MiRNA863-3p sequentially targets negative immune regulator ARLPKs and positive regulator SERRATE upon bacterial infection

Nature Communications

Volumn 7, Issue , 2016, Pages

  Niu, Dongdong ^a,b   Lii, Yifan E ^b   Chellappan, Padmanabhan ^b   Lei, Lei ^c   Peralta, Karl ^b   Jiang, Chunhao ^a,b   Guo, Jianhua ^a   Coaker, Gitta ^c   Jin, Hailing ^b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATYPICAL RECEPTOR LIKE PSEUDOKINASE 1; ATYPICAL RECEPTOR LIKE PSEUDOKINASE 2; MESSENGER RNA; MICRORNA; MICRORNA 863 3P; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; MIRN863 MICRORNA, ARABIDOPSIS; RNA BINDING PROTEIN; SE PROTEIN, ARABIDOPSIS;

BACTERIUM; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNITY; INHIBITION; PATHOGEN; PLANT DEFENSE; PROTEIN;

AGROBACTERIUM; ARTICLE; BACTERIAL PLANT DISEASE; BACTERIAL STRAIN; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE SILENCING; GENE TARGETING; IMMUNE RESPONSE; IMMUNOREGULATION; INFECTION RESISTANCE; INFECTION SENSITIVITY; NEGATIVE FEEDBACK; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT IMMUNITY; PLANT LEAF; PSEUDOMONAS INFECTION; PSEUDOMONAS SYRINGAE; SERRATE GENE; TRANSGENIC PLANT; TRANSLATION REGULATION; ARABIDOPSIS; BINDING SITE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGICAL FEEDBACK; PHYSIOLOGY; PLANT DISEASE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BINDING SITES; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; PLANT DISEASES; PLANT IMMUNITY; PROTEIN BIOSYNTHESIS; PSEUDOMONAS SYRINGAE; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84964642777     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11324     Document Type: Article

References (70)

1. Katiyar-Agarwal, S. & Jin, H. Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 48, 225-246 (2010).
2. Weiberg, A. & Jin, H. Small RNAs-the secret agents in the plant-pathogen interactions. Curr. Opin. Plant Biol. 26, 87-94 (2015).
3. Weiberg, A., Wang, M., Bellinger, M. & Jin, H. Small RNAs: a new paradigm in plant-microbe interactions. Annu. Rev. Phytopathol. 52, 495-516 (2014).
4. Padmanabhan, C., Zhang, X. & Jin, H. Host small RNAs are big contributors to plant innate immunity. Curr. Opin. Plant Biol. 12, 465-472 (2009).
5. Macho, A. P. & Zipfel, C. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54, 263-272 (2014).
6. Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548 (2010).
7. Li, X., Kapos, P. & Zhang, Y. NLRs in plants. Curr. Opin. Immunol. 32, 114-121 (2015).
8. Kunkel, B. N., Bent, A. F., Dahlbeck, D., Innes, R. W. & Staskawicz, B. J. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5, 865-875 (1993).
9. Yu, G. L., Katagiri, F. & Ausubel, F. M. Arabidopsis mutations at the Rps2 locus result in loss of resistance to Pseudomonas-Syringae strains expressing the avirulence gene Avrrpt2. Mol. Plant Microbe In. 6, 434-443 (1993).
10. Weiberg, A. et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118-123 (2013).
11. Martinez de Alba, A. E., Elvira-Matelot, E. & Vaucheret, H. Gene silencing in plants: a diversity of pathways. Biochim. Biophys. Acta 1829, 1300-1308 (2013).
12. Katiyar-Agarwal, S. et al. A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl Acad. Sci. USA 103, 18002-18007 (2006).
13. Katiyar-Agarwal, S., Gao, S., Vivian-Smith, A. & Jin, H. A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev. 21, 3123-3134 (2007).
14. Navarro, L. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439 (2006).
15. Zhang, X. et al. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(∗)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 42, 356-366 (2011).
16. Li, Y. et al. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol. 152, 2222-2231 (2010).
17. Zhang, W. et al. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol. Biol. 75, 93-105 (2011).
18. Yang, L., Liu, Z. Q., Lu, F., Dong, A. W. & Huang, H. SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J. 47, 841-850 (2006).
19. Fang, Y. & Spector, D. L. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17, 818-823 (2007).
20. Dong, Z., Han, M. H. & Fedoroff, N. The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl Acad. Sci. USA 105, 9970-9975 (2008).
21. Lobbes, D., Rallapalli, G., Schmidt, D. D., Martin, C. & Clarke, J. SERRATE: a new player on the plant microRNA scene. EMBO Rep. 7, 1052-1058 (2006).
22. Meyers, B. C. et al. Criteria for annotation of plant MicroRNAs. Plant Cell 20, 3186-3190 (2008).
23. Shiu, S. H. et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234 (2004).
24. Raczynska, K. D. et al. The SERRATE protein is involved in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res. 42, 1224-1244 (2014).
25. Boudeau, J., Miranda-Saavedra, D., Barton, G. J. & Alessi, D. R. Emerging roles of pseudokinases. Trends Cell Biol. 16, 443-452 (2006).
26. Rogers, K. & Chen, X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383-2399 (2013).
27. Liu, J. D., Valencia-Sanchez, M. A., Hannon, G. J. & Parker, R. MicroRNAdependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719-U118 (2005).
28. Clarke, J. H., Tack, D., Findlay, K., Van Montagu, M. & Van Lijsebettens, M. The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J. 20, 493-501 (1999).
29. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657 (2003).
30. Liu, J., Elmore, J. M., Lin, Z. J. & Coaker, G. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9, 137-146 (2011).
31. Nelson, B. K., Cai, X. & Nebenfuhr, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136 (2007).
32. Robatzek, S., Chinchilla, D. & Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542 (2006).
33. Geisler-Lee, J. et al. A predicted interactome for Arabidopsis. Plant Physiol. 145, 317-329 (2007).
34. Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983 (2002).
35. Prigge, M. J. & Wagner, D. R. The arabidopsis serrate gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13, 1263-1279 (2001).
36. Laubinger, S. et al. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 105, 8795-8800 (2008).
37. Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J. L. & Chory, J. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem. Sci. 39, 447-456 (2014).
38. Dong, X. B., Jiang, Z. H., Peng, Y. L. & Zhang, Z. D. Revealing shared and distinct gene network organization in arabidopsis immune responses by integrative analysis. Plant Physiol. 167, 1186-1203 (2015).
39. Antolin-Llovera, M., Ried, M. K., Binder, A. & Parniske, M. Receptor kinase signaling pathways in plant-microbe interactions. Annu. Rev. Phytopathol. 50, 451-473 (2012).
40. Monaghan, J. & Zipfel, C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15, 349-357 (2012).
41. Li, J. & Tax, F. E. Receptor-like kinases: key regulators of plant development and defense. J. Integr. Plant Biol. 55, 1184-1187 (2013).
42. Igarashi, D., Tsuda, K. & Katagiri, F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J. 71, 194-204 (2012).
43. Mosher, S. et al. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J. 73, 469-482 (2013).
44. Gao, M. et al. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6, 34-44 (2009).
45. Halter, T. et al. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24, 134-143 (2014).
46. Castells, E. & Casacuberta, J. M. Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. J. Exp. Bot. 58, 3503-3511 (2007).
47. Reiterer, V., Eyers, P. A. & Farhan, H. Day of the dead: pseudokinases and pseudophosphatases in physiology and disease. Trends Cell Biol. 24, 489-505 (2014).
48. Lewis, J. D. et al. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. Proc. Natl Acad. Sci. USA 110, 18722-18727 (2013).
49. Nimchuk, Z. L., Tarr, P. T. & Meyerowitz, E. M. An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23, 851-854 (2011).
50. Chevalier, D. et al. STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 9074-9079 (2005).
51. Wang, G. et al. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18, 285-295 (2015).
52. Gee, C. L. et al. A phosphorylated pseudokinase complex controls cell wall synthesis in mycobacteria. Sci. Signal. 5, ra7 (2012).
53. Childers, W. S. et al. Cell fate regulation governed by a repurposed bacterial histidine kinase. PLoS Biol. 12, e1001979 (2014).
54. Ladwig, F. et al. Phytosulfokine regulates growth in arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27, 1718-1729 (2015).
55. Fuglsang, A. T. et al. Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. Plant J. 80, 951-964 (2014).
56. Merchante, C., Alonso, J. M. & Stepanova, A. N. Ethylene signaling: simple ligand, complex regulation. Curr. Opin. Plant Biol. 16, 554-560 (2013).
57. Wulfetange, K. et al. The cytokinin receptors of arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 156, 1808-1818 (2011).
58. Koizumi, N. et al. Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol. 127, 949-962 (2001).
59. Voisin, D. et al. Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLoS Genet. 5, e1000703 (2009).
60. Allen, E. et al. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282-1290 (2004).
61. Allen, E., Xie, Z., Gustafson, A. M. & Carrington, J. C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221 (2005).
62. Innes, R. W. et al. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J. 4, 813-820 (1993).
63. Bisgrove, S. R., Simonich, M. T., Smith, N. M., Sattler, A. & Innes, R. W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6, 927-933 (1994).
64. Hinsch, M. & Staskawicz, B. Identification of a new Arabidopsis disease resistance locus, RPs4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi. Mol. Plant Microbe In. 9, 55-61 (1996).
65. Yuan, J. & He, S. Y. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178, 6399-6402 (1996).
66. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121-1133 (2006).
67. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629 (2006).
68. Wang, D., Weaver, N. D., Kesarwani, M. & Dong, X. N. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308, 1036-1040 (2005).
69. Llave, C., Xie, Z. X., Kasschau, K. D. & Carrington, J. C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056 (2002).
70. Caplan, J. L. et al. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host Microbe 6, 457-469 (2009).