Trans-kingdom Cross-Talk: Small RNAs on the Move
This review focuses on the mobility of small RNA (sRNA) molecules from the perspective of trans-kingdom gene silencing. Mobility of sRNA molecules within organisms is a well-known phenomenon, facilitating gene silencing between cells and tissues. sRNA signals are also transmitted between organisms of the same species and of different species. Remarkably, in recent years many examples of RNA-signal exchange have been described to occur between organisms of different kingdoms. These examples are predominantly found in interactions between hosts and their pathogens, parasites, and symbionts. However, they may only represent the tip of the iceberg, since the emerging picture suggests that organisms in biological niches commonly exchange RNA-silencing signals. In this case, we need to take this into account fully to understand how a given biological equilibrium is obtained. Despite many observations of trans-kingdom RNA signal transfer, several mechanistic aspects of these signals remain unknown. Such RNA signal transfer is already being exploited for practical purposes, though. Pathogen genes can be silenced by plant-produced sRNAs designed to affect these genes. This is also known as Host-Induced Genes Silencing (HIGS), and it has the potential to become an important disease-control method in the future.
Vyšlo v časopise:
Trans-kingdom Cross-Talk: Small RNAs on the Move. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004602
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Review
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https://doi.org/10.1371/journal.pgen.1004602
Souhrn
This review focuses on the mobility of small RNA (sRNA) molecules from the perspective of trans-kingdom gene silencing. Mobility of sRNA molecules within organisms is a well-known phenomenon, facilitating gene silencing between cells and tissues. sRNA signals are also transmitted between organisms of the same species and of different species. Remarkably, in recent years many examples of RNA-signal exchange have been described to occur between organisms of different kingdoms. These examples are predominantly found in interactions between hosts and their pathogens, parasites, and symbionts. However, they may only represent the tip of the iceberg, since the emerging picture suggests that organisms in biological niches commonly exchange RNA-silencing signals. In this case, we need to take this into account fully to understand how a given biological equilibrium is obtained. Despite many observations of trans-kingdom RNA signal transfer, several mechanistic aspects of these signals remain unknown. Such RNA signal transfer is already being exploited for practical purposes, though. Pathogen genes can be silenced by plant-produced sRNAs designed to affect these genes. This is also known as Host-Induced Genes Silencing (HIGS), and it has the potential to become an important disease-control method in the future.
Zdroje
1. IzantJG, WeintraubH (1984) Inhibition of thymidine kinase gene expression by anti-sense RNA: molecular approach to genetic analysis. Cell 36: 1007–1015.
2. FireA, XuS, MontgomeryMK, KostasSA, DriverSE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.
3. ChangS-S, ZhangZ, LiuY (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66: 305–323.
4. AxtellMJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64: 137–159.
5. WilsonRC, DoudnaJA (2013) Molecular mechanisms of RNA interference. Annu Rev Biophys 42: 217–239.
6. CastelSE, MartienssenR (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100–112.
7. Martínez de AlbaAE, Elvira-MatelotE, VaucheretH (2013) Gene silencing in plants: a diversity of pathways. Biochim Biophys Acta 1829: 1300–1308.
8. ShabalinaSA, KooninEV (2008) Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 23: 578–587.
9. CeruttiH, Casas-MollanoJA (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50: 81–99.
10. LodishHF, ZhouB, LiuG, ChenC-Z (2008) Micromanagement of the immune system by microRNAs. Nat Rev Immunol 8: 120–130.
11. MelnikBC, JohnSM, SchmitzG (2013) Milk is not just food but most likely a genetic transfection system activating mTORC1 signaling for postnatal growth. Nutr J 12: 103.
12. TomilovA, TomilovaNB, WroblewskiT, MichelmoreR, YoderJI (2008) Trans-specific gene silencing between host and parasitic plants. Plant J 56: 389–397.
13. LiangH, ZenK, ZhangJ, ZhangC-Y, ChenX (2013) New roles for microRNAs in cross-species communication. RNA Biol 10: 367–370.
14. Garcia-SilvaMR, das NevesRFC, Cabrera-CabreraF, SanguinettiJ, MedeirosLC, et al. (2014) Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitol Res 113: 285–304.
15. ChengG, LuoR, HuC, CaoJ, JinY (2013) Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 140: 1751–1761.
16. LaMonteG, PhilipN, ReardonJ, LacsinaJR, MajorosW, et al. (2012) Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12: 187–199.
17. LiuH, WangX, WangH-D, WuJJ, RenJ, et al. (2012) Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat Commun 3: 1073.
18. NowaraD, GayA, LacommeC, ShawJ, RidoutC, et al. (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22: 3130–3141.
19. KochA, KumarN, WeberL, KellerH, ImaniJ, et al. (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci U S A 110: 19324–19329.
20. GhagSB, ShekhawatUKS, GanapathiTR (2014) Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant Biotechnol J 12: 541–553.
21. HelberN, WippelK, SauerN, SchaarschmidtS, HauseB, et al. (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23: 3812–3823.
22. IbrahimHMM, AlkharoufNW, MeyerSLF, AlyMM, Gamal El-DinAEKY, et al. (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol 127: 90–99.
23. WeibergA, WangM, LinF-M, ZhaoH, ZhangZ, et al. (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342: 118–123.
24. MaoY-B, CaiW, WangJ-W, HongG, TaoX, et al. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25: 1307–1313.
25. NunesCC, DeanRA (2012) Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies. Mol Plant Pathol 13: 519–529.
26. TinocoMLP, DiasBBA, Dall'AsttaRC, PamphileJA, AragãoFJL (2010) In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol 8: 27.
27. YinC, JurgensonJE, HulbertSH (2011) Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Mol Plant Microbe Interact 24: 554–561.
28. Vega-ArreguínJC, JallohA, BosJI, MoffettP (2014) Recognition of an Avr3a homologue plays a major role in mediating non-host resistance to Phytophthora capsici in Nicotiana species. Mol Plant Microbe Interact 1–40.
29. ZhangM, WangQ, XuK, MengY, QuanJ, et al. (2011) Production of dsRNA sequences in the host plant is not sufficient to initiate gene silencing in the colonizing oomycete pathogen Phytophthora parasitica. PLoS ONE 6: e28114.
30. BaumJa, BogaertT, ClintonW, HeckGR, FeldmannP, et al. (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25: 1322–1326.
31. BaumJ, PapenfussAT, MairGR, JanseCJ, VlachouD, et al. (2009) Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res 37: 3788–3798.
32. ValadiH, EkströmK, BossiosA, SjöstrandM, LeeJJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654–659.
33. TurchinovichA, WeizL, LangheinzA, BurwinkelB (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39: 7223–7233.
34. VickersKC, PalmisanoBT, ShoucriBM, ShamburekRD, RemaleyAT (2011) MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13: 423–433.
35. WangK, ZhangS, WeberJ, BaxterD, GalasDJ (2010) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 38: 7248–7259.
36. ZhangY, LiuD, ChenX, LiJ, LiL, et al. (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39: 133–144.
37. ArroyoJD, ChevilletJR, KrohEM, RufIK, PritchardCC, et al. (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 108: 5003–5008.
38. WinstonWM, MolodowitchC, HunterCP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295: 2456–2459.
39. McEwanDL, WeismanAS, HunterCP (2012) Uptake of extracellular double-stranded RNA by SID-2. Mol Cell 47: 746–754.
40. SarkiesP, MiskaE (2013) Molecular biology. Is there social RNA? Science 341: 467–468.
41. WolfrumC, ShiS, JayaprakashKN, JayaramanM, WangG, et al. (2007) Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat Biotechnol 25: 1149–1157.
42. UlvilaJ, ParikkaM, KleinoA, SormunenR, EzekowitzRA, et al. (2006) Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 281: 14370–14375.
43. ThéryC (2011) Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3: 15.
44. RaposoG, StoorvogelW (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200: 373–383.
45. GibbingsDJ, CiaudoC, ErhardtM, VoinnetO (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11: 1143–1149.
46. LeeYS, PressmanS, AndressAP, KimK, WhiteJL, et al. (2009) Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11: 1150–1156.
47. KosakaN, IguchiH, YoshiokaY, TakeshitaF, MatsukiY, et al. (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285: 17442–17452.
48. TrajkovicK, HsuC, ChiantiaS, RajendranL, WenzelD, et al. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244–1247.
49. Villarroya-BeltriC, Gutiérrez-VázquezC, Sánchez-CaboF, Pérez-HernándezD, VázquezJ, et al. (2013) Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun 4: 2980.
50. AvinoamO, FridmanK, ValansiC, AbutbulI, Zeev-Ben-MordehaiT, et al. (2011) Conserved eukaryotic fusogens can fuse viral envelopes to cells. Science 332: 589–592.
51. RecordM (2014) Intercellular communication by exosomes in placenta: A possible role in cell fusion? Placenta 35: 297–302.
52. NielsenME, FeechanA, BöhleniusH, UedaT, Thordal-ChristensenH (2012) Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci U S A 109: 11443–11448.
53. MeyerD, PajonkS, MicaliC, O'ConnellR, Schulze-LefertP (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57: 986–999.
54. AnQ, HückelhovenR, KogelK-H, van BelAJE (2006) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8: 1009–1019.
55. ZhangW, PedersenC, KwaaitaalM, GregersenPERL, MørchSM, et al. (2012) Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol Plant Pathol 13: 1110–1119.
56. MolnarA, MelnykCW, BassettA, HardcastleTJ, DunnR, et al. (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872–875.
57. BrosnanCa, MitterN, ChristieM, SmithNA, WaterhousePM, et al. (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc Natl Acad Sci U S A 104: 14741–14746.
58. SchwachF, VaistijFE, JonesL, BaulcombeDC (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138: 1842–1852.
59. TomoyasuY, MillerSC, TomitaS, SchoppmeierM, GrossmannD, et al. (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 9: R10.
60. GrimsonA, FarhKK-H, JohnstonWK, Garrett-EngeleP, LimLP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91–105.
61. LiuQ, WangF, AxtellMJ (2014) Analysis of complementarity requirements for plant microRNA targeting using a Nicotiana benthamiana quantitative transient assay. Plant Cell 26: 741–753.
62. PanwarV, McCallumB, BakkerenG (2013) Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol Biol 81: 595–608.
63. PitinoM, ColemanAD, MaffeiME, RidoutCJ, HogenhoutSA (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 6: e25709.
64. Cavalier-SmithT (1998) A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73: 203–266.
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