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- W2527780086 abstract "The two-spotted spider mite Tetranychus urticae is an extremely polyphagous crop pest. Alongside an unparalleled detoxification potential for plant secondary metabolites, it has recently been shown that spider mites can attenuate or even suppress plant defenses. Salivary constituents, notably effectors, have been proposed to play an important role in manipulating plant defenses and might determine the outcome of plant-mite interactions. Here, the proteomic composition of saliva from T. urticae lines adapted to various host plants—bean, maize, soy, and tomato—was analyzed using a custom-developed feeding assay coupled with nano-LC tandem mass spectrometry. About 90 putative T. urticae salivary proteins were identified. Many are of unknown function, and in numerous cases belonging to multimembered gene families. RNAseq expression analysis revealed that many genes coding for these salivary proteins were highly expressed in the proterosoma, the mite body region that includes the salivary glands. A subset of genes encoding putative salivary proteins was selected for whole-mount in situ hybridization, and were found to be expressed in the anterior and dorsal podocephalic glands. Strikingly, host plant dependent expression was evident for putative salivary proteins, and was further studied in detail by micro-array based genome-wide expression profiling. This meta-analysis revealed for the first time the salivary protein repertoire of a phytophagous chelicerate. The availability of this salivary proteome will assist in unraveling the molecular interface between phytophagous mites and their host plants, and may ultimately facilitate the development of mite-resistant crops. Furthermore, the technique used in this study is a time- and resource-efficient method to examine the salivary protein composition of other small arthropods for which saliva or salivary glands cannot be isolated easily. The two-spotted spider mite Tetranychus urticae is an extremely polyphagous crop pest. Alongside an unparalleled detoxification potential for plant secondary metabolites, it has recently been shown that spider mites can attenuate or even suppress plant defenses. Salivary constituents, notably effectors, have been proposed to play an important role in manipulating plant defenses and might determine the outcome of plant-mite interactions. Here, the proteomic composition of saliva from T. urticae lines adapted to various host plants—bean, maize, soy, and tomato—was analyzed using a custom-developed feeding assay coupled with nano-LC tandem mass spectrometry. About 90 putative T. urticae salivary proteins were identified. Many are of unknown function, and in numerous cases belonging to multimembered gene families. RNAseq expression analysis revealed that many genes coding for these salivary proteins were highly expressed in the proterosoma, the mite body region that includes the salivary glands. A subset of genes encoding putative salivary proteins was selected for whole-mount in situ hybridization, and were found to be expressed in the anterior and dorsal podocephalic glands. Strikingly, host plant dependent expression was evident for putative salivary proteins, and was further studied in detail by micro-array based genome-wide expression profiling. This meta-analysis revealed for the first time the salivary protein repertoire of a phytophagous chelicerate. The availability of this salivary proteome will assist in unraveling the molecular interface between phytophagous mites and their host plants, and may ultimately facilitate the development of mite-resistant crops. Furthermore, the technique used in this study is a time- and resource-efficient method to examine the salivary protein composition of other small arthropods for which saliva or salivary glands cannot be isolated easily. The family of spider mites (Chelicerata: Acari: Tetranychidae) comprises well over 1000 species, including several that are important pests on crops, and about 0.9 billion euro is being spent annually for their control worldwide (1..Migeon, A., and Dorkeld, F., (2006–2016) Spider Mites Web: a comprehensive database for the Tetranychidae.Google Scholar, 2.Van Leeuwen T. Tirry L. Yamamoto A. Nauen R. Dermauw W. The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research.Pestic. Biochem. Physiol. 2015; 121: 12-21Crossref PubMed Scopus (115) Google Scholar). These minute herbivores—about 0.5 mm in size—use their stylets to pierce leaf mesophyll cells and to inject saliva, after which they suck out the cytoplasm. This results in cell death visible as chlorotic spots sometimes accompanied by necrosis, and ultimately in leaf abscission (3.Liesering R. Beitrag zum phytopathologischen Wirkungsmechanismus von Tetranychus urticae Koch (Tetranychidae, Acari).Z. Pflanzenkr. Pflanzenschutz. 1960; 67: 524-542Google Scholar, 4.Tomczyk A. Kropczynska D. Effect on the host plant.in: Helle W. Sabelis M.W. Spider mites. their biology, natural enemies and control. Elsevier Science Publishers B.V., Amsterdam, The Netherlands1985: 317-329Google Scholar). Among the spider mites, the two-spotted spider mite, Tetranychus urticae, is the most polyphagous, having been reported on more than 1000 host plant species in more than 140 different families (1..Migeon, A., and Dorkeld, F., (2006–2016) Spider Mites Web: a comprehensive database for the Tetranychidae.Google Scholar). However, not all these host plants are equally suitable to T. urticae, and host plant acceptance can even differ across mite populations (5.Kant M.R. Sabelis M.W. Haring M.A. Schuurink R.C. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences.Proc. R. Soc. Lond. B Biol. Sci. 2008; 275: 443-452Crossref Scopus (108) Google Scholar, 6.van den Boom C.E.M. van Beek T.A. Dicke M. Differences among plant species in acceptance by the spider mite Tetranychus urticae Koch.J. Appl. Entomol. 2003; 127: 177-183Crossref Scopus (75) Google Scholar, 7.Yano S. Wakabayashi M. Takabayashi J. Takafuji A. Factors determining the host plant range of the phytophagous mite, Tetranychus urticae (Acari: Tetranychidae): a method for quantifying host plant acceptance.Exp. Appl. Acarol. 1998; 22: 595-601Crossref Scopus (48) Google Scholar). Important factors determining host plant acceptance by the herbivore are plant defenses, including physical and molecular-chemical barriers that hamper herbivore feeding (8.Kant M.R. Jonckheere W. Knegt B. Lemos F. Liu J. Schimmel B.C. Villarroel C.A. Ataide L.M. Dermauw W. Glas J.J. Egas M. Janssen A. Van Leeuwen T. Schuurink R.C. Sabelis M.W. Alba J.M. Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities.Annals of Botany. 2015; 115: 1015-1051Crossref PubMed Scopus (0) Google Scholar). Different herbivores can induce a different repertoire of defenses and these differential plant responses are set in motion via herbivore-specific signals, predominantly emanating from their saliva (9.Bonaventure G. VanDoorn A. Baldwin I.T. Herbivore-associated elicitors: FAC signaling and metabolism.Trends Plant Sci. 2011; 16: 294-299Abstract Full Text Full Text PDF PubMed Scopus (163) Google Scholar). Plant defenses are regulated by a set of phytohormones, primarily jasmonates (such as jasmonic acid (JA) 1The abbreviations used are:JAJasmonic AcidDEDifferentially ExpressedFCFold ChangeFDRFalse Discovery RateISHIn Situ HybridizationPSMPeptide Spectrum MatchSASalicylic AcidSPSignal PeptideSpCSpectral Counts.) (10.Wasternack C. Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany.Ann. Botany. 2013; 111: 1021-1058Crossref PubMed Scopus (0) Google Scholar), salicylic acid (SA) (11.Caarls L. Pieterse C.M. Van Wees S.C. How salicylic acid takes transcriptional control over jasmonic acid signaling.Front. Plant Sci. 2015; 6: 170Crossref PubMed Scopus (173) Google Scholar, 12.Mur L.A. Kenton P. Atzorn R. Miersch O. Wasternack C. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death.Plant Physiol. 2006; 140: 249-262Crossref PubMed Scopus (547) Google Scholar), and ethylene (13.Pieterse C.M. Leon-Reyes A. Van der Ent S. Van Wees S.C. Networking by small-molecule hormones in plant immunity.Nat. Chem. Biol. 2009; 5: 308-316Crossref PubMed Scopus (1347) Google Scholar). Hormonal interactions are believed to enable the plant to regulate and customize responses under variable biotic and abiotic stress conditions (14.Erb M. Meldau S. Howe G.A. Role of phytohormones in insect-specific plant reactions.Trends Plant Sci. 2012; 17: 250-259Abstract Full Text Full Text PDF PubMed Scopus (471) Google Scholar). Most spider mites induce a mixture of JA- and SA-defenses (15.Kant M.R. Ament K. Sabelis M.W. Haring M.A. Schuurink R.C. Differential timing of spider mite-induced direct and indirect defenses in tomato plants.Plant Physiol. 2004; 135: 483-495Crossref PubMed Scopus (252) Google Scholar, 16.Glas J.J. Alba J.M. Simoni S. Villarroel C.A. Stoops M. Schimmel B.C. Schuurink R.C. Sabelis M.W. Kant M.R. Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities.BMC Biol. 2014; 12: 98Crossref PubMed Scopus (42) Google Scholar, 17.Matsushima R. Ozawa R. Uefune M. Gotoh T. Takabayashi J. Intraspecies variation in the Kanzawa spider mite differentially affects induced defensive response in lima bean plants.J. Chem. Ecol. 2006; 32: 2501-2512Crossref PubMed Scopus (32) Google Scholar, 18.Zhurov V. Navarro M. Bruinsma K.A. Arbona V. Santamaria M.E. Cazaux M. Wybouw N. Osborne E.J. Ens C. Rioja C. Vermeirssen V Rubio-Somoza I. Krishna P. Diaz I. Schmid M. Gómez-Cadenas A. Van de Peer Y. Grbic M. Clark R.M. Van Leeuwen T. Grbic V. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite.Plant Physiol. 2014; 164: 384-399Crossref PubMed Scopus (52) Google Scholar, 19.Alba J.M. Schimmel B.C. Glas J.J. Ataide L.M. Pappas M.L. Villarroel C.A. Schuurink R.C. Sabelis M.W. Kant M.R. Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk.New Phytol. 2015; 205: 828-840Crossref PubMed Scopus (92) Google Scholar) while a role for ethylene remains elusive (20.Kielkiewicz M. Influence of carmine spider mite Tetranychus cinnabarinus Boisd. (Acarida: Tetranychidae) feeding on ethylene production and the activity of oxidative enzymes in damaged tomato plants.in: Bernini F. Nannelli R. Nuzzaci G. de Lillo E. Acarid Phylogeny and Evolution: Adaptation in Mites and Ticks. Springer, Dordrecht, The Netherlands2002: 389-392Crossref Google Scholar). Jasmonic Acid Differentially Expressed Fold Change False Discovery Rate In Situ Hybridization Peptide Spectrum Match Salicylic Acid Signal Peptide Spectral Counts. It is conceivable that some spider mites have evolved traits that enable them to resist (5.Kant M.R. Sabelis M.W. Haring M.A. Schuurink R.C. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences.Proc. R. Soc. Lond. B Biol. Sci. 2008; 275: 443-452Crossref Scopus (108) Google Scholar, 21.Dermauw W. Wybouw N. Rombauts S. Menten B. Vontas J. Grbić M. Clark R.M. Feyereisen R. Van Leeuwen T. A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: E113-E122Crossref PubMed Scopus (0) Google Scholar, 22.Wybouw N. Dermauw W. Tirry L. Stevens C. Grbić M. Feyereisen R. Van Leeuwen T. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning.eLife. 2014; 3: e02365Crossref PubMed Scopus (73) Google Scholar), attenuate (23.Wybouw N. Zhurov V. Martel C. Bruinsma K.A. Hendrickx F. Grbić V. Van Leeuwen T. Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host.Mol. Ecol. 2015; 24: 4647-4663Crossref PubMed Scopus (48) Google Scholar), or suppress JA- (5.Kant M.R. Sabelis M.W. Haring M.A. Schuurink R.C. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences.Proc. R. Soc. Lond. B Biol. Sci. 2008; 275: 443-452Crossref Scopus (108) Google Scholar) and SA-related defenses (24.Sarmento R.A. Lemos F. Bleeker P.M. Schuurink R.C. Pallini A. Oliveira M.G. Lima E.R. Kant M. Sabelis M.W. Janssen A. A herbivore that manipulates plant defence.Ecol. Lett. 2011; 14: 229-236Crossref PubMed Scopus (148) Google Scholar) to maintain a high fitness (19.Alba J.M. Schimmel B.C. Glas J.J. Ataide L.M. Pappas M.L. Villarroel C.A. Schuurink R.C. Sabelis M.W. Kant M.R. Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk.New Phytol. 2015; 205: 828-840Crossref PubMed Scopus (92) Google Scholar). Although it is largely unknown which terminal plant defenses determine resistance or susceptibility to mites, negative correlations were found between mite fitness and several plant secondary metabolites (18.Zhurov V. Navarro M. Bruinsma K.A. Arbona V. Santamaria M.E. Cazaux M. Wybouw N. Osborne E.J. Ens C. Rioja C. Vermeirssen V Rubio-Somoza I. Krishna P. Diaz I. Schmid M. Gómez-Cadenas A. Van de Peer Y. Grbic M. Clark R.M. Van Leeuwen T. Grbic V. Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite.Plant Physiol. 2014; 164: 384-399Crossref PubMed Scopus (52) Google Scholar, 25.Bleeker P.M. Mirabella R. Diergaarde P.J. VanDoorn A. Tissier A. Kant M.R. Prins M. de Vos M. Haring M.A. Schuurink R.C. Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative.Proc. Natl. Acad. Sci. U.S.A. 2012; 109: 20124-20129Crossref PubMed Scopus (138) Google Scholar, 26.Chatzivasileiadis E.A. Sabelis M.W. Toxicity of methyl ketones from tomato trichomes to Tetranychus urticae Koch.Exp. Appl. Acarol. 1997; 21: 473-484Crossref Google Scholar, 27.Jared J.J. Murungi L.K. Wesonga J. Torto B. Steroidal glycoalkaloids: chemical defence of edible African nightshades against the tomato red spider mite, Tetranychus evansi (Acari: Tetranychidae).Pest Manag. Sci. 2015; (10.1002/ps.4100)PubMed Google Scholar). How plants detect spider mite feeding is poorly understood, but analyses of transcriptional networks have suggested the involvement of receptor-like kinases reminiscent of other plant-herbivore interactions (28.Vandoorn A. de Vos M. Resistance to sap-sucking insects in modern-day agriculture.Front. Plant Sci. 2013; 4: 222Crossref PubMed Scopus (13) Google Scholar). These receptors may be involved in the recognition of molecules (elicitors) released during the onset of the plant-pathogen or plant-herbivore interaction (29.Martel C. Zhurov V. Navarro M. Martinez M. Cazaux M. Auger P. Migeon A. Santamaria M.E. Wybouw N. Diaz I. Van Leeuwen T. Navajas M. Grbic M. Grbic V. Tomato whole genome transcriptional response to Tetranychus urticae identifies divergence of spider mite-induced responses between tomato and Arabidopsis.Mol. Plant. Microbe Interact. 2015; 28: 343-361Crossref PubMed Scopus (45) Google Scholar). Many herbivore elicitors emanate from saliva or regurgitation fluids released on or in the plant during feeding (30.Schmelz E.A. Engelberth J. Alborn H.T. Tumlinson 3rd, J.H. Teal P.E. Phytohormone-based activity mapping of insect herbivore-produced elicitors.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 653-657Crossref PubMed Scopus (163) Google Scholar). Reminiscent of phytopathogens (9.Bonaventure G. VanDoorn A. Baldwin I.T. Herbivore-associated elicitors: FAC signaling and metabolism.Trends Plant Sci. 2011; 16: 294-299Abstract Full Text Full Text PDF PubMed Scopus (163) Google Scholar, 31.Boller T. Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.Annu. Rev. Plant Biol. 2009; 60: 379-406Crossref PubMed Scopus (1886) Google Scholar, 32.Jones J.D. Dangl J.L. The plant immune system.Nature. 2006; 444: 323-329Crossref PubMed Scopus (7005) Google Scholar), herbivores evolved additional salivary molecules to counter the induction of defenses (8.Kant M.R. Jonckheere W. Knegt B. Lemos F. Liu J. Schimmel B.C. Villarroel C.A. Ataide L.M. Dermauw W. Glas J.J. Egas M. Janssen A. Van Leeuwen T. Schuurink R.C. Sabelis M.W. Alba J.M. Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities.Annals of Botany. 2015; 115: 1015-1051Crossref PubMed Scopus (0) Google Scholar, 33.Hogenhout S.A. Bos J.I. Effector proteins that modulate plant–insect interactions.Curr. Opin. Plant Biol. 2011; 14: 422-428Crossref PubMed Scopus (0) Google Scholar, 34.Acevedo F.E. Rivera-Vega L.J. Chung S.H. Ray S. Felton G.W. Cues from chewing insects—the intersection of DAMPs, HAMPs, MAMPs and effectors.Curr. Opin. Plant Biol. 2015; 26: 80-86Crossref PubMed Scopus (83) Google Scholar). Such molecules, enhancing herbivore performance, were originally referred to as “effectors.” Some plant varieties have however evolved the means to recognize these effectors, effectively turning them into elicitors which activate plant defense responses (32.Jones J.D. Dangl J.L. The plant immune system.Nature. 2006; 444: 323-329Crossref PubMed Scopus (7005) Google Scholar, 35.Hogenhout S.A. Van der Hoorn R.A. Terauchi R. Kamoun S. Emerging concepts in effector biology of plant-associated organisms.Mol. Plant. Microbe Interact. 2009; 22: 115-122Crossref PubMed Scopus (448) Google Scholar, 36.Lapin D. Van den Ackerveken G. Susceptibility to plant disease: more than a failure of host immunity.Trends Plant Sci. 2013; 18: 546-554Abstract Full Text Full Text PDF PubMed Google Scholar). Because of this context-dependence (37.Schmelz E.A. Huffaker A. Carroll M.J. Alborn H.T. Ali J.G. Teal P.E. An amino acid substitution inhibits specialist herbivore production of an antagonist effector and recovers insect-induced plant defenses.Plant Physiol. 2012; 160: 1468-1478Crossref PubMed Scopus (21) Google Scholar), a broader inclusive definition of the term effector was suggested (35.Hogenhout S.A. Van der Hoorn R.A. Terauchi R. Kamoun S. Emerging concepts in effector biology of plant-associated organisms.Mol. Plant. Microbe Interact. 2009; 22: 115-122Crossref PubMed Scopus (448) Google Scholar). Effectors are defined as pathogen- or herbivore-secreted proteins and small molecules that alter host-cell structure and function. Effectors are of high interest to the plant breeding industry because they can lead to the identification of resistance genes (R genes) (38.Bent A.F. Mackey D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions.Annu. Rev. Phytopathol. 2007; 45: 399-436Crossref PubMed Scopus (540) Google Scholar) and susceptibility genes (S genes) (39.van Schie C.C. Takken F.L. Susceptibility genes 101: how to be a good host.Annu. Rev. Phytopathol. 2014; 52: 551-581Crossref PubMed Scopus (208) Google Scholar). R genes code for immune receptors, which confer recognition of pathogen- or herbivore-derived effectors or their modification inflicted on a host protein, eventually resulting in the activation of host defenses (39.van Schie C.C. Takken F.L. Susceptibility genes 101: how to be a good host.Annu. Rev. Phytopathol. 2014; 52: 551-581Crossref PubMed Scopus (208) Google Scholar). S genes, on the other hand, can considered to be all plant genes that facilitate infection and support compatibility (39.van Schie C.C. Takken F.L. Susceptibility genes 101: how to be a good host.Annu. Rev. Phytopathol. 2014; 52: 551-581Crossref PubMed Scopus (208) Google Scholar). The vast majority of herbivore effectors emanate from saliva. Silencing salivary effectors in non-arthropod herbivores like nematodes has been shown to reduce their performance (40.Elling A.A. Jones J.T. Functional characterization of nematode effectors in plants.Methods Mol. Biol. 2014; 1127: 113-124Crossref PubMed Scopus (9) Google Scholar). Likewise, silencing salivary effectors in insects like aphids reduced their reproduction (41.Coleman A.D. Wouters R.H. Mugford S.T. Hogenhout S.A. Persistence and transgenerational effect of plant-mediated RNAi in aphids.J. Exp. Bot. 2015; 66: 541-548Crossref PubMed Scopus (50) Google Scholar). These studies indicate that salivary components are key players in the plant-herbivore molecular battlefield, and hence their identification is a high priority. Salivary proteins can be inferred from genomic, transcriptomic and/or proteomic data using a combination of criteria. For example, combining temporal and spatial gene expression data with the predicted presence of an N-terminal signal peptide (SP) in the corresponding proteins results in lists of putative salivary proteins (e.g. (42.Bos J.I. Prince D. Pitino M. Maffei M.E. Win J. Hogenhout S.A. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid).PLoS Genet. 2010; 6: e1001216Crossref PubMed Scopus (292) Google Scholar, 43.Carolan J.C. Caragea D. Reardon K.T. Mutti N.S. Dittmer N. Pappan K. Cui F. Castaneto M. Poulain J. Dossat C. Tagu D. Reese J.C. Reeck G.R. Wilkinson T.L. Edwards O.R. Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach.J. Proteome Res. 2011; 10: 1505-1518Crossref PubMed Scopus (164) Google Scholar)). For T. urticae, an annotated genome is available (44.Grbić M. Van Leeuwen T. Clark R.M. Rombauts S. Rouzé P. Grbić V. Osborne E.J. Dermauw W. Ngoc P.C. Ortego F. Hernández-Crespo P. Diaz I. Martinez M. Navajas M. Sucena É. Magalhães S. Nagy L. Pace R.M. Djuranović S. Smagghe G. Iga M. Christiaens O. Veenstra J.A. Ewer J. Villalobos R.M. Hutter J.L. Hudson S.D. Velez M. Yi S.V. Zeng J. Pires-daSilva A. Roch F. Cazaux M. Navarro M. Zhurov V. Acevedo G. Bjelica A. Fawcett J.A. Bonnet E. Martens C. Baele G. Wissler L. Sanchez-Rodriguez A. Tirry L. Blais C. Demeestere K. Henz S.R. Gregory T.R. Mathieu J. Verdon L. Farinelli L. The genome of Tetranychus urticae reveals herbivorous pest adaptations.Nature. 2011; 479: 487-492Crossref PubMed Scopus (0) Google Scholar), but no salivary gland-specific transcriptome and/or proteome has been obtained yet. It is known that spider mites inject salivary substances into host plant leaves (45.Avery D.J. Briggs J.B. The aetiology and development of damage in young fruit trees infested with fruit tree red spider mite, Panonychus ulmi (Koch).Ann. Appl. Biol. 1968; 61: 277-288Crossref Scopus (26) Google Scholar, 46.Rodriguez J.G. Radiophosphorus in Metabolism Studies in the Two-spotted Spider Mite.J. Econ. Entomol. 1954; 47: 514-517Crossref Google Scholar, 47.Storms J.J.H. Some physiological effects of spider mite infestation on bean plants.Neth. J. Plant Path. 1971; 77: 154-167Crossref Scopus (28) Google Scholar). However, the proteomic composition of these substances has yet to be elucidated. The generation of gland specific transcriptomes and proteomes is hampered by the extremely small size of spider mites and the complex morphology of the glands (48.Mothes U. Seitz K. Fine structure and function of the prosomal glands of the two-spotted spider mite, Tetranychus urticae (Acari, Tetranychidae).Cell Tissue Res. 1981; 221: 339-349Crossref PubMed Scopus (28) Google Scholar) (T. urticae adults have a body length of 400–500 μm with an approximate salivary gland length of 50 μm). Salivation of several eriophyid mite species has been achieved by soaking adult mites into immersion oil (49.De Lillo E. Monfreda R. ‘Salivary secretions’ of eriophyoids (Acari: Eriophyoidea): first results of an experimental model.Exp. Appl. Acarol. 2004; 34: 291-306PubMed Google Scholar), and of Varroa destructor mites by topical application of cholinomimetic agents (50.Richards E.H. Jones B. Bowman A. Salivary secretions from the honeybee mite, Varroa destructor: effects on insect haemocytes and preliminary biochemical characterization.Parasitology. 2011; 138: 602-608Crossref PubMed Scopus (0) Google Scholar). Protein sequences were not obtained in these studies, however. A successful approach for obtaining sufficient amounts of salivary secretions suitable for protein analysis from nonmite arthropods has been to collect secretions from artificial diets encapsulated by a membrane on which feeding has taken place. For example, using this approach, multiple proteins, in a range from 10 to 100, have been identified in the secreted saliva of aphids (51.Nicholson S.J. Hartson S.D. Puterka G.J. Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat.J. Proteomics. 2012; 75: 2252-2268Crossref PubMed Scopus (97) Google Scholar, 52.Vandermoten S. Harmel N. Mazzucchelli G. De Pauw E. Haubruge E. Francis F. Comparative analyses of salivary proteins from three aphid species.Insect Mol. Biol. 2014; 23: 67-77Crossref PubMed Scopus (0) Google Scholar) and true bugs (53.Cooper W.R. Nicholson S.J. Puterka G.J. Salivary Proteins of Lygus hesperus (Hemiptera: Miridae).Ann. Entomol. Soc. Am. 2013; 106: 86-92Crossref Scopus (21) Google Scholar). We developed a set-up for collecting salivary secretions of T. urticae from artificial diet and analyzed the proteomic composition of these secretions. Our approach involved T. urticae lines that were reared on distinct economically important host plants for more than five generations, a period during which adaptation usually occurs (54.Fry J. Evolutionary adaptation to host plants in a laboratory population of the phytophagous mite Tetranychus urticae Koch.Oecologia. 1989; 81: 559-565Crossref PubMed Scopus (58) Google Scholar). By including lines adapted to different hosts, we aimed to discover a broader spectrum of salivary proteins. Mite salivary secretions were harvested using a custom-developed mite feeding assay and subsequently investigated by nano-LC-MS/MS analysis. Additionally, a transcriptome of the proterosoma—harboring the salivary glands—was constructed to validate proteomic data. Evidence for the salivary origin of a selection of identified proteins was obtained by whole-mount in situ hybridizations (ISHs). Furthermore, to assess host-specificity of salivary gland productions, we investigated the host-dependence of expression of genes coding for the identified putative salivary proteins. The results from this study lay the groundwork for an improved understanding of the molecular machinery behind induction or suppression of resistance during plant-mite interactions, and may open new opportunities for mite-resistance plant breeding. The T. urticae London strain has been maintained under laboratory conditions on bean plants (Phaseolus vulgaris cv. “Prelude,” Fabaceae) for many years. The genome of this London strain has been sequenced (44.Grbić M. Van Leeuwen T. Clark R.M. Rombauts S. Rouzé P. Grbić V. Osborne E.J. Dermauw W. Ngoc P.C. Ortego F. Hernández-Crespo P. Diaz I. Martinez M. Navajas M. Sucena É. Magalhães S. Nagy L. Pace R.M. Djuranović S. Smagghe G. Iga M. Christiaens O. Veenstra J.A. Ewer J. Villalobos R.M. Hutter J.L. Hudson S.D. Velez M. Yi S.V. Zeng J. Pires-daSilva A. Roch F. Cazaux M. Navarro M. Zhurov V. Acevedo G. Bjelica A. Fawcett J.A. Bonnet E. Martens C. Baele G. Wissler L. Sanchez-Rodriguez A. Tirry L. Blais C. Demeestere K. Henz S.R. Gregory T.R. Mathieu J. Verdon L. Farinelli L. The genome of Tetranychus urticae reveals herbivorous pest adaptations.Nature. 2011; 479: 487-492Crossref PubMed Scopus (0) Google Scholar). Lines on alternative host plants were established by transferring ∼250 adult female mites from the London strain on bean to new hosts. These new host plants were cotton (Gossypium hirsutum, Malvaceae), maize (Zea mays, cv. “Ronaldinio,” Poaceae), soy (Glycine max, cv. “Merlin,” Fabaceae), and tomato (Solanum lycopersicum, cv “Moneymaker,” Solanaceae). Three independent lines were generated for cotton and tomato, whereas four independent lines were obtained for maize and soy. The mite lines were maintained in a climatically controlled environment at 26 °C with 60% RH, and a light/dark (L:D) photoperiod of 16:8 h. Mites were offered fresh plants as needed, and were used in experiments after 5 generations for all hosts, except tomato, where replicate lines derived from London were adapted and maintained on tomato for over 30 generations (23.Wybouw N. Zhurov V. Martel C. Bruinsma K.A. Hendrickx F. Grbić V. Van Leeuwen T. Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host.Mol. Ecol. 2015; 24: 4647-4663Crossref PubMed Scopus (48) Google Scholar). To collect saliva, spider mites were allowed to feed on an artificial diet. Briefly, a pocket-like invagination was made in stretched Parafilm® M (Sigma, Bornem, Belgium) using a custom built vacuum device (see supplemental Fig. S1), consisting of a 96-well plate (plate thickness 4.2 mm, hole diameter 4.5 mm) fitting on a vacuum manifold plate (Analytical Research Systems, Micanopy, FL) connected to a vacuum pump (model N 035.1.2 A_.18, KNF Neuberger, Freiburg, Germany). Next, 70 μl sterile holidic artificial diet (1/30 diluted aphid diet, (55.Febvay G. Delobel B. Rahbé Y. Influence of the amino acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera: Aphididae).Can. J. Zool. 1988; 66: 2449-2453Crossref Google Scholar)) supp" @default.
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- W2527780086 date "2016-12-01" @default.
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- W2527780086 title "The Salivary Protein Repertoire of the Polyphagous Spider Mite Tetranychus urticae: A Quest for Effectors" @default.
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