{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,26]],"date-time":"2026-10-26T19:52:34Z","timestamp":1793044354238,"version":"4.5.0"},"reference-count":96,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,10,18]],"date-time":"2021-10-18T00:00:00Z","timestamp":1634515200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,10,18]],"date-time":"2021-10-18T00:00:00Z","timestamp":1634515200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100007210","name":"RWTH Aachen University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100007210","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Hormones orchestrate the physiology of organisms. Measuring the activity of defense hormone-responsive genes can help understanding immune signaling and facilitate breeding for plant health. However, different from model species like Arabidopsis, genes that respond to defense hormones salicylic acid (SA) and jasmonic acid (JA) have not been disclosed in the soybean crop. We performed global transcriptome analyses to fill this knowledge gap. Upon exogenous application, endogenous levels of SA and JA increased in leaves. SA predominantly activated genes linked to systemic acquired resistance and defense signaling whereas JA mainly activated wound response-associated genes. In general, SA-responsive genes were activated earlier than those responding to JA. Consistent with the paradigm of biotrophic pathogens predominantly activating SA responses, free SA and here identified most robust SA marker genes\n                    <jats:italic>GmNIMIN1<\/jats:italic>\n                    ,\n                    <jats:italic>GmNIMIN1.2<\/jats:italic>\n                    and\n                    <jats:italic>GmWRK40<\/jats:italic>\n                    were induced upon inoculation with\n                    <jats:italic>Phakopsora pachyrhizi,<\/jats:italic>\n                    whereas JA marker genes did not respond to infection with the biotrophic fungus.\n                    <jats:italic>Spodoptera exigua<\/jats:italic>\n                    larvae caused a strong accumulation of JA-Ile and JA-specific mRNA transcripts of\n                    <jats:italic>GmBPI1<\/jats:italic>\n                    ,\n                    <jats:italic>GmKTI1<\/jats:italic>\n                    and\n                    <jats:italic>GmAAT<\/jats:italic>\n                    whereas neither free SA nor SA-marker gene transcripts accumulated upon insect feeding. Our study provides molecular tools for monitoring the dynamic accumulation of SA and JA, e.g. in a given stress condition.\n                  <\/jats:p>","DOI":"10.1038\/s41598-021-00209-6","type":"journal-article","created":{"date-parts":[[2021,10,18]],"date-time":"2021-10-18T15:27:17Z","timestamp":1634570837000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":44,"title":["Disclosure of salicylic acid and jasmonic acid-responsive genes provides a molecular tool for deciphering stress responses in soybean"],"prefix":"10.1038","volume":"11","author":[{"given":"Sebastian F.","family":"Beyer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paloma S\u00e1nchez","family":"Bel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victor","family":"Flors","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Holger","family":"Schultheiss","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Uwe","family":"Conrath","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caspar J. G.","family":"Langenbach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,10,18]]},"reference":[{"key":"209_CR1","doi-asserted-by":"publisher","first-page":"1624","DOI":"10.1104\/pp.19.01464","volume":"182","author":"J Lamers","year":"2020","unstructured":"Lamers, J., van der Meer, T. & Testerink, C. How plants sense and respond to stressful environments. Plant Physiol. 182, 1624\u20131635 (2020).","journal-title":"Plant Physiol."},{"key":"209_CR2","doi-asserted-by":"publisher","first-page":"978","DOI":"10.1016\/j.cell.2020.04.028","volume":"181","author":"J-M Zhou","year":"2020","unstructured":"Zhou, J.-M. & Zhang, Y. Plant immunity: Danger perception and signaling. Cell 181, 978\u2013989 (2020).","journal-title":"Cell"},{"key":"209_CR3","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1146\/annurev-cellbio-092910-154055","volume":"28","author":"CMJ Pieterse","year":"2012","unstructured":"Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S. C. M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489\u2013521 (2012).","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"209_CR4","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1146\/annurev-phyto-082712-102340","volume":"52","author":"CMJ Pieterse","year":"2014","unstructured":"Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347\u2013375 (2014).","journal-title":"Annu. Rev. Phytopathol."},{"key":"209_CR5","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1104\/pp.107.112029","volume":"146","author":"A Koornneef","year":"2008","unstructured":"Koornneef, A. & Pieterse, C. M. J. Cross talk in defense signaling. Plant Physiol. 146, 839\u2013844 (2008).","journal-title":"Plant Physiol."},{"key":"209_CR6","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1146\/annurev.phyto.41.052002.095505","volume":"43","author":"RM Bostock","year":"2005","unstructured":"Bostock, R. M. Signal crosstalk and induced resistance: Straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43, 545\u2013580 (2005).","journal-title":"Annu. Rev. Phytopathol."},{"key":"209_CR7","doi-asserted-by":"publisher","first-page":"18842","DOI":"10.1073\/pnas.0708139104","volume":"104","author":"SH Spoel","year":"2007","unstructured":"Spoel, S. H., Johnson, J. S. & Dong, X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. 104, 18842\u201318847 (2007).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR8","doi-asserted-by":"publisher","first-page":"1358","DOI":"10.1104\/pp.108.121392","volume":"147","author":"A Koornneef","year":"2008","unstructured":"Koornneef, A. et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358\u20131368 (2008).","journal-title":"Plant Physiol."},{"key":"209_CR9","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1016\/j.molp.2018.05.007","volume":"11","author":"H Cui","year":"2018","unstructured":"Cui, H. et al. Antagonism of transcription factor MYC2 by EDS1\/PAD4 complexes bolsters salicylic acid defense in Arabidopsis effector-triggered immunity. Mol. Plant 11, 1053\u20131066 (2018).","journal-title":"Mol. Plant"},{"key":"209_CR10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpls.2015.00170","volume":"6","author":"L Caarls","year":"2015","unstructured":"Caarls, L., Pieterse, C. M. J. & Van Wees, S. C. M. How salicylic acid takes transcriptional control over jasmonic acid signaling. Front. Plant Sci. 6, 1\u201311 (2015).","journal-title":"Front. Plant Sci."},{"key":"209_CR11","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1046\/j.1365-313x.2001.01050.x","volume":"26","author":"AP Kloek","year":"2001","unstructured":"Kloek, A. P. et al. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J. 26, 509\u2013522 (2001).","journal-title":"Plant J."},{"key":"209_CR12","doi-asserted-by":"publisher","first-page":"1125","DOI":"10.1046\/j.1365-294X.2003.01815.x","volume":"12","author":"MB Traw","year":"2003","unstructured":"Traw, M. B., Kim, J., Enright, S., Cipollini, D. F. & Bergelson, J. Negative cross-talk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12, 1125\u20131135 (2003).","journal-title":"Mol. Ecol."},{"key":"209_CR13","doi-asserted-by":"publisher","first-page":"1025","DOI":"10.1094\/MPMI.2002.15.10.1025","volume":"15","author":"C Ellis","year":"2002","unstructured":"Ellis, C., Karafyllidis, I. & Turner, J. G. Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant-Microbe Interact. 15, 1025\u20131030 (2002).","journal-title":"Mol. Plant-Microbe Interact."},{"key":"209_CR14","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.tplants.2009.03.006","volume":"14","author":"J Ton","year":"2009","unstructured":"Ton, J., Flors, V. & Mauch-Mani, B. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14, 310\u2013317 (2009).","journal-title":"Trends Plant Sci."},{"key":"209_CR15","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1038\/nchembio.1520","volume":"10","author":"E Luna","year":"2014","unstructured":"Luna, E. et al. Plant perception of \u03b2-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat. Chem. Biol. 10, 450\u2013456 (2014).","journal-title":"Nat. Chem. Biol."},{"key":"209_CR16","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1016\/j.tplants.2009.04.005","volume":"14","author":"K Kazan","year":"2009","unstructured":"Kazan, K. & Manners, J. M. Linking development to defense: Auxin in plant-pathogen interactions. Trends Plant Sci. 14, 373\u2013382 (2009).","journal-title":"Trends Plant Sci."},{"key":"209_CR17","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1046\/j.1365-313X.2003.01675.x","volume":"33","author":"H Nakashita","year":"2003","unstructured":"Nakashita, H. et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33, 887\u2013898 (2003).","journal-title":"Plant J."},{"key":"209_CR18","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1016\/j.tplants.2006.10.003","volume":"11","author":"DR Walters","year":"2006","unstructured":"Walters, D. R. & McRoberts, N. Plants and biotrophs: A pivotal role for cytokinins?. Trends Plant Sci. 11, 581\u2013586 (2006).","journal-title":"Trends Plant Sci."},{"key":"209_CR19","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1016\/j.cub.2008.03.060","volume":"18","author":"L Navarro","year":"2008","unstructured":"Navarro, L. et al. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 18, 650\u2013655 (2008).","journal-title":"Curr. Biol."},{"key":"209_CR20","doi-asserted-by":"publisher","first-page":"8849","DOI":"10.1073\/pnas.97.16.8849","volume":"97","author":"DF Klessig","year":"2000","unstructured":"Klessig, D. F. et al. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA. 97, 8849\u20138855 (2000).","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"209_CR21","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.pbi.2019.02.006","volume":"50","author":"M Hartmann","year":"2019","unstructured":"Hartmann, M. & Zeier, J. N-hydroxypipecolic acid and salicylic acid: A metabolic duo for systemic acquired resistance. Curr. Opin. Plant Biol. 50, 44\u201357 (2019).","journal-title":"Curr. Opin. Plant Biol."},{"key":"209_CR22","first-page":"645","volume":"4","author":"S Uknes","year":"1992","unstructured":"Uknes, S. et al. Acquired resistance in arabidopsis. Plant Cell 4, 645\u2013656 (1992).","journal-title":"Plant Cell"},{"key":"209_CR23","doi-asserted-by":"publisher","first-page":"5400","DOI":"10.1093\/emboj\/20.19.5400","volume":"20","author":"BJ Feys","year":"2001","unstructured":"Feys, B. J., Moisan, L. J., Newman, M. A. & Parker, J. E. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400\u20135411 (2001).","journal-title":"EMBO J."},{"key":"209_CR24","doi-asserted-by":"publisher","first-page":"1454","DOI":"10.1016\/j.cell.2018.03.044","volume":"173","author":"Y Ding","year":"2018","unstructured":"Ding, Y. et al. Opposite roles of salicylic acid receptors NPR1 and NPR3\/NPR4 in transcriptional regulation of plant immunity. Cell 173, 1454-1467.e15 (2018).","journal-title":"Cell"},{"key":"209_CR25","doi-asserted-by":"publisher","first-page":"1571","DOI":"10.1105\/tpc.10.9.1571","volume":"10","author":"CM Pieterse","year":"1998","unstructured":"Pieterse, C. M. et al. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 1571\u20131580 (1998).","journal-title":"Plant Cell"},{"key":"209_CR26","doi-asserted-by":"publisher","first-page":"2103","DOI":"10.1105\/tpc.10.12.2103","volume":"10","author":"IAMA Penninckx","year":"1998","unstructured":"Penninckx, I. A. M. A., Thomma, B. P. H. J., Buchala, A., M\u00e9traux, J. P. & Broekaert, W. F. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 2103\u20132113 (1998).","journal-title":"Plant Cell"},{"key":"209_CR27","doi-asserted-by":"publisher","first-page":"866","DOI":"10.1104\/pp.106.090035","volume":"143","author":"SI Zarate","year":"2007","unstructured":"Zarate, S. I., Kempema, L. A. & Walling, L. L. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143, 866\u2013875 (2007).","journal-title":"Plant Physiol."},{"key":"209_CR28","doi-asserted-by":"publisher","first-page":"1560","DOI":"10.1016\/j.phytochem.2009.09.004","volume":"70","author":"J Memelink","year":"2009","unstructured":"Memelink, J. Regulation of gene expression by jasmonate hormones. Phytochemistry 70, 1560\u20131570 (2009).","journal-title":"Phytochemistry"},{"key":"209_CR29","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1104\/pp.115.1.291","volume":"115","author":"R Tenhaken","year":"1997","unstructured":"Tenhaken, R. & R\u00fcbel, C. Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol. 115, 291\u2013298 (1997).","journal-title":"Plant Physiol."},{"key":"209_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-018-33477-w","volume":"8","author":"KM Chapman","year":"2018","unstructured":"Chapman, K. M., Marchi-Werle, L., Hunt, T. E., Heng-Moss, T. M. & Louis, J. Abscisic and jasmonic acids contribute to soybean tolerance to the soybean aphid (Aphis glycines Matsumura). Sci. Rep. 8, 1\u201312 (2018).","journal-title":"Sci. Rep."},{"key":"209_CR31","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s12571-010-0108-x","volume":"3","author":"GL Hartman","year":"2011","unstructured":"Hartman, G. L., West, E. D. & Herman, T. K. Crops that feed the World 2. Soybean\u2014worldwide production, use, and constraints caused by pathogens and pests. Food Secur. 3, 5\u201317 (2011).","journal-title":"Food Secur."},{"key":"209_CR32","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1126\/science.327.5967.804","volume":"327","author":"E Pennisi","year":"2010","unstructured":"Pennisi, E. Armed and dangerous. Science 327, 804\u2013805 (2010).","journal-title":"Science"},{"key":"209_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpls.2016.00797","volume":"7","author":"C Langenbach","year":"2016","unstructured":"Langenbach, C., Campe, R., Beyer, S. F., Mueller, A. N. & Conrath, U. Fighting Asian soybean rust. Front. Plant Sci. 7, 1\u201324 (2016).","journal-title":"Front. Plant Sci."},{"key":"209_CR34","first-page":"39","volume":"13","author":"X-L Zheng","year":"2011","unstructured":"Zheng, X.-L., Cong, X.-P., Wang, X.-P. & Lei, C.-L. A review of geographic distribution, overwintering and migration in Spodoptera exigua Hubner (Lepidoptera: Noctuidae). J. Entomol. Res. Soc. 13, 39\u201348 (2011).","journal-title":"J. Entomol. Res. Soc."},{"key":"209_CR35","doi-asserted-by":"publisher","first-page":"2117","DOI":"10.1105\/tpc.104.023549","volume":"16","author":"PE Staswick","year":"2004","unstructured":"Staswick, P. E. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in arabidopsis. Plant Cell Online 16, 2117\u20132127 (2004).","journal-title":"Plant Cell Online"},{"key":"209_CR36","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1038\/nchembio.161","volume":"5","author":"S Fonseca","year":"2009","unstructured":"Fonseca, S. et al. (+)-7-iso-jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344\u2013350 (2009).","journal-title":"Nat. Chem. Biol."},{"key":"209_CR37","first-page":"241","volume":"5","author":"HS Mason","year":"1993","unstructured":"Mason, H. S., DeWald, D. B. & Mullet, J. E. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5, 241\u2013251 (1993).","journal-title":"Plant Cell"},{"key":"209_CR38","doi-asserted-by":"publisher","first-page":"8113","DOI":"10.1073\/pnas.95.14.8113","volume":"95","author":"IT Baldwin","year":"1998","unstructured":"Baldwin, I. T. Jasmonate-induced responses are costly but benefit plants under attack in native populations. PNAS 95, 8113\u20138118 (1998).","journal-title":"PNAS"},{"key":"209_CR39","doi-asserted-by":"publisher","first-page":"1607","DOI":"10.1073\/pnas.0305096101","volume":"101","author":"JA Zavala","year":"2004","unstructured":"Zavala, J. A., Patankar, A. G., Gase, K. & Baldwin, I. T. Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc. Natl. Acad. Sci. USA. 101, 1607\u20131612 (2004).","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"209_CR40","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.cub.2011.12.015","volume":"22","author":"KM Pajerowska-Mukhtar","year":"2012","unstructured":"Pajerowska-Mukhtar, K. M. et al. The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr. Biol. 22, 103\u2013112 (2012).","journal-title":"Curr. Biol."},{"key":"209_CR41","doi-asserted-by":"publisher","first-page":"5473","DOI":"10.1073\/pnas.94.10.5473","volume":"94","author":"M Mcconn","year":"1997","unstructured":"Mcconn, M., Creelman, R. A., Bell, E., Mullet, J. E. & Browse, J. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA. 94, 5473\u20135477 (1997).","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"209_CR42","doi-asserted-by":"publisher","first-page":"971","DOI":"10.1105\/tpc.104.029108","volume":"17","author":"C Li","year":"2005","unstructured":"Li, C. et al. Role of \u03b2-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17, 971\u2013986 (2005).","journal-title":"Plant Cell"},{"key":"209_CR43","doi-asserted-by":"publisher","first-page":"3117","DOI":"10.1105\/tpc.113.115139","volume":"25","author":"F Schweizer","year":"2013","unstructured":"Schweizer, F. et al. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, andMYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25, 3117\u20133132 (2013).","journal-title":"Plant Cell"},{"key":"209_CR44","first-page":"919","volume":"21","author":"VR Van Oosten","year":"2008","unstructured":"Van Oosten, V. R. et al. Differential effectiveness of microbially induced resistance against herbivorous insects in arabidopsis. Plant Cell 21, 919\u2013930 (2008).","journal-title":"Plant Cell"},{"key":"209_CR45","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/513824","author":"S Farahani","year":"2012","unstructured":"Farahani, S., Talebi, A. A. & Fathipour, Y. Life table of Spodoptera exigua (Lepidoptera: Noctuidae) on five soybean cultivars. Psyche https:\/\/doi.org\/10.1155\/2012\/513824 (2012).","journal-title":"Psyche"},{"key":"209_CR46","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1094\/MPMI-20-8-0887","volume":"20","author":"M van de Mortel","year":"2007","unstructured":"van de Mortel, M. et al. Distinct biphasic mRNA changes in response to Asian soybean rust infection. Mol. Plant Microbe Interact. 20, 887\u2013899 (2007).","journal-title":"Mol. Plant Microbe Interact."},{"key":"209_CR47","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1104\/pp.111.181149","volume":"157","author":"KT Schneider","year":"2011","unstructured":"Schneider, K. T. et al. Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation. Plant Physiol. 157, 355\u2013371 (2011).","journal-title":"Plant Physiol."},{"key":"209_CR48","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1094\/MPMI-08-10-0187","volume":"24","author":"AK Pandey","year":"2011","unstructured":"Pandey, A. K. et al. Functional analysis of the asian soybean rust resistance pathway mediated by Rpp2. Mol. Plant-Microbe Interact. 24, 194\u2013206 (2011).","journal-title":"Mol. Plant-Microbe Interact."},{"key":"209_CR49","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1111\/tpj.14426","volume":"99","author":"SF Beyer","year":"2019","unstructured":"Beyer, S. F. et al. The Arabidopsis non-host defence-associated coumarin scopoletin protects soybean from Asian soybean rust. Plant J. 99, 397\u2013413 (2019).","journal-title":"Plant J."},{"key":"209_CR50","doi-asserted-by":"publisher","first-page":"5245","DOI":"10.1158\/0008-5472.CAN-04-0496","volume":"64","author":"CL Andersen","year":"2004","unstructured":"Andersen, C. L., Jensen, J. L. & \u00d8rntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245\u20135250 (2004).","journal-title":"Cancer Res."},{"key":"209_CR51","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1038\/nature08670","volume":"463","author":"J Schmutz","year":"2010","unstructured":"Schmutz, J. et al. Genome sequence of the palaeopolyploid soybean. Nature 463, 178\u2013183 (2010).","journal-title":"Nature"},{"key":"209_CR52","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1111\/nph.14078","volume":"212","author":"MB Shine","year":"2016","unstructured":"Shine, M. B. et al. Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytol. 212, 327\u2013363 (2016).","journal-title":"New Phytol."},{"key":"209_CR53","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1186\/s12870-016-0749-9","volume":"16","author":"Y Kouzai","year":"2016","unstructured":"Kouzai, Y. et al. Expression profiling of marker genes responsive to the defence-associated phytohormones salicylic acid, jasmonic acid and ethylene in Brachypodium distachyon. BMC Plant Biol. 16, 59 (2016).","journal-title":"BMC Plant Biol."},{"key":"209_CR54","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep14476","volume":"5","author":"Y Kakei","year":"2015","unstructured":"Kakei, Y. et al. Transcriptome analysis of hormone-induced gene expression in Brachypodium distachyon. Sci. Rep. 5, 1\u201314 (2015).","journal-title":"Sci. Rep."},{"key":"209_CR55","doi-asserted-by":"publisher","first-page":"423","DOI":"10.3389\/fpls.2019.00423","volume":"10","author":"I Maruri-L\u00f3pez","year":"2019","unstructured":"Maruri-L\u00f3pez, I., Aviles-Baltazar, N. Y., Buchala, A. & Serrano, M. Intra and extracellular journey of the phytohormone salicylic acid. Front. Plant Sci. 10, 423 (2019).","journal-title":"Front. Plant Sci."},{"key":"209_CR56","doi-asserted-by":"publisher","first-page":"2480","DOI":"10.1073\/pnas.89.6.2480","volume":"89","author":"AJ Enyedi","year":"1992","unstructured":"Enyedi, A. J., Yalpani, N., Silverman, P. & Raskin, I. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. Sci. 89, 2480\u20132484 (1992).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR57","doi-asserted-by":"publisher","first-page":"3321","DOI":"10.1093\/jxb\/err031","volume":"62","author":"M Rivas-San Vicente","year":"2011","unstructured":"Rivas-San Vicente, M. & Plasencia, J. Salicylic acid beyond defence: Its role in plant growth and development. J. Exp. Bot. 62, 3321\u20133338 (2011).","journal-title":"J. Exp. Bot."},{"key":"209_CR58","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1104\/pp.108.2.633","volume":"108","author":"P Silverman","year":"1995","unstructured":"Silverman, P. et al. Salicylic acid in rice (biosynthesis, conjugation, and possible role). Plant Physiol. 108, 633\u2013639 (1995).","journal-title":"Plant Physiol."},{"key":"209_CR59","doi-asserted-by":"publisher","first-page":"46629","DOI":"10.1038\/srep46629","volume":"7","author":"AM George Thompson","year":"2017","unstructured":"George Thompson, A. M., Iancu, C. V., Neet, K. E., Dean, J. V. & Choe, J. Differences in salicylic acid glucose conjugations by UGT74F1 and UGT74F2 from Arabidopsis thaliana. Sci. Rep. 7, 46629 (2017).","journal-title":"Sci. Rep."},{"key":"209_CR60","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1094\/PHYTO.1998.88.7.692","volume":"88","author":"H Lee","year":"1998","unstructured":"Lee, H. & Raskin, I. Glucosylation of salicylic acid in Nicotiana tabacum Cv. Xanthi-nc. Phytopathology 88, 692\u2013697 (1998).","journal-title":"Phytopathology"},{"key":"209_CR61","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1111\/j.0031-9317.2004.0263.x","volume":"120","author":"JV Dean","year":"2004","unstructured":"Dean, J. V. & Mills, J. D. Uptake of salicylic acid 2-O-\u03b2-d-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol. Plant. 120, 603\u2013612 (2004).","journal-title":"Physiol. Plant."},{"key":"209_CR62","first-page":"1845","volume":"6","author":"SA Bowling","year":"1994","unstructured":"Bowling, S. A. et al. A mutation in arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6, 1845\u20131857 (1994).","journal-title":"Plant Cell"},{"key":"209_CR63","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1094\/MPMI.2001.14.10.1131","volume":"14","author":"X Li","year":"2001","unstructured":"Li, X., Clarke, J. D., Zhang, Y. & Dong, X. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant Microbe Interact. 14, 1131\u20131139 (2001).","journal-title":"Mol. Plant Microbe Interact."},{"key":"209_CR64","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1038\/nature01588","volume":"423","author":"D Tian","year":"2003","unstructured":"Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M. & Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74\u201377 (2003).","journal-title":"Nature"},{"key":"209_CR65","doi-asserted-by":"publisher","first-page":"1999","DOI":"10.1093\/pcp\/pct137","volume":"54","author":"K Oka","year":"2013","unstructured":"Oka, K., Kobayashi, M., Mitsuhara, I. & Seo, S. Jasmonic acid negatively regulates resistance to Tobacco mosaic virus in tobacco. Plant Cell Physiol. 54, 1999\u20132010 (2013).","journal-title":"Plant Cell Physiol."},{"key":"209_CR66","doi-asserted-by":"publisher","first-page":"6388","DOI":"10.1073\/pnas.1701101114","volume":"114","author":"L Caarls","year":"2017","unstructured":"Caarls, L. et al. Arabidopsis jasmonate-induced oxygenases down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc. Natl. Acad. Sci. 114, 6388\u20136393 (2017).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR67","doi-asserted-by":"publisher","first-page":"1380","DOI":"10.1073\/pnas.0711203105","volume":"105","author":"L Pauwels","year":"2008","unstructured":"Pauwels, L. et al. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc. Natl. Acad. Sci. 105, 1380\u20131385 (2008).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR68","doi-asserted-by":"publisher","first-page":"1002","DOI":"10.1126\/science.250.4983.1002","volume":"250","author":"J Malamy","year":"1990","unstructured":"Malamy, J., Carr, J. P., Klessig, D. F. & Raskin, I. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002\u20131004 (1990).","journal-title":"Science"},{"key":"209_CR69","doi-asserted-by":"publisher","first-page":"1004","DOI":"10.1126\/science.250.4983.1004","volume":"250","author":"JP Metraux","year":"1990","unstructured":"Metraux, J. P. et al. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004\u20131006 (1990).","journal-title":"Science"},{"key":"209_CR70","doi-asserted-by":"publisher","first-page":"7713","DOI":"10.1073\/pnas.87.19.7713","volume":"87","author":"EE Farmer","year":"1990","unstructured":"Farmer, E. E. & Ryan, C. A. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. 87, 7713\u20137716 (1990).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR71","doi-asserted-by":"publisher","first-page":"1342","DOI":"10.1104\/pp.97.4.1342","volume":"97","author":"JB Rasmussen","year":"1991","unstructured":"Rasmussen, J. B., Hammerschmidt, R. & Zook, M. N. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342\u20131347 (1991).","journal-title":"Plant Physiol."},{"key":"209_CR72","doi-asserted-by":"publisher","first-page":"129","DOI":"10.2307\/3869566","volume":"4","author":"EE Farmer","year":"1992","unstructured":"Farmer, E. E. & Ryan, C. A. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4, 129\u2013134 (1992).","journal-title":"Plant Cell"},{"key":"209_CR73","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.pbi.2019.02.004","volume":"50","author":"Y Zhang","year":"2019","unstructured":"Zhang, Y. & Li, X. Salicylic acid: Biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50, 29\u201336 (2019).","journal-title":"Curr. Opin. Plant Biol."},{"key":"209_CR74","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1074\/jbc.M109287200","volume":"277","author":"E-K Lim","year":"2002","unstructured":"Lim, E.-K. et al. The activity of arabidopsisglycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates. J. Biol. Chem. 277, 586\u2013592 (2002).","journal-title":"J. Biol. Chem."},{"key":"209_CR75","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1126\/science.aaw1720","volume":"365","author":"D Rekhter","year":"2019","unstructured":"Rekhter, D. et al. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 365, 498\u2013502 (2019).","journal-title":"Science"},{"key":"209_CR76","doi-asserted-by":"publisher","first-page":"16855","DOI":"10.1074\/jbc.RA119.009949","volume":"294","author":"CK Holland","year":"2019","unstructured":"Holland, C. K. et al. Brassicaceae-specific Gretchen Hagen 3 acyl acid amido synthetases conjugate amino acids to chorismate, a precursor of aromatic amino acids and salicylic acid. J. Biol. Chem. 294, 16855\u201316864 (2019).","journal-title":"J. Biol. Chem."},{"key":"209_CR77","doi-asserted-by":"publisher","first-page":"1279","DOI":"10.1105\/tpc.104.027441","volume":"17","author":"RR Weigel","year":"2005","unstructured":"Weigel, R. R., Pfitzner, U. M. & Gatz, C. Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17, 1279\u20131291 (2005).","journal-title":"Plant Cell"},{"key":"209_CR78","doi-asserted-by":"publisher","first-page":"e1211222","DOI":"10.1080\/15592324.2016.1211222","volume":"11","author":"R Mohan","year":"2016","unstructured":"Mohan, R., Tai, T., Chen, A., Arnoff, T. & Fu, Z.-Q. Overexpression of Arabidopsis NIMIN1 results in salicylate intolerance. Plant Signal. Behav. 11, e1211222 (2016).","journal-title":"Plant Signal. Behav."},{"key":"209_CR79","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1105\/tpc.16.00681","volume":"29","author":"RP Birkenbihl","year":"2017","unstructured":"Birkenbihl, R. P., Kracher, B., Roccaro, M. & Somssich, I. E. Induced genome-wide binding of three arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell 29, 20\u201338 (2017).","journal-title":"Plant Cell"},{"key":"209_CR80","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1111\/tpj.14124","volume":"97","author":"JK Abeysinghe","year":"2019","unstructured":"Abeysinghe, J. K., Lam, K.-M. & Ng, D. W. K. Differential regulation and interaction of homoeologous WRKY18 and WRKY40 in Arabidopsis allotetraploids and biotic stress responses. Plant J. 97, 352\u2013367 (2019).","journal-title":"Plant J."},{"key":"209_CR81","first-page":"1573","volume":"9","author":"SA Bowling","year":"1997","unstructured":"Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F. & Dong, X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9, 1573\u20131584 (1997).","journal-title":"Plant Cell"},{"key":"209_CR82","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1104\/pp.18.00903","volume":"178","author":"HY Xu","year":"2018","unstructured":"Xu, H. Y. et al. The MAPK kinase kinase GMMEKK1 regulates cell death and defense responses. Plant Physiol. 178, 907\u2013922 (2018).","journal-title":"Plant Physiol."},{"key":"209_CR83","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1186\/s12864-015-2318-2","volume":"16","author":"A Lanubile","year":"2015","unstructured":"Lanubile, A., Muppirala, U. K., Severin, A. J., Marocco, A. & Munkvold, G. P. Transcriptome profiling of soybean (Glycine max) roots challenged with pathogenic and non-pathogenic isolates of Fusarium oxysporum. BMC Genom. 16, 1089 (2015).","journal-title":"BMC Genom."},{"key":"209_CR84","doi-asserted-by":"publisher","first-page":"E6703","DOI":"10.1073\/pnas.1704536114","volume":"114","author":"C Hettenhausen","year":"2017","unstructured":"Hettenhausen, C. et al. Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants. Proc. Natl. Acad. Sci. 114, E6703\u2013E6709 (2017).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"209_CR85","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12864-017-4256-7","volume":"18","author":"W Zeng","year":"2017","unstructured":"Zeng, W. et al. Comparative transcriptome analysis of soybean response to bean pyralid larvae. BMC Genom. 18, 1\u201328 (2017).","journal-title":"BMC Genom."},{"key":"209_CR86","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1146\/annurev-ento-010814-020816","volume":"60","author":"K Zhu-Salzman","year":"2015","unstructured":"Zhu-Salzman, K. & Zeng, R. Insect response to plant defensive protease inhibitors. Annu. Rev. Entomol. 60, 233\u2013252 (2015).","journal-title":"Annu. Rev. Entomol."},{"key":"209_CR87","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1186\/s12864-015-1637-7","volume":"16","author":"A Whaley","year":"2015","unstructured":"Whaley, A. et al. RNA-seq analysis reveals genetic response and tolerance mechanisms to ozone exposure in soybean. BMC Genom. 16, 426 (2015).","journal-title":"BMC Genom."},{"key":"209_CR88","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1046\/j.1365-313X.1997.11020203.x","volume":"11","author":"BL Orvar","year":"1997","unstructured":"Orvar, B. L., McPherson, J. & Ellis, B. E. Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J. 11, 203\u2013212 (1997).","journal-title":"Plant J."},{"key":"209_CR89","doi-asserted-by":"publisher","first-page":"1421","DOI":"10.1094\/MPMI-21-11-1421","volume":"21","author":"M Loehrer","year":"2008","unstructured":"Loehrer, M., Langenbach, C., Goellner, K., Conrath, U. & Schaffrath, U. Characterization of nonhost resistance of Arabidopsis to the asian soybean rust. Mol. Plant-Microbe Interact. 21, 1421\u20131430 (2008).","journal-title":"Mol. Plant-Microbe Interact."},{"key":"209_CR90","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pmpp.2014.04.005","volume":"87","author":"R Campe","year":"2014","unstructured":"Campe, R., Loehrer, M., Conrath, U. & Goellner, K. Phakopsora pachyrhizi induces defense marker genes to necrotrophs in Arabidopsis thaliana. Physiol. Mol. Plant Pathol. 87, 1\u20138 (2014).","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"209_CR91","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1007\/s10142-015-0445-0","volume":"15","author":"MS Alves","year":"2015","unstructured":"Alves, M. S. et al. Differential expression of four soybean bZIP genes during Phakopsora pachyrhizi infection. Funct. Integr. Genomics 15, 685\u2013696 (2015).","journal-title":"Funct. Integr. Genomics"},{"key":"209_CR92","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1007\/s11103-008-9435-0","volume":"69","author":"R Bari","year":"2009","unstructured":"Bari, R. & Jones, J. D. G. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69, 473\u2013488 (2009).","journal-title":"Plant Mol. Biol."},{"key":"209_CR93","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1111\/pce.13105","volume":"41","author":"P S\u00e1nchez-Bel","year":"2018","unstructured":"S\u00e1nchez-Bel, P. et al. Mycorrhizal tomato plants fine tunes the growth-defence balance upon N depleted root environments. Plant. Cell Environ. 41, 406\u2013420 (2018).","journal-title":"Plant. Cell Environ."},{"key":"209_CR94","doi-asserted-by":"publisher","first-page":"1736","DOI":"10.1105\/tpc.108.061143","volume":"20","author":"MK Udvardi","year":"2008","unstructured":"Udvardi, M. K., Czechowski, T. & Scheible, W.-R. Eleven golden rules of quantitative RT-PCR. Plant Cell 20, 1736\u20131737 (2008).","journal-title":"Plant Cell"},{"key":"209_CR95","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/nph.13582","volume":"209","author":"R Campe","year":"2016","unstructured":"Campe, R. et al. ABC transporter PEN3\/PDR8\/ABCG36 interacts with calmodulin that, like PEN3, is required for Arabidopsis nonhost resistance. New Phytol. 209, 1\u2013294 (2016).","journal-title":"New Phytol."},{"key":"209_CR96","doi-asserted-by":"publisher","first-page":"949","DOI":"10.1046\/j.1365-313X.2003.01676.x","volume":"33","author":"O Voinnet","year":"2003","unstructured":"Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949\u2013956 (2003).","journal-title":"Plant J."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-00209-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-00209-6","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-00209-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,7]],"date-time":"2023-02-07T06:17:10Z","timestamp":1675750630000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-00209-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,18]]},"references-count":96,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["209"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-00209-6","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,18]]},"assertion":[{"value":"1 June 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 October 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 October 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"20600"}}