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A double-stranded RNA binding protein, HYL1, regulates plant immunity via the jasmonic acid pathway

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Abstract

MicroRNA (miRNA) and small interference RNA (siRNA) regulate not only plant growth and development, but also various responses to stress, including biotic stress, through post-transcriptional gene regulation. Hyponastic leaves 1 (HYL1), a double-stranded RNA binding protein, plays an important role in miRNA and siRNA processing, along with Dicer-like 1 (DCL1) and Hua Enhancer 1 (HEN1). Of five double-stranded RNA binding protein (DRB) deficient mutants in Arabidopsis, only the hyl1 mutant compromised innate immune responses to Pseudomonas syringae pv. tomato (Pst) DC3000 hrcC infection when compared to wild-type plants. This was similar to the response of the hen1 mutant. Furthermore, the hyl1 mutant was susceptible to Pst (avrRpt2) infections, and showed a delay in the hypersensitive response that should result from gene-for-gene interactions between RPS2 and AvrRpt2. These results suggest that HYL1 is a major contributor in the DRB family, influencing miRNA and siRNA biogenesis and therefore playing essential roles in PAMP- and effect-triggered immune responses in plants. DNA microarray analysis revealed that the expression of genes involved in jasmonic acid (JA) biosynthesis, signal transduction, and downstream responses was significantly upregulated in the hyl1 mutant compared with wild-type plants. Consistent with this, transgenic plants overexpressing HYL1 are hypersensitive to the necrotrophic pathogen Botrytis cinerea, of which resistance is mainly regulated by JA. These results elucidate the importance of small RNA-mediated JA regulation in plant immunity.

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References

  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz, BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Chen X (2005) MicroRNA biogenesis and function in plants. FEBB Lett 579:5923–5931

    Article  CAS  Google Scholar 

  • Chen X (2008) MicroRNA metabolism in plants. Curr Top Microbiol Immunol 320:117–136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Curtin SJ, Watson JM, Smith NA, Eamens AL, Blanchard CL, Waterhouse PM (2008) The roles of plant dsRNA-binding proteins in RNAi-like pathways. FEBS Lett 582:2753–2760

    Article  CAS  PubMed  Google Scholar 

  • Deng WL, Preston G, Collmer A, Chang CJ, Huang HC (1998) Characterization of the hrpC and hrpRS operons of Pseudomonas syringae pathovars syringae, tomato, and glycinea and analysis of the ability of hrpF, hrpG, hrcC, hrpT, and hrpV mutants to elicit the hypersensitive response and disease in plants. J Bacteriol 180:4523–4531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of primiRNA by DCL1. Proc Natl Acad Sci USA 105:9970–9975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eamens AL, Wook Kim K, Waterhouse PM (2012) DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway in Arabidopsis thaliana. Plant Signal Behav 7:1224–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis J, Dodds P (2003) Plant pathology: monitoring a pathogen-targeted host protein. Curr Biol 13:R400–402

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dang JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219

    Article  Google Scholar 

  • Ferrari S, Plotnikova JM, Lorenzo GD, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and EDS4 and PAD4, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Article  CAS  PubMed  Google Scholar 

  • Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, Murai Y, Koiwa H, Seki M, Shinozaki K, Fukuhara T (2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNAbinding proteins in Arabidopsis thaliana. Plant Mol Biol 57:173–188

    Article  CAS  PubMed  Google Scholar 

  • Jin H (2008) Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 582:2679–2684

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 103:18002–18007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katiyar-Agarwal S, Jin H (2010) Role of Small RNAs in Host-Microbe Interactions. Annu Rev Phytopathol 48:225–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102

    Article  CAS  PubMed  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  CAS  PubMed  Google Scholar 

  • Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu YD, Gan QH, Chi XY, Qin S (2008) Roles of microRNA in plant defense and virus offense interaction. Plant Cell Rep 27:1571–1579

    Article  CAS  PubMed  Google Scholar 

  • Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–9677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noir S, Bömer M, Takahashi N, Ishida T, Tsui TL, Balbi V, Shanahan H, Sugimoto K, Devoto A (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 161:1930–1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Somoza I, Cuperus JT, Weigel D, Carrington JC (2009) Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol 12:622–627

    Article  CAS  PubMed  Google Scholar 

  • Song L, Han MH, Lesicka J, Fedoroff N (2007) Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc Natl Acad Sci USA 104:5437–5442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St Johnston D, Brown NH, Gall JG, Jantsch M (1992) A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci USA 89:10979–10983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • Vazquez F, Gasciolli V, Crété P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Yu L, Cao W, Mao Y, Liu Z and He Y (2007) The N-terminal double-stranded RNA binding domains of Arabidopsis HYPONASTIC LEAVES1 are sufficient for pre-microRNA processing. Plant Cell 19:914–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, Yu X, Shen R, He Y (2005) HYL1 gene maintains venation and polarity of leaves. Planta 221:231–242

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Tackmin Kwon.

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Kwon, T. A double-stranded RNA binding protein, HYL1, regulates plant immunity via the jasmonic acid pathway. J. Plant Biol. 59, 506–514 (2016). https://doi.org/10.1007/s12374-016-0303-1

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