A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana.

Cucumber mosaic virus (CMV) encodes the 2b protein, which plays a role in local and systemic virus movement, symptom induction and suppression of RNA silencing. It also disrupts signalling regulated by salicylic acid and jasmonic acid. CMV induced an increase in tolerance to drought in Arabidopsis thaliana. This was caused by the 2b protein, as transgenic plants expressing this viral factor showed increased drought tolerance, but plants infected with CMVΔ2b, a viral mutant lacking the 2b gene, did not. The silencing effector ARGONAUTE1 (AGO1) controls a microRNA-mediated drought tolerance mechanism and, in this study, we noted that plants (dcl2/3/4 triple mutants) lacking functional short-interfering RNA-mediated silencing were also drought tolerant. However, drought tolerance engendered by CMV may be independent of the silencing suppressor activity of the 2b protein. Although CMV infection did not alter the accumulation of the drought response hormone abscisic acid (ABA), 2b-transgenic and ago1-mutant seeds were hypersensitive to ABA-mediated inhibition of germination. However, the induction of ABA-regulated genes in 2b-transgenic and CMV-infected plants was inhibited more strongly than in ago1-mutant plants. The virus engenders drought tolerance by altering the characteristics of the roots and not of the aerial tissues as, compared with the leaves of silencing mutants, leaves excised from CMV-infected or 2b-transgenic plants showed greater stomatal permeability and lost water more rapidly. This further indicates that CMV-induced drought tolerance is not mediated via a change in the silencing-regulated drought response mechanism. Under natural conditions, virus-induced drought tolerance may serve viruses by aiding susceptible hosts to survive periods of environmental stress.

[1]  S. Elena,et al.  A Meta-Analysis Reveals the Commonalities and Differences in Arabidopsis thaliana Response to Different Viral Pathogens , 2012, PloS one.

[2]  Kimihito Ito,et al.  Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors , 2012, Proceedings of the National Academy of Sciences.

[3]  S. Ohki,et al.  Cucumber mosaic virus: viral genes as virulence determinants. , 2012, Molecular plant pathology.

[4]  P. Palukaitis,et al.  RNA binding is more critical to the suppression of silencing function of Cucumber mosaic virus 2b protein than nuclear localization. , 2012, RNA.

[5]  Jianhua Zhu,et al.  Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. , 2012, Biochimica et biophysica acta.

[6]  Hailing Jin,et al.  Transcriptional Regulation of Arabidopsis MIR168a and ARGONAUTE1 Homeostasis in Abscisic Acid and Abiotic Stress Responses1[W] , 2012, Plant Physiology.

[7]  Yuan-yuan Fang,et al.  Suppression of Arabidopsis ARGONAUTE1-Mediated Slicing, Transgene-Induced RNA Silencing, and DNA Methylation by Distinct Domains of the Cucumber mosaic virus 2b Protein[W] , 2012, Plant Cell.

[8]  Mathew G. Lewsey,et al.  Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco , 2011, Scientific reports.

[9]  H. Vaucheret,et al.  The miRNA pathway limits AGO1 availability during siRNA-mediated PTGS defense against exogenous RNA , 2011, Nucleic acids research.

[10]  C. Masuta,et al.  Virus-Induced Necrosis Is a Consequence of Direct Protein-Protein Interaction between a Viral RNA-Silencing Suppressor and a Host Catalase[C][W] , 2011, Plant Physiology.

[11]  X. Deng,et al.  Geminiviruses Subvert Ubiquitination by Altering CSN-Mediated Derubylation of SCF E3 Ligase Complexes and Inhibit Jasmonate Signaling in Arabidopsis thaliana[C][W] , 2011, Plant Cell.

[12]  M. Roossinck The good viruses: viral mutualistic symbioses , 2011, Nature Reviews Microbiology.

[13]  Mathew G. Lewsey,et al.  An Antiviral Defense Role of AGO2 in Plants , 2011, PloS one.

[14]  R. Poethig,et al.  An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana , 2010, Silence.

[15]  E. Grill,et al.  ABA perception and signalling. , 2010, Trends in plant science.

[16]  A. Fraile,et al.  Arabidopsis thaliana as a model for the study of plant–virus co-evolution , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  Mathew G. Lewsey,et al.  Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. , 2010, Molecular plant-microbe interactions : MPMI.

[18]  S. Cutler,et al.  Abscisic acid: emergence of a core signaling network. , 2010, Annual review of plant biology.

[19]  M. Crespi,et al.  miR390, Arabidopsis TAS3 tasiRNAs, and Their AUXIN RESPONSE FACTOR Targets Define an Autoregulatory Network Quantitatively Regulating Lateral Root Growth[W] , 2010, Plant Cell.

[20]  Mathew G. Lewsey,et al.  Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. , 2010, Molecular plant-microbe interactions : MPMI.

[21]  A. Fraile,et al.  The coevolution of plants and viruses: resistance and pathogenicity. , 2010, Advances in virus research.

[22]  Mathew G. Lewsey,et al.  Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid-treated plants. , 2009, The Journal of general virology.

[23]  J. Carr,et al.  Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene. , 2009, The Journal of general virology.

[24]  William Truman,et al.  Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. , 2009, The Plant journal : for cell and molecular biology.

[25]  D. Winstanley,et al.  Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea , 2009, Proceedings of the National Academy of Sciences.

[26]  Fiona C. Robertson,et al.  The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. , 2009, Molecular plant-microbe interactions : MPMI.

[27]  H. Vaucheret,et al.  ARGONAUTE 1 homeostasis invokes the coordinate action of the microRNA and siRNA pathways , 2009, EMBO reports.

[28]  C. Valon,et al.  The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. , 2009, Journal of experimental botany.

[29]  A. Moorman,et al.  Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data , 2009, Nucleic acids research.

[30]  T. Csorba,et al.  RNA silencing: an antiviral mechanism. , 2009, Advances in virus research.

[31]  Fiona C. Robertson,et al.  Interactions between circadian and hormonal signalling in plants , 2009, Plant Molecular Biology.

[32]  L. Sumner,et al.  Virus infection improves drought tolerance. , 2008, The New phytologist.

[33]  Javier F. Palatnik,et al.  Control of Jasmonate Biosynthesis and Senescence by miR319 Targets , 2008, PLoS biology.

[34]  S. Ding,et al.  Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. , 2008, Annual review of phytopathology.

[35]  D. Gibbs,et al.  Branching out in new directions: the control of root architecture by lateral root formation. , 2008, The New phytologist.

[36]  Jianhua Zhu,et al.  The Arabidopsis NFYA5 Transcription Factor Is Regulated Transcriptionally and Posttranscriptionally to Promote Drought Resistance[W] , 2008, The Plant Cell Online.

[37]  M. Grant,et al.  A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress , 2008, Plant Methods.

[38]  W. Du,et al.  The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. , 2008, Plant, cell & environment.

[39]  Joshua S Yuan,et al.  Statistical methods for efficiency adjusted real‐time PCR quantification , 2008, Biotechnology journal.

[40]  C. Masuta,et al.  Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. , 2007, Plant & cell physiology.

[41]  Ramanjulu Sunkar,et al.  Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. , 2007, Trends in plant science.

[42]  Fiona C. Robertson,et al.  Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. , 2007, The Plant journal : for cell and molecular biology.

[43]  R. Redman,et al.  A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance , 2007, Science.

[44]  Nam-Hai Chua,et al.  ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. , 2007, The Plant journal : for cell and molecular biology.

[45]  T. Tuschl,et al.  Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. , 2006, Genes & development.

[46]  A. Si-Ammour,et al.  Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing , 2006, Nucleic acids research.

[47]  Jinsong Bao,et al.  Hierarchical Action and Inhibition of Plant Dicer-Like Proteins in Antiviral Defense , 2006, Science.

[48]  J. Carr,et al.  Plant Metabolism Associated with Resistance and Susceptibility , 2006 .

[49]  D. Baulcombe,et al.  Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. Bartel,et al.  MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genesw⃞ , 2005, The Plant Cell Online.

[51]  N. Chua,et al.  MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development , 2005, The Plant Cell Online.

[52]  N. Eckardt MicroRNAs Regulate Auxin Homeostasis and Plant Development , 2005, The Plant Cell Online.

[53]  G. Sandberg,et al.  Dissecting Arabidopsis lateral root development. , 2003, Trends in plant science.

[54]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[55]  Hur-Song Chang,et al.  Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. , 2003, The Plant journal : for cell and molecular biology.

[56]  Animesh Ray,et al.  DICER-LIKE1: blind men and elephants in Arabidopsis development. , 2002, Trends in plant science.

[57]  Philippe Mourrain,et al.  Fertile Hypomorphic ARGONAUTE (ago1) Mutants Impaired in Post-Transcriptional Gene Silencing and Virus Resistance , 2002, The Plant Cell Online.

[58]  J. Malamy,et al.  Environmental regulation of lateral root initiation in Arabidopsis. , 2001, Plant physiology.

[59]  M. Mayo,et al.  Umbravirus gene expression helps potato leafroll virus to invade mesophyll tissues and to be transmitted mechanically between plants. , 2001, Virology.

[60]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[61]  S. Ding,et al.  The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. , 2001, Molecular plant-microbe interactions : MPMI.

[62]  S. Jacobsen,et al.  Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. , 1999, Development.

[63]  K. Paek,et al.  Isolation of a putative tobacco host factor interacting with cucumber mosaic virus-encoded 2b protein by yeast two-hybrid screening. , 1999, Molecules and cells.

[64]  Perry,et al.  Stability of the aphid transmission phenotype in cucumber mosaic virus , 1999 .

[65]  D. Baulcombe,et al.  Retracted: Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana , 1998, The EMBO journal.

[66]  P. Palukaitis,et al.  Rapid induction and severity of symptoms in zucchini squash (Cucurbita pepo) map to RNA 1 of cucumber mosaic virus. , 1990 .

[67]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[68]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[69]  M. Alexander Why microbial predators and parasites do not eliminate their prey and hosts. , 1981, Annual review of microbiology.