Role of small RNAs in the interaction between Arabidopsis and Pseudomonas syringae

Abstract

Endogenous small RNAs (miRNAs and siRNAs) regulate gene expression in diverse biological processes. Research with the Arabidopsis-Pseudomonas syringae system has shown that small RNAs contribute to plant immunity by regulating the expression of their target genes. Plant immunity can be triggered by pathogen-associated molecular patterns (PAMPs) or effector proteins that are delivered into the host cell by the pathogen. Experimental evidence indicates that the miRNA pathway play a major role in PAMP-triggered immunity while some of the siRNA pathways appear to be more important in effector-triggered immunity. In addition, some P. syringae effector proteins appear to inhibit miRNA biogenesis or function to enhance bacterial virulence. These exciting findings illustrate a new battle ground for plant-pathogen interactions.

Keywords

miRNA / siRNA / PTI / ETI / effectors

References

[1] Agorio A, Vera P (2007). ARGONAUTE4 is required for resistance to Pseudomonas syringae in Arabidopsis. Plant Cell, 19(11): 3778–3790

[2] Baulcombe D (2004). RNA silencing in plants. Nature, 431(7006): 356–363

[3] Boller T, He S Y (2009). Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 324(5928): 742–744

[4] Chapman E J, Carrington J C (2007). Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet, 8(11): 884–896

[5] Chisholm S T, Coaker G, Day B, Staskawicz B J (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124(4): 803–814

[6] Crane Y M, Gelvin S B (2007). RNAi-mediated gene silencing reveals involvement of Arabidopsis chromatin-related genes in Agrobacterium-mediated root transformation. Proc Natl Acad Sci USA, 104(38): 15156–15161

[7] Cui H T, Wang Y J, Xue L, Chu J F, Yan C Y, Fu J H, Chen M S, Innes R W, Zhou J M (2010). Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe, 7(2): 164–175

[8] 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, Carrington J C (2007). High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE, 2(2): e219

[9] Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Boil, 19: 423–430

[10] Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield J W, Robatzek S (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol, 18(23): 1824–1832

[11] He X F, Fang Y Y, Feng L, Guo H S (2008). Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett, 582(16): 2445–2452

[12] Jagadeeswaran G, Saini A, Sunkar R (2009). Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta, 229(4): 1009–1014

[13] Jones J D G, Dangl J L (2006). The plant immune system. Nature, 444(7117): 323–329

[14] Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H L (2007). A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev, 21(23): 3123–3134

[15] Katiyar-Agarwal S, Jin H L (2010). Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol, 48(1): 225–246

[16] Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr, Zhu J K, Staskawicz B J, Jin H L (2006). A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA, 103(47): 18002–18007

[17] Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crété P, Voinnet O, Robaglia C (2009). Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell, 21(6): 1762–1768

[18] Li X Y, Lin H, Zhang W G, Zou Y, Zhang J, Tang X Y, Zhou J M (2005). Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA, 102(36): 12990–12995

[19] Li Y, Zhang Q Q, Zhang J G, Wu L, Qi Y J, Zhou J M (2010). Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol, 152(4): 2222–2231

[20] Liu J, Elmore J M, Lin Z J, Coaker G (2011). A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe, 9(2): 137–146

[21] Lu S F, Sun Y H, Amerson H, Chiang V L (2007). MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J, 51(6): 1077–1098

[22] Morel J B, Godon C, Mourrain P, Béclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H (2002). Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell, 14(3): 629–639

[23] Mori I C, Schroeder J I (2004). Reactive oxygen species activation of plant Ca²⁺ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol, 135(2): 702–708

[24] Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel J B, Jouette D, Lacombe A M, Nikic S, Picault N, Rémoué K, Sanial M, Vo T A, Vaucheret H (2000). ArabidopsisSGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell, 101(5): 533–542

[25] Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones J D (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312(5772): 436–439

[26] Navarro L, Jay F, Nomura K, He S Y, Voinnet O (2008). Suppression of the microRNA pathway by bacterial effector proteins. Science, 321(5891): 964–967

[27] Padmanabhan C, Zhang X, Jin H L (2009). Host small RNAs are big contributors to plant innate immunity. Curr Opin Plant Biol, 12(4): 465–472

[28] Sarris P F, Gao S, Karademiris K, Jin H, Kalantidis K, Panopoulos N J (2011). Phytobacterial type III effectors HopX1, HopAB1 and HopF2 enhance sense-post transcriptional gene silencing independently of plant R gene-effector recognition. Mol Plant Microbe Interact, 24(8): 907–907

[29] Wang Y J, Li J F, Hou S G, Wang X W, Li Y, Ren D T, Chen S, Tang X Y, Zhou J M (2010). A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell, 22(6): 2033–2044

[30] Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D (2010). The type III effector HopF2_Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc Natl Acad Sci USA, 107(5): 2349–2354

[31] Xiang T T, Zong N, Zou Y, Wu Y, Zhang J, Xing W M, Li Y, Tang X Y, Zhu L H, Chai J J, Zhou J M (2008). Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol, 18(1): 74–80

[32] Yan Y, Zhang Y, Yang K, Sun Z, Fu Y, Chen X, Fang R (2011). Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J, 65(5): 820–828

[33] Yu D, Fan B, MacFarlane S A, Chen Z (2003). Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant Microbe Interact, 16(3): 206–216

[34] Zhang J, Li W, Xiang T T, Liu Z X, Laluk K, Ding X J, Zou Y, Gao M H, Zhang X J, Chen S, Mengiste T, Zhang Y L, Zhou J M (2010). Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe, 7(4): 290–301

[35] Zhang J, Shao F, Li Y, Cui H T, Chen L J, Li H T, Zou Y, Long C Z, Lan L F, Chai J J, Chen S, Tang X Y, Zhou J M (2007). A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe, 1(3): 175–185

[36] Zhang X, Zhao H, Gao S, Wang W C, Katiyar-Agarwal S, Huang H D, Raikhel N, Jin H (2011). Arabidopsis Argonaute 2 regulates innate immunity via miRNA393^*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell, 42(3): 356–366

[37] Zhou H, Lin J, Johnson A, Morgan R L, Zhong W, Ma W (2011). Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host Microbe, 9(3): 177–186

[38] Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010). Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot, 61(15): 4157–4168

[39] Zhou X, Sunkar R, Jin H, Zhu J K, Zhang W (2009). Genome-wide identification and analysis of small RNAs originated from natural antisense transcripts in Oryza sativa. Genome Res, 19(1): 70–78

[40] Zilberman D, Cao X, Jacobsen S E (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science, 299(5607): 716–719

[41] Zilberman D, Cao X F, Johansen L K, Xie Z X, Carrington J C, Jacobsen S E (2004). Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol, 14(13): 1214–1220

[42] Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones J D, Boller T, Felix G (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 125(4): 749–760

[43] Zipfel C, Robatzek S, Navarro L, Oakeley E J, Jones J D, Felix G, Boller T (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428(6984): 764–767

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg