in chromerids is involved in the alternative processing of polycistronic precursors covering multiple photosynthesis genes, and appears to be associated with high levels of transcript abundance. We propose that changes to the chloroplast transcript processing machinery were an important step in the loss of photosynthesis in ancestors of parasitic apicomplexans.
Vyšlo v časopise:
Evolution of Chloroplast Transcript Processing in and Its Chromerid Algal Relatives. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004008
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004008
Souhrn
It is well understood that apicomplexan parasites, such as the malaria pathogen Plasmodium, are descended from free-living algae, and maintain a vestigial chloroplast that has secondarily lost all genes of photosynthetic function. Recently, two fully photosynthetic relatives of parasitic apicomplexans have been identified, the ‘chromerid’ algae Chromera velia and Vitrella brassicaformis, which retain photosynthesis genes within their chloroplasts. Elucidating the processes governing gene expression in chromerid chloroplasts might provide valuable insights into the origins of parasitism in the apicomplexans. We have characterised chloroplast transcript processing pathways in C. velia, V. brassicaformis and P. falciparum with a focus on the addition of an unusual, 3′ poly(U) tail. We demonstrate that poly(U) tails in chromerids are preferentially added to transcripts that encode proteins that are directly involved in photosynthetic electron transfer, over transcripts for proteins that are not involved in photosynthesis. To our knowledge, this represents the first chloroplast transcript processing pathway to be associated with a particular functional category of genes. In contrast, Plasmodium chloroplast transcripts are not polyuridylylated. We additionally present evidence that poly(U) tail addition in chromerids is involved in the alternative processing of polycistronic precursors covering multiple photosynthesis genes, and appears to be associated with high levels of transcript abundance. We propose that changes to the chloroplast transcript processing machinery were an important step in the loss of photosynthesis in ancestors of parasitic apicomplexans.
Zdroje
1. WalkerG, DorrellRG, SchlachtA, DacksJB (2011) Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitol 138: 1638–1663.
2. BlouinNA, LaneCE (2012) Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. Bioessays 34: 226–335.
3. WickettNJ, HonaasLA, WafulaEK, DasM, HuangK, et al. (2011) Transcriptomes of the parasitic plant family Orobanchaceae reveal surprising conservation of chlorophyll synthesis. Curr Biol 21: 2098–2104.
4. TillichM, KrauseK (2010) The ins and outs of editing and splicing of plastid RNAs: lessons from parasitic plants. Nat Biotechnol 27: 256–266.
5. AllenJF (2003) The function of genomes in bioenergetic organelles. Phil Trans R Soc Biol Sci 358: 19–37.
6. DorrellRG, HoweCJ (2012) What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. J Cell Sci 125: 1865–1875.
7. BarbrookAC, HoweCJ, PurtonS (2006) Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci 11: 101–108.
8. McFaddenGI, ReithME, MunhollandJ, Lang-UnnaschN (1996) Plastid in human parasites. Nature 381: 482.
9. FicheraME, RoosDS (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407–409.
10. LimL, McFaddenGI (2010) The evolution, metabolism and functions of the apicoplast. Phil Trans R Soc Biol Sci 365: 749–763.
11. JanouškovecJ, HorákA, OborníkM, LukešJ, KeelingPJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107: 10949–10954.
12. DorrellRG, HoweCJ (2012) Functional remodeling of RNA processing in replacement chloroplasts by pathways retained from their predecessors. Proc Natl Acad Sci USA 18879–18884.
13. HoweCJ, NisbetRER, BarbrookAC (2008) The remarkable chloroplast genome of dinoflagellates. J Exp Bot 59: 1035–1045.
14. ZaunerS, GreilingerD, LaatschT, KowallikKV, MaierUG (2004) Substitutional editing of transcripts from genes of cyanobacterial origin in the dinoflagellate Ceratium horridum. FEBS Lett 577: 535–538.
15. DangY, GreenBR (2010) Long transcripts from dinoflagellate chloroplast minicircles suggest “rolling circle” transcription. J Biol Chem 285: 5196–5203.
16. WangYL, MorseD (2006) Rampant polyuridylylation of plastid gene transcripts in the dinoflagellate Lingulodinium. Nucl Acids Res 34: 613–619.
17. AdlerBK, HarrisME, BertrandKI, HajdukSL (1991) Modification of Trypanosoma brucei mitochondrial ribosomal RNA by post-transcriptional 3′ polyuridine tail formation. Mol Cell Biol 11: 5878–5884.
18. LangeH, SementFM, CanadayJ, GagliardiD (2009) Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci 14: 497–504.
19. MooreRB, OborníkM, JanouškovecJ, ChrudimskyT, VancovaM, et al. (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451: 959–963.
20. OborníkM, ModryD, LukešM, Cernotikova-StribrnaE, CihlarJ, et al. (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163: 306–323.
21. CumboVR, BairdAH, MooreRB, NegriAP, NeilanBA, et al. (2012) Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist 164: 237–244.
22. JanouškovecJ, HorákA, BarottKL, RohwerFL, KeelingPJ (2012) Environmental distribution of coral-associated relatives of apicomplexan parasites. ISME J 7: 444–447.
23. JanouškovecJ, HorákA, BarottKL, RohwerFL, KeelingPJ (2012) Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr Biol 22: 518–519.
24. ParfreyLW, LahrDJ, KnollAH, KatzLA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108: 13624–13629.
25. ShihPM, MatzkeNJ (2013) Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci USA 110: 12355–12360.
26. OkamotoN, McFaddenGI (2008) The mother of all parasites. Future Microbiol 3: 391–395.
27. QuiggA, KotabováE, JarešováJ, KaňaR, SetlíkJ, et al. (2012) Photosynthesis in Chromera velia represents a simple system with high efficiency. PLoS One 7: 47036.
28. BottéCY, Yamaryo-BottéY, JanouškovecJ, RupasingheT, KeelingPJ, et al. (2011) Identification of plant-like galactolipids in Chromera velia, a photosynthetic relative of malaria parasites. J Biol Chem 286: 29893–29903.
29. KorenyL, SobotkaR, JanouškovecJ, KeelingPJ, OborníkM (2011) Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell 23: 3454–3462.
30. KotabováE, KaňaR, JarešováJ, PrášilO (2011) Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation. FEBS Lett 585: 1941–1945.
31. BottéCY, Yamaryo-BottéY, RupasingheTW, MullinKA, MacraeJI, et al. (2013) Atypical lipid composition in the purified relict plastid (apicoplast) of malaria parasites. Proc Natl Acad Sci USA 110: 7506–7511.
32. JanouškovecJ, SobotkaR, LaiDH, FlegontovP, KoníkP, et al. (2013) Split photosystem protein, linear-mapping topology, and growth of structural complexity in the plastid genome of Chromera velia. Mol Biol Evol 30: 2447–2462.
33. BarbrookAC, DorrellRG, BurrowsJ, PlenderleithLJ, NisbetRER, et al. (2012) Polyuridylylation and processing of transcripts from multiple gene minicircles in chloroplasts of the dinoflagellate Amphidinium carterae. Plant Mol Biol 79: 347–357.
34. HedtkeB, BörnerT, WeiheA (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis.. Science 277: 809–811.
35. LiereK, WeiheA, BörnerT (2011) The transcription machineries of plant mitochondria and chloroplasts: Composition, function, and regulation. J Plant Physiol 168: 1345–1360.
36. ZhelyazkovaP, SharmaCM, FörstnerKU, LiereK, VogelJ, et al. (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24: 123–136.
37. HanaokaM, KanamaruK, FujiwaraM, TakahashiH, TanakaK (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep 6: 545–550.
38. KahlauS, BockR (2008) Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20: 856–874.
39. NoordallyZB, IshiiK, AtkinsKA, WetherillSJ, KusakinaJ, et al. (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339: 1316–1319.
40. TengCY, DangY, DanneJC, WallerRF, GreenBR (2013) Mitochondrial genes of dinoflagellates are transcribed by a nuclear-encoded single-subunit RNA polymerase. PLoS One 8: 65387.
41. YinC, RichterU, BoernerT, WeiheA (2010) Evolution of plant phage-type RNA polymerases: the genome of the basal angiosperm Nuphar advena encodes two mitochondrial and one plastid phage-type RNA polymerases. BMC Evol Biol 10: 379.
42. ReeseMG (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comp Chem 26: 51–56.
43. DangY, GreenBR (2009) Substitutional editing of Heterocapsa triquetra chloroplast transcripts and a folding model for its divergent chloroplast 16S rRNA. Gene 442: 73–80.
44. KrauseK, MaierRM, KoferW, KrupinskaK, HerrmannRG (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: 1022–1030.
45. NakamuraT, FuruhashiY, HasegawaK, HashimotoH, WatanabeK, et al. (2003) Array-based analysis on tobacco plastid transcripts: preparation of a genomic microarray containing all genes and all intergenic regions. Plant Cell Physiol 44: 861–867.
46. StrittmatterG, KösselH (1984) Cotranscription and processing of 23S, 4.5S and 5S rRNA in chloroplasts from Zea mays. Nucl Acids Res 12: 7633–7647.
47. BarkanA, WalkerM, NolascoM, JohnsonD (1994) A nuclear mutation in maize blocks the processing and translation of several chloroplast messenger RNAs and provides evidence for the differential translation of alternative messenger RNA forms. EMBO J 13: 3170–3181.
48. NisbetRER, HillerRG, BarryER, SkeneP, BarbrookAC, et al. (2008) Transcript analysis of dinoflagellate plastid gene minicircles. Protist 159: 31–39.
49. HwangSR, TabitaFR (1991) Cotranscription, deduced primary structure, and expression of the chloroplast-encoded rbcL and rbcS genes of the marine diatom Cylindrotheca sp. strain N1. J Biol Chem 266: 6271–6279.
50. VeraA, MatsubayashiT, SugiuraM (1992) Active transcription from a promoter positioned within the coding region of a divergently oriented gene: the tobacco chloroplast rpl32 gene. Mol Gen Genet 233: 151–156.
51. NelsonMJ, DangYK, FilekE, ZhangZD, YuVWC, et al. (2007) Identification and transcription of transfer RNA genes in dinoflagellate plastid minicircles. Gene 392: 291–298.
52. ChaseCD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23: 81–90.
53. WuX, LiuM, DownieB, LiangC, JiG, et al. (2011) Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc Natl Acad Sci USA 108: 12533–12538.
54. WangET, SandbergR, LuoS, KhrebtukovaI, ZhangL, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 7221.
55. BachvaroffTR, ConcepcionGT, RogersCR, HermanEM, DelwicheCF (2004) Dinoflagellate expressed indicate massive transfer to the nuclear genome sequence tag data of chloroplast genes. Protist 155: 65–78.
56. HackettJD, YoonHS, SoaresMB, BonaldoMF, CasavantTL, et al. (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 14: 213–218.
57. FunkHT, BergS, KrupinskaK, MaierUG, KrauseK (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7: 45.
58. TarrSJ, NisbetRE, HoweCJ (2012) Transcript level responses of Plasmodium falciparum to antimycin A. Protist 163: 755–766.
59. Kyes S (2004) Reliable RNA Preparation for Plasmodium falciparum. In: Methods in Malaria Research, 4th ed. Virginia: Manassas.
60. PhillipsMJ, DelsucF, PennyD (2004) Genome-scale phylogeny and the detection of systematic biases. Mol Biol Evol 21: 1455–1458.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 1
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- GATA6 Is a Crucial Regulator of Shh in the Limb Bud
- Large Inverted Duplications in the Human Genome Form via a Fold-Back Mechanism
- Down-Regulation of eIF4GII by miR-520c-3p Represses Diffuse Large B Cell Lymphoma Development
- Genome Sequencing Highlights the Dynamic Early History of Dogs