AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling

Highlight The transcription factor WRKY22 increases susceptibility to aphids in Arabidopsis via the suppression of salicylic acid signalling.

[1]  Maurice W. Sabelis,et al.  World Crop Pests , 2000 .

[2]  G. Jander,et al.  Biochemistry and molecular biology of Arabidopsis–aphid interactions , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[3]  C. Wilkerson,et al.  Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Dinesh Yadav,et al.  Pectin lyase: A review , 2009 .

[5]  R. Solano,et al.  ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant Defense Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007468. , 2003, The Plant Cell Online.

[6]  F. Divol,et al.  Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. , 2007, Plant, cell & environment.

[7]  Michael L. Creech,et al.  Integration of biological networks and gene expression data using Cytoscape , 2007, Nature Protocols.

[8]  L. Walling.  Avoiding Effective Defenses: Strategies Employed by Phloem-Feeding Insects1 , 2008, Plant Physiology.

[9]  S. Spoel,et al.  Making sense of hormone crosstalk during plant immune responses. , 2008, Cell host & microbe.

[10]  C. Pieterse,et al.  Hormonal modulation of plant immunity. , 2012, Annual review of cell and developmental biology.

[11]  I. Kaloshian,et al.  Mi-1-Mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. , 2006, Molecular plant-microbe interactions : MPMI.

[12]  E. Weiler,et al.  Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Qian,et al.  Thirty-seven transcription factor genes differentially respond to a harpin protein and affect resistance to the green peach aphid in Arabidopsis , 2010, Journal of Biosciences.

[14]  Huaiyu Mi,et al.  The InterPro protein families database: the classification resource after 15 years , 2014, Nucleic Acids Res..

[15]  C. Pieterse,et al.  Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions , 2015, Front. Plant Sci..

[16]  George Karlin-Neumann,et al.  Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. , 2003, The Plant journal : for cell and molecular biology.

[17]  T. Eulgem,et al.  The WRKY superfamily of plant transcription factors. , 2000, Trends in plant science.

[18]  Martin J. Mueller,et al.  Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. , 2005, Molecular plant-microbe interactions : MPMI.

[19]  P. Hedley,et al.  Vitamin C and the abscisic acid-insensitive 4 transcription factor are important determinants of aphid resistance in Arabidopsis. , 2013, Antioxidants & redox signaling.

[20]  W. F. Tjallingii.  Electrical recording of stylet penetration activities. , 1988 .

[21]  W. F. Tjallingii,et al.  Tissue localisation of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs , 1993 .

[22]  W. F. Tjallingii.  Sieve element acceptance by aphids , 1994 .

[23]  Y. Miao,et al.  Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis , 2005, Plant Molecular Biology.

[24]  Jian-Kang Zhu,et al.  The Arabidopsis Cold-Responsive Transcriptome and Its Regulation by ICE1w⃞ , 2005, The Plant Cell Online.

[25]  A. Schikora,et al.  N-Acyl-Homoserine Lactone Confers Resistance toward Biotrophic and Hemibiotrophic Pathogens via Altered Activation of AtMPK61[C][W] , 2011, Plant Physiology.

[26]  Bjarni J. Vilhjálmsson,et al.  Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines , 2010 .

[27]  Nobutaka Mitsuda,et al.  Functional analysis of transcription factors in Arabidopsis. , 2009, Plant & cell physiology.

[28]  M. J. Moloi,et al.  The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. , 2006, Journal of plant physiology.

[29]  B. Thomma,et al.  Concomitant Activation of Jasmonate and Ethylene Response Pathways Is Required for Induction of a Plant Defensin Gene in Arabidopsis , 1998, Plant Cell.

[30]  Su-Hyun Han,et al.  Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. , 2013, Plant & cell physiology.

[31]  Mary Hummerick,et al.  Genome-wide expression analysis of reactive oxygen species gene network in Mizuna plants grown in long-term spaceflight , 2014, BMC Plant Biology.

[32]  P. Vidhyasekaran.  PAMP Signals in Plant Innate Immunity: Signal Perception and Transduction , 2013 .

[33]  Zhixiang Chen,et al.  Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response , 2004, Plant Molecular Biology.

[34]  M. Shih,et al.  Submergence Confers Immunity Mediated by the WRKY22 Transcription Factor in Arabidopsis[W] , 2013, Plant Cell.

[35]  David G Hendrickson,et al.  Differential analysis of gene regulation at transcript resolution with RNA-seq , 2012, Nature Biotechnology.

[36]  Martin Kuiper,et al.  BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks , 2005, Bioinform..

[37]  Jing Li,et al.  The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense On-line version contains Web-only data. , 2004, The Plant Cell Online.

[38]  Yi Li,et al.  WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. , 2007, Plant & cell physiology.

[39]  Helena Oakey,et al.  Joint modeling of additive and non-additive genetic line effects in single field trials , 2006, Theoretical and Applied Genetics.

[40]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[41]  Ulrike Zentgraf,et al.  The Antagonist Function of Arabidopsis WRKY53 and ESR/ESP in Leaf Senescence Is Modulated by the Jasmonic and Salicylic Acid Equilibrium , 2007, The Plant Cell Online.

[42]  M. Dicke,et al.  Feeding behaviour and performance of different populations of the black currant‐lettuce aphid, Nasonovia ribisnigri, on resistant and susceptible lettuce , 2013 .

[43]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[44]  Björn Olsson,et al.  BMC Genomics BioMed Central , 2007 .

[45]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[46]  J. Cornelis,et al.  Impact of rice cultivar and organ on elemental composition of phytoliths and the release of bio-available silicon , 2014, Front. Plant Sci..

[47]  E. Bornberg-Bauer,et al.  The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. , 2007, The Plant journal : for cell and molecular biology.

[48]  T. Joshi,et al.  Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores , 2014, Front. Plant Sci..

[49]  A. Pfitzner,et al.  NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants , 2001, Plant Molecular Biology.

[50]  K. D. Pandey,et al.  Comparative transcriptome analysis of Gossypium hirsutum L. in response to sap sucking insects: aphid and whitefly , 2013, BMC Genomics.

[51]  O. E. Krips,et al.  High-throughput phenotyping of plant resistance to aphids by automated video tracking , 2015, Plant Methods.

[52]  D. L. McLEAN,et al.  A Technique for Electronically Recording Aphid Feeding and Salivation , 1964, Nature.

[53]  C. Pieterse,et al.  Significance of inducible defense-related proteins in infected plants. , 2006, Annual review of phytopathology.

[54]  Joy Bergelson,et al.  Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[55]  L. Taiz,et al.  Plant Cell Expansion: Regulation of Cell Wall Mechanical Properties , 1984 .

[56]  I. Somssich,et al.  The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways , 2007, Planta.

[57]  G. Moore,et al.  Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. , 2015, Molecular plant pathology.

[58]  C. Gatz,et al.  Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis , 2005, The Plant Cell Online.

[59]  T. Lumley,et al.  gplots: Various R Programming Tools for Plotting Data , 2015 .

[60]  Willem Kruijer,et al.  Marker-Based Estimation of Heritability in Immortal Populations , 2014, Genetics.

[61]  M. Nordborg,et al.  A Coastal Cline in Sodium Accumulation in Arabidopsis thaliana Is Driven by Natural Variation of the Sodium Transporter AtHKT1;1 , 2010, PLoS genetics.

[62]  D. Navarre,et al.  Low Oleic Acid-Derived Repression of Jasmonic Acid-Inducible Defense Responses Requires the WRKY50 and WRKY51 Proteins1[W][OA] , 2010, Plant Physiology.

[63]  T. Mészáros,et al.  The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. , 2006, The Plant journal : for cell and molecular biology.

[64]  R. Hancock,et al.  Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects. , 2015, Journal of experimental botany.

[65]  F. Ausubel,et al.  Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. , 2008, Molecular plant.

[66]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[67]  J. Bos,et al.  Toward understanding the role of aphid effectors in plant infestation. , 2013, Molecular plant-microbe interactions : MPMI.

[68]  N. Brisson,et al.  The Conjugated Auxin Indole-3-Acetic Acid–Aspartic Acid Promotes Plant Disease Development[C][W] , 2012, Plant Cell.

[69]  Han Chen,et al.  Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress , 2010, BMC Plant Biology.

[70]  Yan Zou,et al.  Overexpression of AHL20 negatively regulates defenses in Arabidopsis. , 2010, Journal of integrative plant biology.

[71]  J. Schultz,et al.  Major Signaling Pathways Modulate Arabidopsis Glucosinolate Accumulation and Response to Both Phloem-Feeding and Chewing Insects1 , 2005, Plant Physiology.

[72]  J. C. del Pozo,et al.  The TRANSPLANTA collection of Arabidopsis lines: a resource for functional analysis of transcription factors based on their conditional overexpression. , 2014, The Plant journal : for cell and molecular biology.

[73]  J. Louis,et al.  Arabidopsis thaliana—Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids , 2013, Front. Plant Sci..

[74]  J. Qian,et al.  Harpin-induced expression and transgenic overexpression of the phloem protein gene AtPP2-A1 in Arabidopsis repress phloem feeding of the green peach aphid Myzus persicae , 2011, BMC Plant Biology.

[75]  J. Braam,et al.  Arabidopsis Touch-Induced Morphogenesis Is Jasmonate Mediated and Protects against Pests , 2012, Current Biology.

[76]  R. Hehl,et al.  AthaMap web tools for the analysis of transcriptional and posttranscriptional regulation of gene expression in Arabidopsis thaliana. , 2014, Methods in molecular biology.

[77]  P. Winge,et al.  Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae , 2007 .

[78]  K. Shirasu,et al.  The Activated SA and JA Signaling Pathways Have an Influence on flg22-Triggered Oxidative Burst and Callose Deposition , 2014, PloS one.

[79]  T. Lange,et al.  Touch-induced changes in Arabidopsis morphology dependent on gibberellin breakdown , 2015, Nature Plants.

[80]  C. Smith,et al.  The molecular bases of plant resistance and defense responses to aphid feeding: current status , 2007 .

[81]  Sheng Yang He,et al.  Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. , 2006, The Plant journal : for cell and molecular biology.

[82]  J. Ecker,et al.  The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[83]  J. Braam,et al.  Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. , 2004, The New phytologist.

[84]  E. Prado,et al.  Behavioral Evidence for Local Reduction of Aphid-Induced Resistance , 2007, Journal of insect science.

[85]  Xiaoping Zhou,et al.  WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis , 2011, Molecules and cells.

[86]  Mark Zander,et al.  SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. , 2007, The Plant journal : for cell and molecular biology.

[87]  J. V. van Loon,et al.  Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: transcription of a monoterpene synthase gene and volatile emission , 2014, Journal of experimental botany.

[88]  K. Wilson.  Plant Cell Walls , 1953, Nature.

[89]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[90]  Jonathan D. G. Jones,et al.  The Transcriptional Innate Immune Response to flg22. Interplay and Overlap with Avr Gene-Dependent Defense Responses and Bacterial Pathogenesis1[w] , 2004, Plant Physiology.

[91]  Karsten M. Borgwardt,et al.  Whole-genome sequencing of multiple Arabidopsis thaliana populations , 2011, Nature Genetics.

[92]  Björn Usadel,et al.  Reverse Engineering: A Key Component of Systems Biology to Unravel Global Abiotic Stress Cross-Talk , 2012, Front. Plant Sci..

[93]  Pankaj Barah,et al.  Molecular Signatures in Arabidopsis thaliana in Response to Insect Attack and Bacterial Infection , 2013, PloS one.

[94]  P. Vidhyasekaran.  PAMP Signals in Plant Innate Immunity , 2014, Signaling and Communication in Plants.

[95]  A. Auton,et al.  Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel , 2011, Nature Genetics.

[96]  Detlef Weigel,et al.  The Scale of Population Structure in Arabidopsis thaliana , 2010, PLoS genetics.

[97]  F. Paolocci,et al.  Gene expression profiles of O3-treated Arabidopsis plants. , 2006, Plant, cell & environment.

[98]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[99]  Alexandra M. E. Jones,et al.  Molecular crosstalk between PAMP-triggered immunity and photosynthesis. , 2012, Molecular plant-microbe interactions : MPMI.

[100]  Paul R. Ebert,et al.  Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis , 2004, The Plant Cell Online.

[101]  Di Liu,et al.  DATF: a database of Arabidopsis transcription factors , 2005, Bioinform..

[102]  R. Solano,et al.  JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis , 2004, The Plant Cell Online.

[103]  K. Shinozaki,et al.  Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. , 2000, The Plant journal : for cell and molecular biology.