{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,16]],"date-time":"2026-02-16T08:38:35Z","timestamp":1771231115003,"version":"3.50.1"},"reference-count":57,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2018,6,15]],"date-time":"2018-06-15T00:00:00Z","timestamp":1529020800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Sara Magalh\u00e3es","award":["COMPCON GA 725419"],"award-info":[{"award-number":["COMPCON GA 725419"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Some herbivores suppress plant defenses, which may be viewed as a result of the coevolutionary arms race between plants and herbivores. However, this ability is usually studied in a one-herbivore-one-plant system, which hampers comparative studies that could corroborate this hypothesis. Here, we extend this paradigm and ask whether the herbivorous spider-mite Tetranychus evansi, which suppresses the jasmonic-acid pathway in tomato plants, is also able to suppress defenses in other host plants at different phylogenetic distances from tomatoes. We test this using different plants from the Solanales order, namely tomato, jimsonweed, tobacco, and morning glory (three Solanaceae and one Convolvulaceae), and bean plants (Fabales). First, we compare the performance of T. evansi to that of the other two most-commonly found species of the same genus, T. urticae and T. ludeni, on several plants. We found that the performance of T. evansi is higher than that of the other species only on tomato plants. We then showed, by measuring trypsin inhibitor activity and life history traits of conspecific mites on either clean or pre-infested plants, that T. evansi can suppress plant defenses on all plants except tobacco. This study suggests that the suppression of plant defenses may occur on host plants other than those to which herbivores are adapted.<\/jats:p>","DOI":"10.3390\/ijms19061783","type":"journal-article","created":{"date-parts":[[2018,6,15]],"date-time":"2018-06-15T11:21:20Z","timestamp":1529061680000},"page":"1783","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants"],"prefix":"10.3390","volume":"19","author":[{"given":"J\u00e9ssica T.","family":"Paulo","sequence":"first","affiliation":[{"name":"cE3c Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1649-004 Lisboa, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Diogo P.","family":"Godinho","sequence":"additional","affiliation":[{"name":"cE3c Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1649-004 Lisboa, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4904-7470","authenticated-orcid":false,"given":"Anabela","family":"Silva","sequence":"additional","affiliation":[{"name":"BioISI, Biosystems and Integrative Sciences Institute, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1649-004 Lisboa, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8294-7924","authenticated-orcid":false,"given":"Cristina","family":"Branquinho","sequence":"additional","affiliation":[{"name":"cE3c Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1649-004 Lisboa, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara","family":"Magalh\u00e3es","sequence":"additional","affiliation":[{"name":"cE3c Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ci\u00eancias, Universidade de Lisboa, 1649-004 Lisboa, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2018,6,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/S0169-5347(98)01576-6","article-title":"The ecology and evolution of plant tolerance to herbivory","volume":"14","author":"Strauss","year":"1999","journal-title":"Trends Ecol. Evol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1146\/annurev.es.20.110189.001555","article-title":"Induced Plant Responses to Herbivory","volume":"20","author":"Karban","year":"1989","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1146\/annurev.ecolsys.33.010802.150443","article-title":"Herbivore Offense","volume":"33","author":"Karban","year":"2002","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"586","DOI":"10.2307\/2406212","article-title":"Butterflies and Plants: A Study in Coevolution","volume":"18","author":"Ehrlich","year":"1964","journal-title":"Evolution"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1146\/annurev.ento.48.091801.112629","article-title":"Contact chemoreception in feeding by Phytophagous Insects","volume":"48","author":"Chapman","year":"2003","journal-title":"Annu. Rev. Entomol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.phytochem.2003.10.016","article-title":"Cyanogenic glucosides and plant\u2013insect interactions","volume":"65","author":"Zagrobelny","year":"2004","journal-title":"Phytochemistry"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1111\/j.1365-313X.2005.02623.x","article-title":"Using \u2018mute\u2019 plants to translate volatile signals","volume":"45","author":"Paschold","year":"2006","journal-title":"Plant J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/S0965-1748(00)00024-2","article-title":"Inducible P450s of the CYP9 family from larval Manduca sexta midgut","volume":"30","author":"Stevens","year":"2000","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1349","DOI":"10.1023\/A:1016292317948","article-title":"Dietary and developmental influences on induced detoxification in an oligophage","volume":"28","author":"Cianfrogna","year":"2002","journal-title":"J. Chem. Ecol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1038\/nature01003","article-title":"Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes","volume":"419","author":"Li","year":"2002","journal-title":"Nature"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1038\/416599a","article-title":"Caterpillar saliva beats plant defences","volume":"416","author":"Musser","year":"2002","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kant, M.R., Sabelis, M.W., Haring, M.A., and Schuurink, R.C. (2008). Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc. R. Soc. B, 443\u2013452.","DOI":"10.1098\/rspb.2007.1277"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1111\/1365-2435.12405","article-title":"The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato","volume":"29","author":"Su","year":"2015","journal-title":"Funct. Ecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1111\/j.1365-2435.2011.01902.x","article-title":"Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: From insect performance to gene transcription","volume":"26","author":"Soler","year":"2012","journal-title":"Funct. Ecol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/j.1461-0248.2010.01575.x","article-title":"A herbivore that manipulates plant defence","volume":"14","author":"Sarmento","year":"2011","journal-title":"Ecol. Lett."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s00442-015-3434-z","article-title":"Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics","volume":"180","author":"Godinho","year":"2016","journal-title":"Oecologia"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1016\/j.pbi.2011.05.003","article-title":"Effector proteins that modulate plant-insect interactions","volume":"14","author":"Hogenhout","year":"2011","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1080\/17429145.2010.551670","article-title":"Avoidance and suppression of plant defenses by herbivores and pathogens","volume":"6","author":"Alba","year":"2011","journal-title":"J. Plant Interact."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.cois.2016.01.002","article-title":"Jasmonate signalling in plants shapes plant-insect interaction ecology","volume":"14","author":"Lortzing","year":"2016","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1146\/annurev.arplant.53.100301.135207","article-title":"Plant Responses to Insect Herbivory: The EmergingMolecular Analysis","volume":"53","author":"Kessler","year":"2002","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1007\/s10886-010-9854-7","article-title":"Molecular, Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds","volume":"36","author":"Musser","year":"2010","journal-title":"J. Chem. Ecol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1007\/s00442-011-2015-z","article-title":"An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores","volume":"167","author":"Kliebenstein","year":"2011","journal-title":"Oecologia"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/arch.20039","article-title":"Evidence That the Caterpillar Salivary Enzyme Glucose Oxidase Provides Herbivore Offense in Solanaceous Plants","volume":"137","author":"Musser","year":"2005","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1007\/BF00216738","article-title":"Fine structure and function of the prosomal glands of the two-spotted spider mite, Tetranychus urticae (Acari, Tetranychidae)","volume":"221","author":"Mothes","year":"1981","journal-title":"Cell Tissue Res."},{"key":"ref_25","unstructured":"Helle, W., and Sabelis, M.W. (1985). Spider Mites Their Biology, Natural Enemies and Control, Elsevier."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1104\/pp.103.038315","article-title":"Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants","volume":"135","author":"Kant","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"4647","DOI":"10.1111\/mec.13330","article-title":"Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host","volume":"24","author":"Wybouw","year":"2015","journal-title":"Mol. Ecol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1093\/aob\/mcv054","article-title":"Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities","volume":"115","author":"Kant","year":"2015","journal-title":"Ann. Bot."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1104\/pp.005314","article-title":"Resistance of Cultivated Tomato to Cell Content-Feeding Herbivores Is Regulated by the Octadecanoid-Signaling Pathway","volume":"130","author":"Li","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1104\/pp.104.048694","article-title":"Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato","volume":"135","author":"Ament","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1371\/journal.pone.0043011","article-title":"Gene pyramiding of peptidase inhibitors enhances plant resistance to the spider mite Tetranychus urticae","volume":"7","author":"Santamaria","year":"2012","journal-title":"PLoS ONE"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1111\/nph.13075","article-title":"Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk","volume":"205","author":"Alba","year":"2015","journal-title":"New Phytol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Eich, E. (2008). Solanaceae and Convolvulaceae: Secondary Metabolites, Springer Science & Business Media.","DOI":"10.1007\/978-3-540-74541-9"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Migeon, A., Nouguier, E., Dorkeld, F., Cbgp, U.M.R., Ird, I., Montpellier, C., and Cedex, M. (2010). Spider Mites Web: A comprehensive database for the Tetranychidae Alain. Trends Acarol., 557\u2013560.","DOI":"10.1007\/978-90-481-9837-5_96"},{"key":"ref_35","first-page":"fiy015","article-title":"Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe","volume":"94","author":"Santos","year":"2018","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1755","DOI":"10.1104\/pp.103.024323","article-title":"Convergent Responses to Stress. Solar Ultraviolet-B Radiation and Manduca sexta Herbivory Elicit Overlapping Transcriptional Responses in Field-Grown Plants of Nicotiana longiflora","volume":"132","author":"Izaguirre","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1093\/aob\/mcl226","article-title":"Solar Ultraviolet-B Radiation and Insect Herbivory Trigger Partially Overlapping Phenolic Responses in Nicotiana attenuata and Nicotiana longiflora","volume":"99","author":"Izaguirre","year":"2007","journal-title":"Ann. Bot."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1073\/pnas.0305096101","article-title":"Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata","volume":"101","author":"Zavala","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","first-page":"181","article-title":"Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): Clonning, functional expression, and induction by wounding and herbivory","volume":"1","author":"Haruta","year":"2001","journal-title":"Plant Mol. Biol."},{"key":"ref_40","first-page":"1197","article-title":"JIPs and RIPs: The Regulation of Plant Gene Expression by Jasmonates in Response to Environmental Cues and Pathogens","volume":"6","author":"Reinbothe","year":"1994","journal-title":"Plant Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1104\/pp.59.3.437","article-title":"Wound-induced Accumulation of Trypsin Inhibitor Activities in Plant Leaves: Survey of Several Plant Genera","volume":"59","author":"Ryan","year":"1977","journal-title":"Plant Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1007\/s002990050304","article-title":"Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura","volume":"16","author":"Yeh","year":"1997","journal-title":"Plant Cell Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1038\/21420","article-title":"Jasmonate-inducible plant defences cause increased parasitism of herbivores","volume":"399","author":"Thaler","year":"1999","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1023\/A:1005540107957","article-title":"Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus","volume":"26","author":"Cipollini","year":"2000","journal-title":"J. Chem. Ecol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1023\/A:1010384805014","article-title":"Plant density and nutrient availability constrain constitutive and wound-induced expression of trypsin inhibitors in Brassica napus","volume":"27","author":"Cipollini","year":"2001","journal-title":"J. Chem. Ecol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1111\/j.1461-0248.2004.00684.x","article-title":"Conceptual issues in local adaptation","volume":"7","author":"Kawecki","year":"2004","journal-title":"Ecol. Lett."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1104\/pp.010762","article-title":"An Ecologically Motivated Analysis of Plant-Herbivore Interactions in Native Tobacco","volume":"127","author":"Baldwin","year":"2001","journal-title":"Plant Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2653","DOI":"10.1111\/j.1420-9101.2011.02388.x","article-title":"Environmental effects on the detection of adaptation","volume":"24","author":"Blanchet","year":"2011","journal-title":"J. Evol. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.jinsphys.2015.05.002","article-title":"Digestive proteases in bodies and faeces of the two-spotted spider mite, Tetranychus urticae","volume":"78","author":"Grbic","year":"2015","journal-title":"J. Insect Physiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00442-015-3344-0","article-title":"Herbivores with similar feeding modes interact through the induction of different plant responses","volume":"180","author":"Pallini","year":"2016","journal-title":"Oecologia"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Kassell, B., Radicevic, M., Berlow, S., Pea, R.J., and Laskowski, M. (1970). Bovine Trypsin-Kallikrein Inhibitor (Kunitz Inhibitor, Basic Pancreatic Trypsin Inhibitor, Polyvalent Inhibitor from Bovine Organs), Academic Press.","DOI":"10.1016\/0076-6879(70)19074-4"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/bimj.200810425","article-title":"Simultaneous Inference in General Parametric Models","volume":"50","author":"Hothorn","year":"2008","journal-title":"Biom. J."},{"key":"ref_54","unstructured":"Therneau, T.M. (2012). coxme: Mixed Effects Cox Models. R-Package Descr., 1\u201314."},{"key":"ref_55","unstructured":"Crawley, M.J. (2012). The R Book, John Wiley & Sons."},{"key":"ref_56","first-page":"1","article-title":"Fitting linear mixed-effects models using lme4","volume":"67","author":"Bates","year":"2014","journal-title":"J. Stat. Softw."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1080\/10556788.2011.597854","article-title":"AD Model Builder: Using automatic differentiation for statistical inference of highly parameterized complex nonlinear models","volume":"27","author":"Fournier","year":"2012","journal-title":"Optim. Methods Softw."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/19\/6\/1783\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:08:56Z","timestamp":1760195336000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/19\/6\/1783"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,6,15]]},"references-count":57,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2018,6]]}},"alternative-id":["ijms19061783"],"URL":"https:\/\/doi.org\/10.3390\/ijms19061783","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,6,15]]}}}