Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection

Current Opinion in Plant Biology

Volumn 38, Issue , 2017, Pages 133-141

  Wang, Ming ^a   Thomas, Nicholas ^a   Jin, Hailing ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT RNA; SMALL INTERFERING RNA;

GENETICS; HOST PATHOGEN INTERACTION; PHYSIOLOGY; PLANT IMMUNITY; VIRULENCE;

HOST-PATHOGEN INTERACTIONS; PLANT IMMUNITY; RNA, PLANT; RNA, SMALL INTERFERING; VIRULENCE;

EID: 85019763900     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2017.05.003     Document Type: Review

References (80)

1. Oerke, E.C., Crop losses to pests. J. Agric. Sci. 144 (2006), 31–43.
2. Sharma, R.R., Singh, D., Singh, R., Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol. Control 50 (2009), 205–221.
3. Kader, A.A., Increasing food availability by reducing postharvest losses of fresh produce. Proceedings of the 5th International Postharvest Symposium vols. 1–3 (2005), 2169–2175.
4. Baulcombe, D., RNA silencing in plants. Nature 431 (2004), 356–363.
5. Kim, V.N., Han, J., Siomi, M.C., Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10 (2009), 126–139.
6. Vaten, A., Dettmer, J., Wu, S., Stierhof, Y.D., Miyashima, S., Yadav, S.R., Roberts, C.J., Campilho, A., Bulone, V., Lichtenberger, R., et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21 (2011), 1144–1155.
7. Brunkard, J.O., Zambryski, P.C., Plasmodesmata enable multicellularity: new insights into their evolution, biogenesis, and functions in development and immunity. Curr. Opin. Plant Biol. 35 (2016), 76–83.
8. Molnar, A., Melnyk, C.W., Bassett, A., Hardcastle, T.J., Dunn, R., Baulcombe, D.C., Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328 (2010), 872–875.
9. Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J.C., Voinnet, O., Small RNA duplexes function as mobile silencing signals between plant cells. Science 328 (2010), 912–916.
10. Voinnet, O., Vain, P., Angell, S., Baulcombe, D.C., Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95 (1998), 177–187.
11. Buhtz, A., Springer, F., Chappell, L., Baulcombe, D.C., Kehr, J., Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 53 (2008), 739–749.
12. Valiunas, V., Polosina, Y.Y., Miller, H., Potapova, I.A., Valiuniene, L., Doronin, S., Mathias, R.T., Robinson, R.B., Rosen, M.R., Cohen, I.S., et al. Connexin-specific cell-to-cell transfer of short interfering RNA by gap junctions. J. Physiol. 568 (2005), 459–468.
13. Lim, P.K., Bliss, S.A., Patel, S.A., Taborga, M., Dave, M.A., Gregory, L.A., Greco, S.J., Bryan, M., Patel, P.S., Rameshwar, P., Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 71 (2011), 1550–1560.
14. Katakowski, M., Buller, B., Wang, X.L., Rogers, T., Chopp, M., Functional microRNA is transferred between glioma cells. Cancer Res. 70 (2010), 8259–8263.
15. Aucher, A., Rudnicka, D., Davis, D.M., MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J. Immunol. 191 (2013), 6250–6260.
16. • Winston, W.M., Molodowitch, C., Hunter, C.P., Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295 (2002), 2456–2459 This work used mutant screening to identify regulators of systemic RNA interference. The group identified the systemic RNA interference-deficient (sid) gene SID-1 in C. elegans. This gene encoded a transmembrane protein that did not affect the initiation of RNAi, but was required for the propogation of systemic RNAi and RNA transport.
17. Feinberg, E.H., Hunter, C.P., Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301 (2003), 1545–1547.
18. Hinas, A., Wright, A.J., Hunter, C.P., SID-5 is an endosome-associated protein required for efficient systemic RNAi in C. elegans. Curr. Biol. 22 (2012), 1938–1943.
19. • Winston, W.M., Sutherlin, M., Wright, A.J., Feinberg, E.H., Hunter, C.P., Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 10565–10570 This study identified another systemic RNA interference-deficient (sid) gene SID-2 in C. elegans. SID-2 encodes a transmembrane protein expressed in the intestinal lumin. The sid-2 mutant failed to initiate RNAi after RNA soaking, while RNA injection and transgene expression still trigger systemic RNAi. This work suggested that SID-2 is required in the enviromental dsRNA uptake into the intestinal cells, but not in the systemic RNAi spreading.
20. Arroyo, J.D., Chevillet, J.R., Kroh, E.M., Ruf, I.K., Pritchard, C.C., Gibson, D.F., Mitchell, P.S., Bennett, C.F., Pogosova-Agadjanyan, E.L., Stirewalt, D.L., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 5003–5008.
21. Turchinovich, A., Weiz, L., Langheinz, A., Burwinkel, B., Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39 (2011), 7223–7233.
22. • Vickers, K.C., Palmisano, B.T., Shoucri, B.M., Shamburek, R.D., Remaley, A.T., MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 13 (2011), 423–433 The authors showed that the human plasma high-density lipoprotein (HDL) associates with miRNAs and protects them from degradation during transport to recipient cells. These miRNAs maintained the ability to silence genes in the recipient cells. This study provided an alternative strategy of vesicle-free miRNA transportation in the body fluid.
23. Cocucci, E., Meldolesi, J., Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 25 (2015), 364–372.
24. Raposo, G., Stoorvogel, W., Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200 (2013), 373–383.
25. Mittelbrunn, M., Sanchez-Madrid, F., Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell Biol. 13 (2012), 328–335.
26. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J., Lotvall, J.O., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 9, 2007 654–U672.
27. Kosaka, N., Iguchi, H., Ochiya, T., Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 101 (2010), 2087–2092.
28. Skog, J., Wurdinger, T., van Rijn, S., Meijer, D.H., Gainche, L., Sena-Esteves, M., Curry, W.T., Carter, B.S., Krichevsky, A.M., Breakefield, X.O., Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol., 10, 2008 1470–U1209.
29. • Thomou, T., Mori, M.A., Dreyfuss, J.M., Konishi, M., Sakaguchi, M., Wolfrum, C., Rao, T.N., Winnay, J.N., Garcia-Martin, R., Grinspoon, S.K., et al. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature 542 (2017), 450–455 In this study, Dicer gene in the mouse adipose tissue were specifically knocked out, the exosome associated circulating miRNAs were largetly reduced, suggesting that adipose tissue is a major source for circulating miRNAs. Moreover, they also showed that the adipose tissue derived exosomal circulating miRNA could regulate the expression of target genes in the liver tissue.
30. Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., Hristov, M., Koppel, T., Jahantigh, M.N., Lutgens, E., et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal., 2, 2009, ra81.
31. Weiberg, A., Bellinger, M., Jin, H.L., Conversations between kingdoms: small RNAs. Curr. Opin. Biotechnol. 32 (2015), 207–215.
32. Knip, M., Constantin, M.E., Thordal-Christensen, H., Trans-kingdom cross-talk: small RNAs on the move. PLoS Genet., 10, 2014, e1004602.
33. Weiberg, A., Wang, M., Bellinger, M., Jin, H., Small RNAs: a new paradigm in plant-microbe interactions. Annu. Rev. Phytopathol. 52 (2014), 495–516.
34. Wang, M., Weiberg, A., Jin, H., Pathogen small RNAs: a new class of effectors for pathogen attacks. Mol. Plant Pathol. 16 (2015), 219–223.
35. •• Weiberg, A., Wang, M., Lin, F.M., Zhao, H., Zhang, Z., Kaloshian, I., Huang, H.D., Jin, H., Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342 (2013), 118–123 The study provided the first example of naturally occurring cross-kingdom RNAi that employed as an aggressive virulence mechanism by an aggressive fungal pathogen B. cinerea. The fungal pathogen delivers sRNAs into host plant cells during infection and these fungal sRNAs silence host immunity genes by hijacking the host's Argonaute 1 protein. These mobile fungal sRNAs serve as a novel class of effectors to suppress host immunity.
36. Baulcombe, D., Plant science. Small RNA—the secret of noble rot. Science 342 (2013), 45–46.
37. • Wang, M., Weiberg, A., Dellota, E. Jr, Yamane, D., Jin, H., Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol., 2017, 1–8 The authors identified a B. cinerea sRNA effector, Bc-siR37, which was produced from gene coding region. Bc-siR37 was also delivered into Arabidopsis and associated with Argonaute 1 protein to silence its host target genes. They further showed that three of these target genes, At-WRKY7, At-FEI2 and At-PMR6 were involved in plant immunity against B. cinerea.
38. Kazan, K., Lyons, R., Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26 (2014), 2285–2309.
39. Ellendorff, U., Fradin, E.F., de Jonge, R., Thomma, B.P.H.J., RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60 (2009), 591–602.
40. •• Wang, M., Weiberg, A., Lin, F.M., Thomma, B.P., Huang, H.D., Jin, H., Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants, 2, 2016, 16151 This study demonstrated that cross-kingdom RNAi is bidirectional. sRNAs from transgenic plants can be delivered into pathogen cells and induce silencing of fungal genes. Moreover, this work also showed for the first time that fungal cells can directly take up sRNAs and double-stranded RNAs from the environment, which enables the development of RNA-based disease control tools. Direction application of fungal DCL-targeting RNAs largely reduced the fungal diseases on fruits, vegetables and flowers. This novel approach is more environmentally sustainable and friendly than current fungicides and is likely more socially acceptable than GMO-based approaches to disease management.
41. Zhu, S.L., Wang, S., Lin, Y., Jiang, P.Y., Cui, X.B., Wang, X.Y., Zhang, Y.B., Pan, W.Q., Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum. Parasit. Vectors, 9, 2016.
42. Lambertz, U., Ovando, M.E.O., Vasconcelos, E.J.R., Unrau, P.J., Myler, P.J., Reiner, N.E., Small RNAs derived from tRNAs and rRNAs are highly enriched in exosomes from both old and new world Leishmania providing evidence for conserved exosomal RNA packaging. BMC Genom., 16, 2015.
43. Zhu, L.H., Liu, J.T., Dao, J.W., Lu, K., Li, H., Gu, H.M., Liu, J.M., Feng, X.G., Cheng, G.F., Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite–host interactions. Sci. Rep., 6, 2016.
44. Twu, O., de Miguel, N., Lustig, G., Stevens, G.C., Vashisht, A.A., Wohlschlegel, J.A., Johnson, P.J., Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathog., 9, 2013.
45. •• Buck, A.H., Coakley, G., Simbari, F., McSorley, H.J., Quintana, J.F., Le Bihan, T., Kumar, S., Abreu-Goodger, C., Lear, M., Harcus, Y., et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat. Commun., 5, 2014, 5488 This group showed that mammalian parasitic nematodes secrete exosomes that containing nematode miRNAs into host cells. These nematode miRNAs silence host genes involved in inflammation and immunity. Their results suggest that animal parasites utilize exosomes to deliver small RNAs into host cells to modulate host immunity genes via cross-kingdom RNAi.
46. Peres da Silva, R., Puccia, R., Rodrigues, M.L., Oliveira, D.L., Joffe, L.S., Cesar, G.V., Nimrichter, L., Goldenberg, S., Alves, L.R., Extracellular vesicle-mediated export of fungal RNA. Sci. Rep., 5, 2015, 7763.
47. • Lin, S., Cheng, S., Song, B., Zhong, X., Lin, X., Li, W., Li, L., Zhang, Y., Zhang, H., Ji, Z., et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350 (2015), 691–694 Genome sequencing of the endosymbiont dinoflagellate Symbiodinium kawagutii revealed a group of miRNAs that have the potential to target host coral genes as well as similar genes of its own, suggesting that these miRNAs may regulate gene expression in both the symbiont and the host.
48. Mayoral, J.G., Hussain, M., Joubert, D.A., Iturbe-Ormaetxe, I., O'Neill, S.L., Asgari, S., Wolbachia small noncoding RNAs and their role in cross-kingdom communications. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 18721–18726.
49. Nunes, C.C., Dean, R.A., Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies. Mol. Plant Pathol. 13 (2012), 519–529.
50. Nowara, D., Gay, A., Lacomme, C., Shaw, J., Ridout, C., Douchkov, D., Hensel, G., Kumlehn, J., Schweizer, P., HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22 (2010), 3130–3141.
51. •• Huang, G.Z., Allen, R., Davis, E.L., Baum, T.J., Hussey, R.S., Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 14302–14306 This work showed that transgenic Arabidopsis plants expressing dsRNAs that target a nematode parasitism gene were resistant against root knot nematodes. This was the first report of host-induced gene silencing for plant protection.
52. •• Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P., Chen, X.Y., Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25 (2007), 1307–1313 In this paper, the cotton bollworm (Helicoverpa armigera) insect pest was fed with cotton leaves expressing dsRNAs that target a cytochrome P450 gene (CYP6AE14), which is important for cotton bollworm tolerance to gossypol. Suppression of this gene impaired the larval growth, supporting that host-induced gene silencing is also efficient for plant protection against insect pests.
53. •• Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25 (2007), 1322–1326 The authors showed that injecting dsRNAs that targeting several coleopteran insect pest genes induced gene silencing and led to significant lavarl mortality. Moreover, in planta expression of insect gene-targeting dsRNAs significantly protected plants from western corn rootworm (WCR) Diabrotica virgifera virgifera LeConte.
54. Garbian, Y., Maori, E., Kalev, H., Shafir, S., Sela, I., Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population. PLoS Pathog., 8, 2012.
55. •• Zhang, T., Zhao, Y.L., Zhao, J.H., Wang, S., Jin, Y., Chen, Z.Q., Fang, Y.Y., Hua, C.L., Ding, S.W., Guo, H.S., Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants, 2, 2016, 16153 This work showed that several abundant cotton endogenous miRNAs were delivered into fungal pathogen Verticillium dahliae to induce trans-kingdom RNAi and suppressed pathogen virulence.
56. •• LaMonte, G., Philip, N., Reardon, J., Lacsina, J.R., Majoros, W., Chapman, L., Thornburg, C.D., Telen, M.J., Ohler, U., Nicchitta, C.V., et al. Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12 (2012), 187–199 Sickle cell erythrocytes of anemia patients accumulate higher levels of miR-451 and let-7i, which are transferred into parasite P. falciparum cells. These miRNAs are fused with targeted parasite mRNAs at 5′ UTR region and form chimeric structures that suppress mRNA translation. This work provided evidence that animal hosts also export sRNAs into interacting parasite cells and suppress its virulence.
57. Duraisingh, M.T., Lodish, H.F., Sickle cell microRNAs inhibit the malaria parasite. Cell Host Microbe 12 (2012), 127–128.
58. • Liu, S., da Cunha, A.P., Rezende, R.M., Cialic, R., Wei, Z., Bry, L., Comstock, L.E., Gandhi, R., Weiner, H.L., The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe 19 (2016), 32–43 In this study, the miRNAs in the mouse and human feces have been identified. These host fecal miRNAs entered the bacteria cells and regulated the transcript level of gut bacteria targets, thus affected the growth of gut bacteria.
59. Koch, A., Kumar, N., Weber, L., Keller, H., Imani, J., Kogel, K.H., Host-induced gene silencing of cytochrome P450 lanosterol C14 alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 19324–19329.
60. Vega-Arreguin, J.C., Jalloh, A., Bos, J.I., Moffett, P., Recognition of an Avr3a homologue plays a major role in mediating nonhost resistance to Phytophthora capsici in Nicotiana species. Mol. Plant–Microbe Interact. 27 (2014), 770–780.
61. Jahan, S.N., Asman, A.K.M., Corcoran, P., Fogelqvist, J., Vetukuri, R.R., Dixelius, C., Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J. Exp. Bot. 66 (2015), 2785–2794.
62. Whangbo, J.S., Hunter, C.P., Environmental RNA interference. Trends Genet. 24 (2008), 297–305.
63. McEwan, D.L., Weisman, A.S., Huntert, C.P., Uptake of extracellular double-stranded RNA by SID-2. Mol. Cell 47 (2012), 746–754.
64. Jose, A.M., Kim, Y.A., Leal-Ekman, S., Hunter, C.P., Conserved tyrosine kinase promotes the import of silencing RNA into Caenorhabditis elegans cells. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 14520–14525.
65. •• Koch, A., Biedenkopf, D., Furch, A., Weber, L., Rossbach, O., Abdellatef, E., Linicus, L., Johannsmeier, J., Jelonek, L., Goesmann, A., et al. An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathog., 12, 2016, e1005901 This study demonstrated that RNAs sprayed on the surface of barley leaves are taken up by the plant cells and then travel into fungal pathogen Fusarium graminearum cells to silence pathogen virulence genes. The RNAs can also systemically move into untreated leaf parts to inhibit fungal infection. This study showed that RNA spray induced gene silencing is an effective tool for plant protection against fungal pathogens in a monocot.
66. Wang, M., Jin, H., Spray-induced gene silencing: a powerful innovative strategy for crop protection. Trends Microbiol. 25 (2017), 4–6.
67. •• Mitter, N., Worrall, E.A., Robinson, K.E., Li, P., Jain, R.G., Taochy, C., Fletcher, S.J., Carroll, B.J., Lu, G.Q., Xu, Z.P., Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants, 3, 2017, 16207 This report showed that topical application of dsRNAs on the plant leaves can protect the plants from viral infection. More importantly, the protection can be significantly extended when loading the dsRNAs on layered double hydroxide (LDH) clay nanosheets, because the LDH clay nanosheets protect dsRNAs from degradation and from being washed off from plant leaves. This was the first example of using nanosheets to deliver dsRNAs for plant protection.
68. • Saleh, M.C., van Rij, R.P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P.H., Andino, R., The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol., 8, 2006 793–U719 Genome-wide genetic screening identified several receptors in the endocytosis pathways that are involved in dsRNA uptake in Drosophila melanogaster S2 cells. The authors showed that homologs of these genes in C. elegans are also essential for the spread of systemic RNAi, which suggests that endocytosis-mediated dsRNA uptake pathway might be evolutionarily conserved.
69. Ivashuta, S., Zhang, Y.J., Wiggins, B.E., Ramaseshadri, P., Segers, G.C., Johnson, S., Meyer, S.E., Kerstetter, R.A., McNulty, B.C., Bolognesi, R., et al. Environmental RNAi in herbivorous insects. RNA 21 (2015), 840–850.
70. Pridgeon, J.W., Zhao, L.M., Becnel, J.J., Strickman, D.A., Clark, G.G., Linthicum, K.J., Topically applied AaeIAP1 double-stranded RNA kills female adults of Aedes aegypti. J. Med. Entomol. 45 (2008), 414–420.
71. Wang, Y.B., Zhang, H., Li, H.C., Miao, X.X., Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS One, 6, 2011.
72. Killiny, N., Hajeri, S., Tiwari, S., Gowda, S., Stelinski, L.L., Double-stranded RNA uptake through topical application, mediates silencing of five CYP4 genes and suppresses insecticide resistance in Diaphorina citri. PLoS One, 9, 2014.
73. San Miguel, K., Scott, J.G., The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide. Pest Manag. Sci. 72 (2016), 801–809.
74. • Li, H., Guan, R., Guo, H., Miao, X., New insights into an RNAi approach for plant defence against piercing-sucking and stem-borer insect pests. Plant Cell Environ. 38 (2015), 2277–2285 Rice plants take up dsRNAs when their roots were soaked in dsRNA solution. These rice plants exhibit enhanced disease resistance against insect pest. This study showed that application of dsRNA through irrigation could be a potential plant protection strategy.
75. Gong, L., Chen, Y., Hu, Z., Hu, M.Y., Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions. PLoS One, 8, 2013.
76. Ladewig, K., Xu, Z.P., Lu, G.Q., Layered double hydroxide nanoparticles in gene and drug delivery. Expert Opin. Drug Deliv. 6 (2009), 907–922.
77. Kanasty, R., Dorkin, J.R., Vegas, A., Anderson, D., Delivery materials for siRNA therapeutics. Nat. Mater. 12 (2013), 967–977.
78. Magan, N., Aldred, D., Post-harvest control strategies: minimizing mycotoxins in the food chain. Int. J. Food Microbiol. 119 (2007), 131–139.
79. Sarkies, P., Miska, E.A., Small RNAs break out: the molecular cell biology of mobile small RNAs. Nat. Rev. Mol. Cell Biol. 15 (2014), 525–535.
80. •• Lewsey, M.G., Hardcastle, T.J., Melnyk, C.W., Molnar, A., Valli, A., Urich, M.A., Nery, J.R., Baulcombe, D.C., Ecker, J.R., Mobile small RNAs regulate genome-wide DNA methylation. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E801–E810 Genome-wide profiling of grafted Arabidopsis root materials has identified sRNAs that are overlapped in grafting sets of C24/C24 (shoot/root), C24/Col, Col/Col, and C24/dcl234 but not in dcl234/dcl234, suggesting that these sRNAs are shoot derived mobile sRNAs. These mobile sRNAs induce root DNA methylation at thousands of different loci, most of which are in non-CG contexts. This study provides an example of systemically mobile 24 nt sRNAs that direct DNA methylation.