Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana.

Myzus persicae (green peach aphid) feeding on Arabidopsis thaliana induces a defence response, quantified as reduced aphid progeny production, in infested leaves but not in other parts of the plant. Similarly, infiltration of aphid saliva into Arabidopsis leaves causes only a local increase in aphid resistance. Further characterization of the defence-eliciting salivary components indicates that Arabidopsis recognizes a proteinaceous elicitor with a size between 3 and 10 kD. Genetic analysis using well-characterized Arabidopsis mutants shows that saliva-induced resistance against M. persicae is independent of the known defence signalling pathways involving salicylic acid, jasmonate and ethylene. Among 78 Arabidopsis genes that were induced by aphid saliva infiltration, 52 had been identified previously as aphid-induced, but few are responsive to the well-known plant defence signalling molecules salicylic acid and jasmonate. Quantitative PCR analyses confirm expression of saliva-induced genes. In particular, expression of a set of O-methyltransferases, which may be involved in the synthesis of aphid-repellent glucosinolates, was significantly up-regulated by both M. persicae feeding and treatment with aphid saliva. However, this did not correlate with increased production of 4-methoxyindol-3-ylmethylglucosinolate, suggesting that aphid salivary components trigger an Arabidopsis defence response that is independent of this aphid-deterrent glucosinolate.

[1]  G. Jander,et al.  Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. , 2007, The Plant journal : for cell and molecular biology.

[2]  J. Turner,et al.  Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. , 2002, Molecular plant-microbe interactions : MPMI.

[3]  H. Vogel,et al.  The Gene Controlling the Indole Glucosinolate Modifier1 Quantitative Trait Locus Alters Indole Glucosinolate Structures and Aphid Resistance in Arabidopsis[W] , 2009, The Plant Cell Online.

[4]  Tommy S. Jørstad,et al.  Towards global understanding of plant defence against aphids--timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. , 2008, Plant, cell & environment.

[5]  F. Goggin,et al.  Plant-aphid interactions: molecular and ecological perspectives. , 2007, Current opinion in plant biology.

[6]  L. Walling,et al.  Arabidopsis Transcriptome Changes in Response to Phloem-Feeding Silverleaf Whitefly Nymphs. Similarities and Distinctions in Responses to Aphids1[W][OA] , 2006, Plant Physiology.

[7]  S. Rhee,et al.  Functional Annotation of the Arabidopsis Genome Using Controlled Vocabularies1 , 2004, Plant Physiology.

[8]  Karam B. Singh,et al.  Characterization of Pea Aphid Resistance in Medicago truncatula1[W][OA] , 2008, Plant Physiology.

[9]  I. Baldwin,et al.  Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. , 2001, Plant physiology.

[10]  J. Bodeau,et al.  The Root Knot Nematode Resistance Gene Mi from Tomato Is a Member of the Leucine Zipper, Nucleotide Binding, Leucine-Rich Repeat Family of Plant Genes , 1998, Plant Cell.

[11]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[12]  T. Mitchell-Olds,et al.  Mapping of QTL for Resistance against the Crucifer Specialist Herbivore Pieris brassicae in a New Arabidopsis Inbred Line Population, Da(1)-12×Ei-2 , 2007, PloS one.

[13]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[14]  L. Walling,et al.  Silverleaf Whitefly Induces Salicylic Acid Defenses and Suppresses Effectual Jasmonic Acid Defenses1[W][OA] , 2006, Plant Physiology.

[15]  P. Schulze-Lefert,et al.  A Glucosinolate Metabolism Pathway in Living Plant Cells Mediates Broad-Spectrum Antifungal Defense , 2009, Science.

[16]  Ted C. J. Turlings,et al.  An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion , 1997 .

[17]  P. Chourey,et al.  Fragments of ATP synthase mediate plant perception of insect attack. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Pritchard,et al.  Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. , 2007, Bulletin of entomological research.

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

[20]  P. Ashton,et al.  The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry , 2009, Proteomics.

[21]  J. Glazebrook,et al.  Arabidopsis Cytochrome P450 Monooxygenase 71A13 Catalyzes the Conversion of Indole-3-Acetaldoxime in Camalexin Synthesis[W] , 2007, The Plant Cell Online.

[22]  G. Thompson,et al.  Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. , 2001, Plant physiology.

[23]  Zhiwei Xu,et al.  Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1 , 2004, Plant Molecular Biology.

[24]  W. F. Tjallingii,et al.  Salivary secretions by aphids interacting with proteins of phloem wound responses. , 2006, Journal of experimental botany.

[25]  G. Mazzucchelli,et al.  Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae , 2008, Insect molecular biology.

[26]  R. Last,et al.  Arabidopsis Mutants Lacking Phenolic Sunscreens Exhibit Enhanced Ultraviolet-B Injury and Oxidative Damage , 1995, Plant physiology.

[27]  G. Reeck,et al.  RNAi Knockdown of a Salivary Transcript Leading to Lethality in the Pea Aphid, Acyrthosiphon pisum , 2006, Journal of insect science.

[28]  H. Alborn,et al.  Cowpea Chloroplastic ATP Synthase Is the Source of Multiple Plant Defense Elicitors during Insect Herbivory12[W][OA] , 2007, Plant Physiology.

[29]  Frederick M. Ausubel,et al.  Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response , 2009, Science.

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

[31]  Venkatramana Pegadaraju,et al.  Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. , 2007, The Plant journal : for cell and molecular biology.

[32]  T. Speed,et al.  Summaries of Affymetrix GeneChip probe level data. , 2003, Nucleic acids research.

[33]  G. Thompson,et al.  Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. , 2002, Archives of insect biochemistry and physiology.

[34]  B. Gill,et al.  Identification of microsatellite markers linked to Russian wheat aphid resistance genes Dn4 and Dn6 , 2002, Theoretical and Applied Genetics.

[35]  A. Koornneef Cross-talk in plant defense signaling: Antagonism between salicylate and jasmonate pathways in Arabidopsis , 2008 .

[36]  G. Thompson,et al.  Mapping of Cotton-Melon Aphid Resistance in Melon , 2001 .

[37]  J. Tumlinson,et al.  Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles , 2007, Proceedings of the National Academy of Sciences.

[38]  Barbara Ann Halkier,et al.  Biology and biochemistry of glucosinolates. , 2006, Annual review of plant biology.

[39]  L. M. Schoonhoven,et al.  Insect-plant biology , 1998 .

[40]  I. Kaloshian,et al.  The nematode resistance gene Mi of tomato confers resistance against the potato aphid. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  K. Pappan,et al.  A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant , 2008, Proceedings of the National Academy of Sciences.

[42]  D. Scheel,et al.  The coi1-16 Mutant Harbors a Second Site Mutation Rendering PEN2 Nonfunctional , 2008, The Plant Cell Online.

[43]  W. F. Tjallingii,et al.  Molecular sabotage of plant defense by aphid saliva , 2007, Proceedings of the National Academy of Sciences.

[44]  V. Williamson,et al.  The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. , 2003, Molecular plant-microbe interactions : MPMI.

[45]  J. Glazebrook,et al.  Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase , 1999, Plant Cell.

[46]  B. Halkier,et al.  CYP71B15 (PAD3) Catalyzes the Final Step in Camalexin Biosynthesis1 , 2006, Plant Physiology.

[47]  Torsten Will,et al.  Physical and chemical interactions between aphids and plants. , 2006, Journal of experimental botany.

[48]  B. Gill,et al.  Microsatellite markers linked to six Russian wheat aphid resistance genes in wheat , 2001, Theoretical and Applied Genetics.

[49]  H. S. Jacob,et al.  Aphid Resistance in Medicago truncatula Involves Antixenosis and Phloem-Specific, Inducible Antibiosis, and Maps to a Single Locus Flanked by NBS-LRR Resistance Gene Analogs1 , 2005, Plant Physiology.

[50]  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.

[51]  R. Last,et al.  Characterization of the Arabidopsis TU8 Glucosinolate Mutation,an Allele of TERMINAL FLOWER2 , 2004, Plant Molecular Biology.

[52]  Venkatramana Pegadaraju,et al.  Premature Leaf Senescence Modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 Gene Is Associated with Defense against the Phloem-Feeding Green Peach Aphid1[W] , 2005, Plant Physiology.

[53]  Y. Benjamini,et al.  Controlling the false discovery rate in behavior genetics research , 2001, Behavioural Brain Research.

[54]  G. Jander,et al.  Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. , 2006, The Plant journal : for cell and molecular biology.

[55]  A. Cherqui,et al.  Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. , 2000, Journal of insect physiology.

[56]  Gordon K Smyth,et al.  Statistical Applications in Genetics and Molecular Biology Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments , 2011 .

[57]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[58]  Cecilia Tamborindeguy,et al.  Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design , 2007, BMC Genomics.

[59]  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 .