{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,1]],"date-time":"2025-10-01T16:18:27Z","timestamp":1759335507658,"version":"3.37.3"},"reference-count":38,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2020,9,16]],"date-time":"2020-09-16T00:00:00Z","timestamp":1600214400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100008982","name":"National Science Foundation","doi-asserted-by":"publisher","award":["NSF-DEB 1256769"],"award-info":[{"award-number":["NSF-DEB 1256769"]}],"id":[{"id":"10.13039\/501100008982","id-type":"DOI","asserted-by":"publisher"}]},{"name":"USDA McIntire-Stennis","award":["RI0017-MS979"],"award-info":[{"award-number":["RI0017-MS979"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,10,17]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Hemlock woolly adelgid is an invasive piercing-sucking insect in eastern North America, which upon infestation of its main host, eastern hemlock (\u2018hemlock\u2019), improves attraction and performance of folivorous insects on hemlock. This increased performance may be mediated by hemlock woolly adelgid feeding causing antagonism between the the jasmonic acid and other hormone pathways. In a common garden experiments using hemlock woolly adelgid infestation and induction with methyl jasmonate (MeJA) and measures of secondary metabolite contents and defense-associated enzyme activities, we explored the impact of hemlock woolly adelgid feeding on the local and systemic induction of jasmonic acid (JA)-elicited defenses. We found that in local tissue hemlock woolly adelgid or MeJA exposure resulted in unique induced phenotypes, whereas the combined treatment resulted in an induced phenotype that was a mixture of the two individual treatments. We also found that if the plant was infested with hemlock woolly adelgid, the systemic response of the plant was dominated by hemlock woolly adelgid, regardless of whether MeJA was applied. Interestingly, in the absence of hemlock woolly adelgid, hemlock plants had a very weak systemic response to MeJA. We conclude that hemlock woolly adelgid infestation prevents systemic induction of JA-elicited defenses. Taken together, compromised local JA-elicited defenses combined with weak systemic induction could be major contributors to increased folivore performance on hemlock woolly adelgid-infested hemlock.<\/jats:p>","DOI":"10.1093\/ee\/nvaa104","type":"journal-article","created":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T19:21:51Z","timestamp":1597346511000},"page":"1226-1231","source":"Crossref","is-referenced-by-count":2,"title":["Impact of Hemlock Woolly Adelgid (Hemiptera: Adelgidae) Infestation on the Jasmonic Acid-Elicited Defenses of Tsuga canadensis (Pinales: Pinaceae)"],"prefix":"10.1093","volume":"49","author":[{"given":"Chad M","family":"Rigsby","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ian G","family":"Kinahan","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amelia","family":"May","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amy","family":"Kostka","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nick","family":"Houseman","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Suzanne K","family":"Savage","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elizabeth R","family":"Whitney","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evan L","family":"Preisser","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, The University of Rhode Island, Kingston, RI"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2020,9,16]]},"reference":[{"key":"2020101711052321700_CIT0001","doi-asserted-by":"crossref","first-page":"8113","DOI":"10.1073\/pnas.95.14.8113","article-title":"Jasmonate-induced responses are costly but benefit plants under attack in native populations","volume":"95","author":"Baldwin","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2020101711052321700_CIT0002","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1055\/s-2005-872705","article-title":"Fine-tuning plant defence signaling: Salicylate versus jasmonate","volume":"8","author":"Beckers","year":"2006","journal-title":"Plant. Biol"},{"key":"2020101711052321700_CIT0003","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: a practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. B"},{"key":"2020101711052321700_CIT0004","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1111\/j.1461-9563.2007.00334.x","article-title":"Factors effecting settlement rate of the hemlock woolly adelgid, Adelges tsugae","volume":"9","author":"Butin","year":"2007","journal-title":"Agric. For. Entomol"},{"key":"2020101711052321700_CIT0005","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.postharvbio.2005.12.017","article-title":"Effect of salicylic acid on phenylpropanoids and phenylalanine ammonia-lyase in harvested grape berries","volume":"40","author":"Chen","year":"2006","journal-title":"Postharvest Biol. Tec"},{"key":"2020101711052321700_CIT0006","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1890\/02-0615","article-title":"Stretching the limits of plasticity: can a plant defend against both competitors and herbivores?","volume":"85","author":"Cipollini","year":"2004","journal-title":"Ecology"},{"key":"2020101711052321700_CIT0007","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1242\/dev.087650","article-title":"Gibberellin signaling in plants","volume":"140","author":"Davi\u00e8re","year":"2013","journal-title":"Development"},{"key":"2020101711052321700_CIT0008","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.molp.2015.09.011","article-title":"A pivotal role of DELLAs in regulating multiple hormone signals","volume":"9","author":"Davi\u00e8re","year":"2016","journal-title":"Mol. Plant"},{"key":"2020101711052321700_CIT0009","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/BF02059604","article-title":"Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper","volume":"20","author":"Felton","year":"1994","journal-title":"J. Chem. Ecol"},{"key":"2020101711052321700_CIT0010","doi-asserted-by":"crossref","first-page":"10242","DOI":"10.3390\/ijms140510242","article-title":"Plant defense against insect herbivores","volume":"14","author":"F\u00fcrstenberg-H\u00e4gg","year":"2013","journal-title":"Int. J. Mol. Sci"},{"key":"2020101711052321700_CIT0011","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1007\/s00442-007-0792-1","article-title":"Costs and benefits of induced resistance in a clonal plant network","volume":"153","author":"G\u00f3mez","year":"2007","journal-title":"Oecologia"},{"key":"2020101711052321700_CIT0037","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1007\/s00442-012-2267-2","article-title":"Exotic herbivores on a shared host: tissue quality after individual, simultaneous, and sequential attack","volume":"169","author":"G\u00f3mez","year":"2012","journal-title":"Oecologia"},{"key":"2020101711052321700_CIT0012","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1080\/11956860.2000.11682573","article-title":"Understory microclimate and photosynthetic response of saplings in an old-growth eastern hemlock (Tsuga canadensis L.) forest","volume":"7","author":"Hadley","year":"2000","journal-title":"Ecoscience"},{"key":"2020101711052321700_CIT0013","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1007\/s00114-006-0129-7","article-title":"Induced resistance enzymes in wild plants-do \u2018early birds\u2019 escape from pathogen attack?","volume":"93","author":"Heil","year":"2006","journal-title":"Naturwissenschaften"},{"key":"2020101711052321700_CIT0014","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.tplants.2008.03.005","article-title":"Long-distance signalling in plant defence","volume":"13","author":"Heil","year":"2008","journal-title":"Trends Plant Sci"},{"key":"2020101711052321700_CIT0015","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/S0065-2296(09)51015-4","article-title":"Ecological consequences of plant defense signaling,","volume-title":"Advances in botanical research Vol. 51","author":"Heil","year":"2009"},{"key":"2020101711052321700_CIT0016","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1093\/ee\/nvu012","article-title":"Effects of light and water availability on the performance of hemlock woolly Adelgid (Hemiptera: Adelgidae)","volume":"44","author":"Hickin","year":"2015","journal-title":"Environ. Entomol"},{"key":"2020101711052321700_CIT0017","doi-asserted-by":"crossref","first-page":"730","DOI":"10.4236\/ajac.2014.511081","article-title":"Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide","volume":"5","author":"Junglee","year":"2014","journal-title":"Am. J. Anal. Chem"},{"key":"2020101711052321700_CIT0018","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":"2020101711052321700_CIT0032","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1111\/een.12829","article-title":"Facilitation between invasive herbivores: hemlock woolly adelgid increases gypsy moth preference for and performance on eastern hemlock","volume":"45","author":"Kinahan","year":"2019","journal-title":"Ecol. Entomol"},{"key":"2020101711052321700_CIT0019","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1038\/nature06520","article-title":"A molecular framework for light and gibberellin control of cell elongation","volume":"451","author":"de Lucas","year":"2008","journal-title":"Nature"},{"key":"2020101711052321700_CIT0020","first-page":"1","article-title":"Caterpillars on the foliage of conifers in the Northeastern United States (Revised)","author":"Maier","year":"2011","journal-title":"USDA FHTET-2011-07"},{"key":"2020101711052321700_CIT0021","doi-asserted-by":"crossref","first-page":"2034","DOI":"10.1111\/1365-2435.12911","article-title":"Spatial and temporal components of induced plant responses in the context of herbivore life history and impact on host","volume":"31","author":"Mason","year":"2017","journal-title":"Funct. Ecol"},{"key":"2020101711052321700_CIT0022","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3389\/fpls.2013.00043","article-title":"The identification and differential expression of Eucalyptus grandis pathogenesis-related genes in response to salicylic acid and methyl jasmonate","volume":"4","author":"Naidoo","year":"2013","journal-title":"Front. Plant Sci"},{"key":"2020101711052321700_CIT0023","doi-asserted-by":"crossref","first-page":"2231","DOI":"10.1007\/s10886-005-7099-7","article-title":"Herbivores, vascular pathways, and systemic induction: facts and artifacts","volume":"31","author":"Orians","year":"2005","journal-title":"J. Chem. Ecol"},{"key":"2020101711052321700_CIT0033","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1603\/EN13358","article-title":"Hemlock woolly adelgid (Hemiptera: Adelgidae) induces twig volatiles of eastern hemlock in a forest setting","volume":"43","author":"Pezet","year":"2014","journal-title":"Environ. Entomol"},{"key":"2020101711052321700_CIT0034","doi-asserted-by":"crossref","first-page":"1090","DOI":"10.1007\/s10886-013-0300-5","article-title":"Hemlock woolly adelgid and elongate hemlock scale induce changes in foliar and twig volatiles of eastern hemlock","volume":"39","author":"Pezet","year":"2013","journal-title":"J. Chem. Ecol"},{"key":"2020101711052321700_CIT0035","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1007\/s10886-011-9962-z","article-title":"Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis)","volume":"37","author":"Radville","year":"2011","journal-title":"J. Chem. Ecol"},{"key":"2020101711052321700_CIT0024","doi-asserted-by":"crossref","first-page":"1791","DOI":"10.1111\/pce.12985","article-title":"Defence syndromes in lodgepole - whitebark pine ecosystems relate to degree of historical exposure to mountain pine beetles","volume":"40","author":"Raffa","year":"2017","journal-title":"Plant. Cell Environ"},{"volume-title":"R: A Language and Environment for Statistical Computing","year":"2020","author":"R Development Core Team.","key":"2020101711052321700_CIT0036"},{"key":"2020101711052321700_CIT0025","doi-asserted-by":"crossref","first-page":"219","DOI":"10.3390\/plants8070219","article-title":"Using game theory to understand systemic acquired resistance as a bet-hedging option for increasing fitness when disease is uncertain","volume":"8","author":"Reynolds","year":"2019","journal-title":"Plants"},{"key":"2020101711052321700_CIT0026","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1007\/s10886-016-0736-5","article-title":"Higher activities of defense-associated enzymes may contribute to greater resistance of manchurian ash to emerald ash borer than a closely related and susceptible congener","volume":"42","author":"Rigsby","year":"2016","journal-title":"J. Chem. Ecol"},{"key":"2020101711052321700_CIT0027","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1111\/afe.12292","article-title":"Girdling increases survival and growth of emerald ash borer larvae on Manchurian ash","volume":"21","author":"Rigsby","year":"2018","journal-title":"Agr. For. Entomol"},{"key":"2020101711052321700_CIT0028","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1111\/afe.12324","article-title":"Conifer responses to a stylet-feeding invasive herbivore and induction with methyl jasmonate: impact on the expression of induced defences and a native folivore","volume":"21","author":"Rigsby","year":"2019","journal-title":"Agr. For. Entomol"},{"key":"2020101711052321700_CIT0038","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1007\/s00442-018-4063-0","article-title":"Two invasive herbivores on a shared host: patterns and consequences of phytohormone induction","volume":"186","author":"Schaeffer","year":"2018","journal-title":"Oecologia"},{"key":"2020101711052321700_CIT0030","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.4161\/psb.21663","article-title":"Mechanisms of plant defense against insect herbivores","volume":"7","author":"War","year":"2012","journal-title":"Plant Signal. Behav"},{"key":"2020101711052321700_CIT0031","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1093\/aob\/mct067","article-title":"Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany","volume":"111","author":"Wasternack","year":"2013","journal-title":"Ann. Bot"},{"key":"2020101711052321700_CIT0039","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3390\/insects7030045","article-title":"Impact of an invasive insect and plant defense on a native forest defoliator","volume":"7","author":"Wilson","year":"2016","journal-title":"Insects"}],"container-title":["Environmental Entomology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/ee\/article-pdf\/49\/5\/1226\/33925196\/nvaa104.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ee\/article-pdf\/49\/5\/1226\/33925196\/nvaa104.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,11]],"date-time":"2024-08-11T19:52:00Z","timestamp":1723405920000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ee\/article\/49\/5\/1226\/5906425"}},"subtitle":[],"editor":[{"given":"Jared","family":"Ali","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2020,9,16]]},"references-count":38,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,9,16]]},"published-print":{"date-parts":[[2020,10,17]]}},"URL":"https:\/\/doi.org\/10.1093\/ee\/nvaa104","relation":{},"ISSN":["0046-225X","1938-2936"],"issn-type":[{"type":"print","value":"0046-225X"},{"type":"electronic","value":"1938-2936"}],"subject":[],"published-other":{"date-parts":[[2020,10]]},"published":{"date-parts":[[2020,9,16]]}}}