Small RNAs-the secret agents in the plant-pathogen interactions

Current Opinion in Plant Biology

Volumn 26, Issue , 2015, Pages 87-94

  Weiberg, Arne ^a   Jin, Hailing ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA;

SMALL INTERFERING RNA;

GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; PARASITOLOGY; PLANT; VIRULENCE;

HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; PLANTS; RNA, SMALL INTERFERING; VIRULENCE;

EID: 84932630904     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2015.05.033     Document Type: Review

References (86)

1. Seo J.K., Wu J., Lii Y., Li Y., Jin H. Contribution of small RNA pathway components in plant immunity. Mol Plant Microbe Interact 2013, 26:617-625.
2. Staiger D., Korneli C., Lummer M., Navarro L. Emerging role for RNA-based regulation in plant immunity. New Phytol 2013, 197:394-404.
3. Weiberg A., Wang M., Bellinger M., Jin H. Small RNAs: a new paradigm in plant-microbe interactions. Annu Rev Phytopathol 2014, 52:495-516.
4. Yang L., Huang H. Roles of small RNAs in plant disease resistance. J Integr Plant Biol 2014, 56:962-970.
5. Chacko N., Lin X. Non-coding RNAs in the development and pathogenesis of eukaryotic microbes. Appl Microbiol Biotechnol 2013, 97:7989-7997.
6. Wang M., Weiberg A., Jin H. Pathogen small RNAs: a new class of effectors for pathogen attacks. Mol Plant Pathol 2015, 16:219-223.
7. Brosnan C.A., Voinnet O. Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr Opin Plant Biol 2011, 14:580-587.
8. Melnyk C.W., Molnar A., Bassett A., Baulcombe D.C. Mobile 24nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr Biol 2011, 21:1678-1683.
9. Molnar A., Melnyk C., Baulcombe D.C. Silencing signals in plants: a long journey for small RNAs. Genome Biol 2011, 12:215.
10. Sarkies P., Miska E.A. Small RNAs break out: the molecular cell biology of mobile small RNAs. Nat Rev Mol Cell Biol 2014, 15:525-535.
11. Knip M., Constantin M.E., Thordal-Christensen H. Trans-kingdom cross-talk: small RNAs on the move. PLoS Genet 2014, 10:e1004602.
12. Weiberg A., Bellinger M., Jin H. Conversations between kingdoms: small RNAs. Curr Opin Biotechnol 2015, 32C:207-215.
13. Koch A., Kogel K.H. New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol J 2014, 12:821-831.
14. 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 2012, 13:519-529.
15. 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 2014, 5:5488.
16. 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 2013, 342:118-123.
17. Jin H. Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 2008, 582:2679-2684.
18. Katiyar-Agarwal S., Jin H. Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 2010, 48:225-246.
19. Padmanabhan C., Zhang X., Jin H. Host small RNAs are big contributors to plant innate immunity. Curr Opin Plant Biol 2009, 12:465-472.
20. Ruiz-Ferrer V., Voinnet O. Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 2009, 60:485-510.
21. Fahlgren N., Howell M.D., Kasschau K.D., Chapman E.J., Sullivan C.M., Cumbie J.S., Givan S.A., Law T.F., Grant S.R., Dangl J.L., et al. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2007, 2:e219.
22. Li Y., Zhang Q., Zhang J., Wu L., Qi Y., Zhou J.M. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 2010, 152:2222-2231.
23. Zhang W., Gao S., Zhou X., Chellappan P., Chen Z., Zhou X., Zhang X., Fromuth N., Coutino G., Coffey M., et al. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 2011, 75:93-105.
24. Zhang X., Zhao H., Gao S., Wang W.C., Katiyar-Agarwal S., Huang H.D., Raikhel N., Jin H. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 2011, 42:356-366.
25. Katiyar-Agarwal S., Gao S., Vivian-Smith A., Jin H. A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 2007, 21:3123-3134.
26. Katiyar-Agarwal S., Morgan R., Dahlbeck D., Borsani O., Villegas A., Zhu J.K., Staskawicz B.J., Jin H. A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci U S A 2006, 103:18002-18007.
27. Li F., Pignatta D., Bendix C., Brunkard J.O., Cohn M.M., Tung J., Sun H., Kumar P., Baker B. MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci U S A 2012, 109:1790-1795.
28. Shivaprasad P.V., Chen H.M., Patel K., Bond D.M., Santos B.A., Baulcombe D.C. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 2012, 24:859-874.
29. Zhai J., Jeong D.H., De Paoli E., Park S., Rosen B.D., Li Y., Gonzalez A.J., Yan Z., Kitto S.L., Grusak M.A., et al. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 2011, 25:2540-2553.
30. Zhu Q.H., Fan L., Liu Y., Xu H., Llewellyn D., Wilson I. miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLOS ONE 2013, 8:e84390.
31. Navarro L., Jay F., Nomura K., He S.Y., Voinnet O. Suppression of the microRNA pathway by bacterial effector proteins. Science 2008, 321:964-967.
32. Deleris A., Gallego-Bartolome J., Bao J., Kasschau K.D., Carrington J.C., Voinnet O. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 2006, 313:68-71.
33. Vaucheret H. Plant ARGONAUTES. Trends Plant Sci 2008, 13:350-358.
34. Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M., Voinnet O., Jones J.D. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312:436-439.
35. Zhang X., Niu D., Carbonell A., Wang A., Lee A., Tun V., Wang Z., Carrington J.C., Chang C.E., Jin H. ARGONAUTE PIWI domain and microRNA duplex structure regulate small RNA sorting in Arabidopsis. Nat Commun 2014, 5:5468.
36. Ghildiyal M., Xu J., Seitz H., Weng Z., Zamore P.D. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. RNA 2010, 16:43-56.
37. Kang S.M., Choi J.W., Hong S.H., Lee H.J. Up-regulation of microRNA* strands by their target transcripts. Int J Mol Sci 2013, 14:13231-13240.
38. Ellendorff U., Fradin E.F., de Jonge R., Thomma B.P. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 2009, 60:591-602.
39. Boccara M., Sarazin A., Thiebeauld O., Jay F., Voinnet O., Navarro L., Colot V. The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathog 2014, 10:e1003883.
40. Boccara M., Sarazin A., Thiebeauld O., Jay F., Voinnet O., Navarro L., Colot V. Correction: the Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathog 2015, 11:e1004814.
41. Dowen R.H., Pelizzola M., Schmitz R.J., Lister R., Dowen J.M., Nery J.R., Dixon J.E., Ecker J.R. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 2012, 109:E2183-E2191.
42. Yu A., Lepere G., Jay F., Wang J., Bapaume L., Wang Y., Abraham A.L., Penterman J., Fischer R.L., Voinnet O., et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci U S A 2013, 110:2389-2394.
43. Le T.N., Schumann U., Smith N.A., Tiwari S., Au P.C., Zhu Q.H., Taylor J.M., Kazan K., Llewellyn D.J., Zhang R., et al. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biol 2014, 15:458.
44. Lopez A., Ramirez V., Garcia-Andrade J., Flors V., Vera P. The RNA silencing enzyme RNA polymerase v is required for plant immunity. PLoS Genet 2011, 7:e1002434.
45. Luna E., Bruce T.J., Roberts M.R., Flors V., Ton J. Next-generation systemic acquired resistance. Plant Physiol 2012, 158:844-853.
46. Filiatrault M.J., Stodghill P.V., Bronstein P.A., Moll S., Lindeberg M., Grills G., Schweitzer P., Wang W., Schroth G.P., Luo S., et al. Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 2010, 192:2359-2372.
47. Jiang R.P., Tang D.J., Chen X.L., He Y.Q., Feng J.X., Jiang B.L., Lu G.T., Lin M., Tang J.L. Identification of four novel small non-coding RNAs from Xanthomonas campestris pathovar campestris. BMC Genomics 2010, 11:316.
48. Liang H., Zhao Y.T., Zhang J.Q., Wang X.J., Fang R.X., Jia Y.T. Identification and functional characterization of small non-coding RNAs in Xanthomonas oryzae pathovar oryzae. BMC Genomics 2011, 12:87.
49. Schmidtke C., Findeiss S., Sharma C.M., Kuhfuss J., Hoffmann S., Vogel J., Stadler P.F., Bonas U. Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 2012, 40:2020-2031.
50. Wilms I., Overloper A., Nowrousian M., Sharma C.M., Narberhaus F. Deep sequencing uncovers numerous small RNAs on all four replicons of the plant pathogen Agrobacterium tumefaciens. RNA Biol 2012, 9:446-457.
51. Schmidtke C., Abendroth U., Brock J., Serrania J., Becker A., Bonas U. Small RNA sX13: a multifaceted regulator of virulence in the plant pathogen Xanthomonas. PLoS Pathog 2013, 9:e1003626.
52. Chao N.X., Wei K., Chen Q., Meng Q.L., Tang D.J., He Y.Q., Lu G.T., Jiang B.L., Liang X.X., Feng J.X., et al. The rsmA-like gene rsmA(Xcc) of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Mol Plant Microbe Interact 2008, 21:411-423.
53. Wilms I., Moller P., Stock A.M., Gurski R., Lai E.M., Narberhaus F. Hfq influences multiple transport systems and virulence in the plant pathogen Agrobacterium tumefaciens. J Bacteriol 2012, 194:5209-5217.
54. Nunes C.C., Gowda M., Sailsbery J., Xue M., Chen F., Brown D.E., Oh Y., Mitchell T.K., Dean R.A. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genomics 2011, 12:288.
55. Raman V., Simon S.A., Romag A., Demirci F., Mathioni S.M., Zhai J., Meyers B.C., Donofrio N.M. Physiological stressors and invasive plant infections alter the small RNA transcriptome of the rice blast fungus, Magnaporthe oryzae. BMC Genomics 2013, 14:326.
56. Fahlgren N., Bollmann S.R., Kasschau K.D., Cuperus J.T., Press C.M., Sullivan C.M., Chapman E.J., Hoyer J.S., Gilbert K.B., Grunwald N.J., et al. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLOS ONE 2013, 8:e77181.
57. Vetukuri R.R., Asman A.K., Tellgren-Roth C., Jahan S.N., Reimegard J., Fogelqvist J., Savenkov E., Soderbom F., Avrova A.O., Whisson S.C., et al. Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLOS ONE 2012, 7:e51399.
58. Whisson S., Vetukuri R., Avrova A., Dixelius C. Can silencing of transposons contribute to variation in effector gene expression in Phytophthora infestans?. Mob Genet Elements 2012, 2:110-114.
59. Qutob D., Chapman B.P., Gijzen M. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat Commun 2013, 4:1349.
60. Koch A., Kumar N., Weber L., Keller H., Imani J., Kogel K.H. Host-induced gene silencing of cytochrome P450 lanosterol C14alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci U S A 2013, 110:19324-19329.
61. 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 2010, 22:3130-3141.
62. 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 2012, 12:187-199.
63. Liu H., Wang X., Wang H.D., Wu J., Ren J., Meng L., Wu Q., Dong H., Wu J., Kao T.Y., et al. Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat Commun 2012, 3:1073.
64. 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 2014, 111:18721-18726.
65. Cheng G., Luo R., Hu C., Cao J., Jin Y. Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 2013, 140:1751-1761.
66. Garcia-Silva M.R., das Neves R.F., Cabrera-Cabrera F., Sanguinetti J., Medeiros L.C., Robello C., Naya H., Fernandez-Calero T., Souto-Padron T., de Souza W., et al. Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitol Res 2014, 113:285-304.
67. Quintana J.F., Makepeace B.L., Babayan S.A., Ivens A., Pfarr K.M., Blaxter M., Debrah A., Wanji S., Ngangyung H.F., Bah G.S., et al. Extracellular Onchocerca-derived small RNAs in host nodules and blood. Parasit Vectors 2015, 8:58.
68. Katoch R., Sethi A., Thakur N., Murdock L.L. RNAi for insect control: current perspective and future challenges. Appl Biochem Biotechnol 2013, 171:847-873.
69. Lilley C.J., Davies L.J., Urwin P.E. RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 2012, 139:630-640.
70. Zhang H., Li H.C., Miao X.X. Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci 2013, 20:15-30.
71. 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 2007, 25:1322-1326.
72. Alakonya A., Kumar R., Koenig D., Kimura S., Townsley B., Runo S., Garces H.M., Kang J., Yanez A., David-Schwartz R., et al. Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 2012, 24:3153-3166.
73. Kim G., LeBlanc M.L., Wafula E.K., dePamphilis C.W., Westwood J.H. Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 2014, 345:808-811.
74. LeBlanc M., Kim G., Patel B., Stromberg V., Westwood J. Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol 2013, 200:1225-1233.
75. Westwood J.H., Roney J.K., Khatibi P.A., Stromberg V.K. RNA translocation between parasitic plants and their hosts. Pest Manage Sci 2009, 65:533-539.
76. Aidoo M., Terlouw D.J., Kolczak M.S., McElroy P.D., ter Kuile F.O., Kariuki S., Nahlen B.L., Lal A.A., Udhayakumar V. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 2002, 359:1311-1312.
77. 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 2007, 25:1307-1313.
78. Zhang J., Khan S.A., Hasse C., Ruf S., Heckel D.G., Bock R. Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 2015, 347:991-994.
79. Ding Y., Robinson D.G., Jiang L. Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol 2014, 29:107-115.
80. Drakakaki G., Dandekar A. Protein secretion: how many secretory routes does a plant cell have?. Plant Sci 2013, 203-204:74-78.
81. Baisa G.A., Mayers J.R., Bednarek S.Y. Budding and braking news about clathrin-mediated endocytosis. Curr Opin Plant Biol 2013, 16:718-725.
82. Fan L., Li R., Pan J., Ding Z., Lin J. Endocytosis and its regulation in plants. Trends Plant Sci 2015, 20:388-397.
83. Huckelhoven R. Transport and secretion in plant-microbe interactions. Curr Opin Plant Biol 2007, 10:573-579.
84. Freidit Frey N., Robatzek S. Trafficking vesicles: pro or contra pathogens?. Curr Opin Plant Biol 2009, 12:437-443.
85. Kale S.D., Tyler B.M. Entry of oomycete and fungal effectors into plant and animal host cells. Cell Microbiol 2011, 13:1839-1848.
86. Mittelbrunn M., Sanchez-Madrid F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 2012, 13:328-335.