{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,8]],"date-time":"2026-06-08T14:20:15Z","timestamp":1780928415856,"version":"3.54.1"},"reference-count":79,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,6,8]],"date-time":"2026-06-08T00:00:00Z","timestamp":1780876800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,6,8]],"date-time":"2026-06-08T00:00:00Z","timestamp":1780876800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100008131","name":"Rheinische Friedrich-Wilhelms-Universit\u00e4t Bonn","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100008131","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                    Enolase (2-phospho-D-glycerate hydrolase, EC 4.2.1.11) is a conserved glycolytic enzyme that catalyzes the reversible dehydration of 2-phosphoglycerate to phosphoenolpyruvate. In animal- and entomopathogenic nematodes, enolase has been shown to interact with host organisms and activate immune responses. In the plant-parasitic cyst nematode\n                    <jats:italic>Heterodera schachtii<\/jats:italic>\n                    , an established model species, enolase is hypothesized to be similarly exposed to host plant tissues during infection, based on its identification in the secretomes of related plant-parasitic nematodes. Unlike animals, plants lack an adaptive immune system and instead rely on innate immune responses to detect pathogen-derived molecules. Therefore, we investigated whether\n                    <jats:italic>H. schachtii<\/jats:italic>\n                    enolase can activate plant immune responses and influence growth and development in its host,\n                    <jats:italic>Arabidopsis thaliana<\/jats:italic>\n                    . Recombinant\n                    <jats:italic>H. schachtii<\/jats:italic>\n                    enolase was heterologously expressed in\n                    <jats:italic>Escherichia coli<\/jats:italic>\n                    and confirmed to be enzymatically active. Treatment of\n                    <jats:italic>A. thaliana<\/jats:italic>\n                    seedlings with purified enolase did not induce reactive oxygen species production, a hallmark of early plant immune activation. A concentration of 85\n                    <jats:inline-formula>\n                      <jats:tex-math>$$\\upmu$$<\/jats:tex-math>\n                    <\/jats:inline-formula>\n                    g\/ml had no effect on plant growth; only at the highest applied concentrations (425\u2013850\n                    <jats:inline-formula>\n                      <jats:tex-math>$$\\upmu$$<\/jats:tex-math>\n                    <\/jats:inline-formula>\n                    g\/ml) was shoot growth reduced, while root growth remained unaffected. Consistently, quantitative PCR analysis of canonical defense marker genes (\n                    <jats:italic>FRK1<\/jats:italic>\n                    ,\n                    <jats:italic>NHL10<\/jats:italic>\n                    ,\n                    <jats:italic>PAD3<\/jats:italic>\n                    ,\n                    <jats:italic>CYP81F2<\/jats:italic>\n                    , and\n                    <jats:italic>JAZ10<\/jats:italic>\n                    ) showed no robust transcriptional activation of plant immune pathways. Together, these results indicate that\n                    <jats:italic>H. schachtii<\/jats:italic>\n                    enolase does not function as an elicitor of canonical plant immune responses.\n                  <\/jats:p>","DOI":"10.1038\/s41598-026-56477-7","type":"journal-article","created":{"date-parts":[[2026,6,8]],"date-time":"2026-06-08T13:14:05Z","timestamp":1780924445000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Heterodera schachtii enolase does not elicit canonical immune responses in Arabidopsis thaliana"],"prefix":"10.1038","volume":"16","author":[{"given":"Maximilian F.","family":"Euler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neil Pep Dave N.","family":"Sumaya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seema","family":"Aslam","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes","family":"Lerch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Badou","family":"Mendy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florian M. W.","family":"Grundler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,6,8]]},"reference":[{"key":"56477_CR1","first-page":"60","volume":"273","author":"K Lohman","year":"1934","unstructured":"Lohman, K. & Meyerhof, O. Enzymatic transformation of phosphoglyceric acid into pyruvic acid and phosphoric acid. Biochem. Z. 273, 60\u201372 (1934).","journal-title":"Biochem. Z."},{"key":"56477_CR2","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1007\/BF01482279","volume":"29","author":"OH Warburg","year":"1941","unstructured":"Warburg, O. H. & Christian, W. Isolierung und Kristallisation des G\u00e4rungsfragments Enolase. Naturwissenschaften 29, 589\u2013590. https:\/\/doi.org\/10.1007\/BF01482279 (1941).","journal-title":"Naturwissenschaften"},{"key":"56477_CR3","doi-asserted-by":"publisher","first-page":"736","DOI":"10.1016\/S0959-440X(96)80002-9","volume":"6","author":"GH Reed","year":"1996","unstructured":"Reed, G. H., Poyner, R. R., Larsen, T. M., Wedekind, J. E. & Rayment, I. Structural and mechanistic studies of enolase. Curr. Opin. Struct. Biol. 6, 736\u2013743. https:\/\/doi.org\/10.1016\/S0959-440X(96)80002-9 (1996).","journal-title":"Curr. Opin. Struct. Biol."},{"key":"56477_CR4","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/0005-2795(75)90328-1","volume":"405","author":"C Rider","year":"1975","unstructured":"Rider, C. & Taylor, C. Enolase isoenzymes. Biochim. Biophys. Acta (BBA) Protein Struct. 405, 175\u2013187. https:\/\/doi.org\/10.1016\/0005-2795(75)90328-1 (1975).","journal-title":"Biochim. Biophys. Acta (BBA) Protein Struct."},{"key":"56477_CR5","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1159\/000132960","volume":"54","author":"SP Craig","year":"1990","unstructured":"Craig, S. P., Day, I. N., Thompson, R. J. & Craig, I. W. Localisation of neurone-specific enolase (ENO2) to 12pl3. Cytogenet. Cell Genet. 54, 71\u201373. https:\/\/doi.org\/10.1159\/000132960 (1990).","journal-title":"Cytogenet. Cell Genet."},{"key":"56477_CR6","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/0888-7543(90)90467-9","volume":"6","author":"S Feo","year":"1990","unstructured":"Feo, S. et al. The gene for the muscle-specific enolase is on the short arm of human chromosome 17. Genomics 6, 192\u2013194. https:\/\/doi.org\/10.1016\/0888-7543(90)90467-9 (1990).","journal-title":"Genomics"},{"key":"56477_CR7","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1105\/tpc.3.7.719","volume":"3","author":"D Van Der Straeten","year":"1991","unstructured":"Van Der Straeten, D., Rodrigues-Pousada, R. A., Goodman, H. M. & Van Montagu, M. Plant enolase: Gene structure, expression, and evolution. Plant Cell 3, 719\u2013735. https:\/\/doi.org\/10.1105\/tpc.3.7.719 (1991).","journal-title":"Plant Cell"},{"key":"56477_CR8","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1007\/PL00000910","volume":"58","author":"V Pancholi","year":"2001","unstructured":"Pancholi, V. Multifunctional $$\\alpha$$-enolase: its role in diseases. Cell. Mol. Life Sci. CMLS 58, 902\u2013920. https:\/\/doi.org\/10.1007\/PL00000910 (2001).","journal-title":"Cell. Mol. Life Sci. CMLS"},{"key":"56477_CR9","doi-asserted-by":"publisher","first-page":"1609","DOI":"10.1101\/gad.385706","volume":"20","author":"N Entelis","year":"2006","unstructured":"Entelis, N. et al. A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev. 20, 1609\u20131620. https:\/\/doi.org\/10.1101\/gad.385706 (2006).","journal-title":"Genes Dev."},{"key":"56477_CR10","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1016\/j.bbagen.2007.01.015","volume":"1770","author":"A Keller","year":"2007","unstructured":"Keller, A. et al. Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim. Biophys. Acta - Gener. Subj. 1770, 919\u2013926. https:\/\/doi.org\/10.1016\/j.bbagen.2007.01.015 (2007).","journal-title":"Biochim. Biophys. Acta - Gener. Subj."},{"key":"56477_CR11","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/S0014-5793(00)01494-0","volume":"473","author":"S Feo","year":"2000","unstructured":"Feo, S., Arcuri, D., Piddini, E., Passantino, R. & Giallongo, A. ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: Relationship with Myc promoter-binding protein 1 (MBP-1). FEBS Lett. 473, 47\u201352. https:\/\/doi.org\/10.1016\/S0014-5793(00)01494-0 (2000).","journal-title":"FEBS Lett."},{"key":"56477_CR12","doi-asserted-by":"publisher","first-page":"2012","DOI":"10.1155\/2012\/156795","volume":"1\u201312","author":"\u00c0 D\u00edaz-Ramos","year":"2012","unstructured":"D\u00edaz-Ramos, \u00c0., Roig-Borrellas, A., Garc\u00eda-Melero, A. & L\u00f3pez-Alemany, R. $$\\alpha$$-Enolase, a multifunctional protein: Its role on pathophysiological situations. J. Biomed. Biotechnol. 1\u201312, 2012. https:\/\/doi.org\/10.1155\/2012\/156795 (2012).","journal-title":"J. Biomed. Biotechnol."},{"key":"56477_CR13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.compbiolchem.2015.04.010","volume":"58","author":"GP Paludo","year":"2015","unstructured":"Paludo, G. P., Lorenzatto, K. R., Bonatto, D. & Ferreira, H. B. Systems biology approach reveals possible evolutionarily conserved moonlighting functions for enolase. Comput. Biol. Chem. 58, 1\u20138. https:\/\/doi.org\/10.1016\/j.compbiolchem.2015.04.010 (2015).","journal-title":"Comput. Biol. Chem."},{"key":"56477_CR14","doi-asserted-by":"publisher","first-page":"1745","DOI":"10.1093\/plcell\/koab283","volume":"34","author":"L Yang","year":"2022","unstructured":"Yang, L. et al. Reduction of the canonical function of a glycolytic enzyme enolase triggers immune responses that further affect metabolism and growth in Arabidopsis. Plant Cell 34, 1745\u20131767. https:\/\/doi.org\/10.1093\/plcell\/koab283 (2022).","journal-title":"Plant Cell"},{"key":"56477_CR15","doi-asserted-by":"publisher","first-page":"7006","DOI":"10.1046\/j.1432-1327.2000.01801.x","volume":"267","author":"S Wagner","year":"2000","unstructured":"Wagner, S. et al. Hev b 9, an enolase and a new cross-reactive allergen from Hevea latex and molds. Eur. J. Biochem. 267, 7006\u20137014. https:\/\/doi.org\/10.1046\/j.1432-1327.2000.01801.x (2000).","journal-title":"Eur. J. Biochem."},{"key":"56477_CR16","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1067\/mai.2000.110799","volume":"106","author":"B Simon-Nobbe","year":"2000","unstructured":"Simon-Nobbe, B. et al. IgE-binding epitopes of enolases, a class of highly conserved fungal allergens. J. Allergy Clin. Immunol. 106, 887\u2013895. https:\/\/doi.org\/10.1067\/mai.2000.110799 (2000).","journal-title":"J. Allergy Clin. Immunol."},{"key":"56477_CR17","doi-asserted-by":"publisher","first-page":"6789","DOI":"10.1128\/jb.174.21.6789-6799.1992","volume":"174","author":"P Sundstrom","year":"1992","unstructured":"Sundstrom, P. & Aliaga, G. R. Molecular cloning of cDNA and analysis of protein secondary structure of Candida albicans enolase, an abundant, immunodominant glycolytic enzyme. J. Bacteriol. 174, 6789\u20136799. https:\/\/doi.org\/10.1128\/jb.174.21.6789-6799.1992 (1992).","journal-title":"J. Bacteriol."},{"key":"56477_CR18","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1093\/infdis\/170.2.390","volume":"170","author":"P Sundstrom","year":"1994","unstructured":"Sundstrom, P., Jensen, J. & Balish, E. Humoral and cellular immune responses to enolase after alimentary tract colonization or intravenous immunization with Candida albicans. J. Inf. Dis. 170, 390\u2013395. https:\/\/doi.org\/10.1093\/infdis\/170.2.390 (1994).","journal-title":"J. Inf. Dis."},{"key":"56477_CR19","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1099\/00221287-143-2-313","volume":"143","author":"P Eroles","year":"1997","unstructured":"Eroles, P., Sentandreu, M., Elorza, M. V. & Sentandreu, R. The highly immunogenic enolase and Hsp70p are adventitious Candida albicans cell wall proteins. Microbiology 143, 313\u2013320. https:\/\/doi.org\/10.1099\/00221287-143-2-313 (1997).","journal-title":"Microbiology"},{"key":"56477_CR20","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1111\/j.1365-2222.1995.tb01090.x","volume":"25","author":"K Ito","year":"1995","unstructured":"Ito, K., Ishiguro, A., Kanbe, T., Tanaka, K. & Torii, S. Characterization of IgE-binding epitopes on Candida albicans enolase. Clin. Exp. Allergy 25, 529\u2013535. https:\/\/doi.org\/10.1111\/j.1365-2222.1995.tb01090.x (1995).","journal-title":"Clin. Exp. Allergy"},{"key":"56477_CR21","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1159\/000234572","volume":"86","author":"BA Baldo","year":"1988","unstructured":"Baldo, B. A. & Baker, R. S. Inhalant allergies to fungi: Reactions to bakers\u2019 yeast (Saccharomyces cerevisiae) and identification of bakers\u2019 yeast enolase as an important allergen. Int. Arch. Allergy and Immunol. 86, 201\u2013208. https:\/\/doi.org\/10.1159\/000234572 (1988).","journal-title":"Int. Arch. Allergy and Immunol."},{"key":"56477_CR22","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1016\/S0378-1097(99)00310-9","volume":"177","author":"SR Edwards","year":"1999","unstructured":"Edwards, S. R., Braley, R. & Chaffin, W. L. Enolase is present in the cell wall of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 177, 211\u2013216. https:\/\/doi.org\/10.1016\/S0378-1097(99)00310-9 (1999).","journal-title":"FEMS Microbiol. Lett."},{"key":"56477_CR23","doi-asserted-by":"publisher","first-page":"14523","DOI":"10.1074\/jbc.M600911200","volume":"281","author":"BL Decker","year":"2006","unstructured":"Decker, B. L. & Wickner, W. T. Enolase activates homotypic vacuole fusion and protein transport to the vacuole in yeast. J. Biol. Chem. 281, 14523\u201314528. https:\/\/doi.org\/10.1074\/jbc.M600911200 (2006).","journal-title":"J. Biol. Chem."},{"key":"56477_CR24","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.exppara.2007.03.011","volume":"117","author":"A Marcilla","year":"2007","unstructured":"Marcilla, A. et al. Echinostoma caproni: Identification of enolase in excretory\/secretory products, molecular cloning, and functional expression. Exp. Parasitol. 117, 57\u201364. https:\/\/doi.org\/10.1016\/j.exppara.2007.03.011 (2007).","journal-title":"Exp. Parasitol."},{"key":"56477_CR25","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1000192","author":"S Bellafiore","year":"2008","unstructured":"Bellafiore, S. et al. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathogens https:\/\/doi.org\/10.1371\/journal.ppat.1000192 (2008).","journal-title":"PLoS Pathogens"},{"key":"56477_CR26","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0002467","author":"T Wang","year":"2013","unstructured":"Wang, T. et al. Proteomic analysis of the excretory-secretory products from larval stages of Ascaris suum reveals high abundance of glycosyl hydrolases. PLoS Negl. Trop. Dis. https:\/\/doi.org\/10.1371\/journal.pntd.0002467 (2013).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"56477_CR27","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.exppara.2016.12.001","volume":"172","author":"S Umair","year":"2017","unstructured":"Umair, S., Bouchet, C. L., Knight, J. S., Pernthaner, A. & Simpson, H. V. Molecular and biochemical characterisation and recognition by the immune host of the enolase of the abomasal nematode parasite Teladorsagia circumcincta. Exp. Parasitol. 172, 30\u201338. https:\/\/doi.org\/10.1016\/j.exppara.2016.12.001 (2017).","journal-title":"Exp. Parasitol."},{"key":"56477_CR28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fimmu.2018.00850","volume":"9","author":"RM Eichenberger","year":"2018","unstructured":"Eichenberger, R. M. et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front. Immunol. 9, 1\u201314. https:\/\/doi.org\/10.3389\/fimmu.2018.00850 (2018).","journal-title":"Front. Immunol."},{"key":"56477_CR29","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1038\/nrm.2017.125","volume":"19","author":"G Van Niel","year":"2018","unstructured":"Van Niel, G., D\u2019Angelo, G. & Raposo, G. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Biol. 19, 213\u2013228. https:\/\/doi.org\/10.1038\/nrm.2017.125 (2018).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"56477_CR30","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.molbiopara.2012.06.006","volume":"185","author":"H Liu","year":"2012","unstructured":"Liu, H. et al. Steinernema glaseri surface enolase: Molecular cloning, biological characterization, and role in host immune suppression. Mol. Biochem. Parasitol. 185, 89\u201398. https:\/\/doi.org\/10.1016\/j.molbiopara.2012.06.006 (2012).","journal-title":"Mol. Biochem. Parasitol."},{"key":"56477_CR31","doi-asserted-by":"publisher","first-page":"3478","DOI":"10.1016\/j.vaccine.2012.02.075","volume":"30","author":"N Chen","year":"2012","unstructured":"Chen, N. et al. Ascaris suum enolase is a potential vaccine candidate against ascariasis. Vaccine 30, 3478\u20133482. https:\/\/doi.org\/10.1016\/j.vaccine.2012.02.075 (2012).","journal-title":"Vaccine"},{"key":"56477_CR32","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1515\/ap-2018-0029","volume":"63","author":"X Zhang","year":"2018","unstructured":"Zhang, X., Xu, L., Song, X., Li, X. & Yan, R. Molecular cloning of enolase from Trichinella spiralis and the protective immunity in mice. Acta Parasitol. 63, 252\u2013260. https:\/\/doi.org\/10.1515\/ap-2018-0029 (2018).","journal-title":"Acta Parasitol."},{"key":"56477_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00430-005-0236-7","volume":"195","author":"E Rodr\u00edguez","year":"2006","unstructured":"Rodr\u00edguez, E. et al. A recombinant enolase from Anisakis simplex is differentially recognized in natural human and mouse experimental infections. Med. Microbiol. Immunol. 195, 1\u201310. https:\/\/doi.org\/10.1007\/s00430-005-0236-7 (2006).","journal-title":"Med. Microbiol. Immunol."},{"key":"56477_CR34","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","volume":"3","author":"S Savary","year":"2019","unstructured":"Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430\u2013439. https:\/\/doi.org\/10.1038\/s41559-018-0793-y (2019).","journal-title":"Nat. Ecol. Evol."},{"key":"56477_CR35","doi-asserted-by":"publisher","first-page":"6190","DOI":"10.1038\/s41467-022-33769-w","volume":"13","author":"S Siddique","year":"2022","unstructured":"Siddique, S. et al. The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5. Nat. Commun. https:\/\/doi.org\/10.1038\/s41467-022-33769-w (2022).","journal-title":"Nat. Commun."},{"key":"56477_CR36","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1023\/A:1008609409465","volume":"103","author":"M Sobczak","year":"1997","unstructured":"Sobczak, M., Golinowski, W. & Grundler, F. M. Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur. J. Plant Pathol. 103, 113\u2013124. https:\/\/doi.org\/10.1023\/A:1008609409465 (1997).","journal-title":"Eur. J. Plant Pathol."},{"key":"56477_CR37","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1038\/s41586-024-07487-w","volume":"630","author":"J Abramson","year":"2024","unstructured":"Abramson, J. et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 630, 493\u2013500. https:\/\/doi.org\/10.1038\/s41586-024-07487-w (2024).","journal-title":"Nature"},{"key":"56477_CR38","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1038\/333683a0","volume":"333","author":"L Lebioda","year":"1988","unstructured":"Lebioda, L. & Stec, B. Crystal structure of enolase indicates that enolase and pyruvate kinase evolved from a common ancestor. Nature 333, 683\u2013686. https:\/\/doi.org\/10.1038\/333683a0 (1988).","journal-title":"Nature"},{"key":"56477_CR39","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1038\/s41587-021-01156-3","volume":"40","author":"F Teufel","year":"2022","unstructured":"Teufel, F. et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat. Biotechnol. 40, 1023\u20131025. https:\/\/doi.org\/10.1038\/s41587-021-01156-3 (2022).","journal-title":"Nat. Biotechnol."},{"key":"56477_CR40","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1104\/pp.106.079467","volume":"141","author":"MA Torres","year":"2006","unstructured":"Torres, M. A., Jones, J. D. & Dangl, J. L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373\u2013378. https:\/\/doi.org\/10.1104\/pp.106.079467 (2006).","journal-title":"Plant Physiol."},{"key":"56477_CR41","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1038\/415977a","volume":"415","author":"T Asai","year":"2002","unstructured":"Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977\u2013983. https:\/\/doi.org\/10.1038\/415977a (2002).","journal-title":"Nature"},{"key":"56477_CR42","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1016\/j.plantsci.2004.09.016","volume":"168","author":"MS Zheng","year":"2005","unstructured":"Zheng, M. S., Takahashi, H., Miyazaki, A., Yamaguchi, K. & Kusano, T. Identification of the cis-acting elements in Arabidopsis thaliana NHL10 promoter responsible for leaf senescence, the hypersensitive response against Cucumber mosaic virus infection, and spermine treatment. Plant Sci. 168, 415\u2013422. https:\/\/doi.org\/10.1016\/j.plantsci.2004.09.016 (2005).","journal-title":"Plant Sci."},{"key":"56477_CR43","doi-asserted-by":"publisher","first-page":"2419","DOI":"10.1105\/tpc.11.12.2419","volume":"11","author":"N Zhou","year":"1999","unstructured":"Zhou, N., Tootle, T. L. & Glazebrook, J. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11, 2419\u20132428. https:\/\/doi.org\/10.1105\/tpc.11.12.2419 (1999).","journal-title":"Plant Cell"},{"key":"56477_CR44","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1105\/tpc.108.063115","volume":"21","author":"M Pfalz","year":"2009","unstructured":"Pfalz, M., Vogel, H. & Kroymann, J. The gene controlling the Indole Glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21, 985\u2013999. https:\/\/doi.org\/10.1105\/tpc.108.063115 (2009).","journal-title":"Plant Cell"},{"key":"56477_CR45","doi-asserted-by":"publisher","first-page":"952","DOI":"10.1104\/pp.107.115691","volume":"146","author":"HS Chung","year":"2008","unstructured":"Chung, H. S. et al. Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 146, 952\u2013964. https:\/\/doi.org\/10.1104\/pp.107.115691 (2008).","journal-title":"Plant Physiol."},{"key":"56477_CR46","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1105\/tpc.16.00931","volume":"29","author":"TL Karasov","year":"2017","unstructured":"Karasov, T. L., Chae, E., Herman, J. J. & Bergelson, J. Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29, 666\u2013680. https:\/\/doi.org\/10.1105\/tpc.16.00931 (2017).","journal-title":"Plant Cell"},{"key":"56477_CR47","doi-asserted-by":"publisher","first-page":"2753","DOI":"10.1128\/mcb.7.8.2753-2761.1987","volume":"7","author":"R Cohen","year":"1987","unstructured":"Cohen, R., Yokoi, T., Holland, J. P., Pepper, A. E. & Holland, M. J. Transcription of the constitutively expressed yeast enolase gene ENO1 is mediated by positive and negative cis-acting regulatory sequences. Mol. Cell. Biol. 7, 2753\u20132761. https:\/\/doi.org\/10.1128\/mcb.7.8.2753-2761.1987 (1987).","journal-title":"Mol. Cell. Biol."},{"key":"56477_CR48","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1006\/jmbi.2001.4730","volume":"309","author":"F Dzierszinski","year":"2001","unstructured":"Dzierszinski, F., Mortuaire, M., Dendouga, N., Popescu, O. & Tomavo, S. Differential expression of two plant-like enolases with distinct enzymatic and antigenic properties during stage conversion of the protozoan parasite Toxoplasma gondii. J. Mol. Biol. 309, 1017\u20131027. https:\/\/doi.org\/10.1006\/jmbi.2001.4730 (2001).","journal-title":"J. Mol. Biol."},{"key":"56477_CR49","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1093\/abbs\/gmq084","volume":"42","author":"Y Liu","year":"2010","unstructured":"Liu, Y. et al. CDNA cloning and expression pattern of two enolase genes from the Chinese oak silkworm, Antheraea pernyi. Acta Biochim. Biophys. Sin. 42, 816\u2013826. https:\/\/doi.org\/10.1093\/abbs\/gmq084 (2010).","journal-title":"Acta Biochim. Biophys. Sin."},{"key":"56477_CR50","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/vaccines8030415","volume":"8","author":"Z Li","year":"2020","unstructured":"Li, Z. et al. An unbiased immunization strategy results in the identification of enolase as a potential marker for nanobody-based detection of Trypanosoma evansi. Vaccines 8, 1\u201320. https:\/\/doi.org\/10.3390\/vaccines8030415 (2020).","journal-title":"Vaccines"},{"key":"56477_CR51","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens10070825","author":"T Wang","year":"2021","unstructured":"Wang, T. & Gasser, R. B. Prospects of using high-throughput proteomics to underpin the discovery of animal host-nematode interactions. Pathogens https:\/\/doi.org\/10.3390\/pathogens10070825 (2021).","journal-title":"Pathogens"},{"key":"56477_CR52","doi-asserted-by":"publisher","first-page":"16136","DOI":"10.1074\/jbc.M400139200","volume":"279","author":"NM Stano","year":"2004","unstructured":"Stano, N. M. & Patel, S. S. t7 lysozyme represses T7 RNA polymerase transcription by destabilizing the open complex during initiation. J. Biol. Chem. 279, 16136\u201316143. https:\/\/doi.org\/10.1074\/jbc.M400139200 (2004).","journal-title":"J. Biol. Chem."},{"key":"56477_CR53","doi-asserted-by":"publisher","first-page":"21731","DOI":"10.1021\/acs.jafc.4c05931","volume":"72","author":"J Gao","year":"2024","unstructured":"Gao, J. et al. Molecular cloning, prokaryotic expression, and immunological characterization of $$\\beta$$-enolase from grass carp (Ctenopharyngodon idella). J. Agric. Food Chem. 72, 21731\u201321740. https:\/\/doi.org\/10.1021\/acs.jafc.4c05931 (2024).","journal-title":"J. Agric. Food Chem."},{"key":"56477_CR54","doi-asserted-by":"publisher","first-page":"7181","DOI":"10.1016\/s0021-9258(18)34554-x","volume":"257","author":"L McAlister","year":"1982","unstructured":"McAlister, L. & Holland, M. J. Targeted deletion of a yeast enolase structural gene: Identification and isolation of yeast enolase isozymes. J. Biol. Chem. 257, 7181\u20137188. https:\/\/doi.org\/10.1016\/s0021-9258(18)34554-x (1982).","journal-title":"J. Biol. Chem."},{"key":"56477_CR55","doi-asserted-by":"publisher","first-page":"12526","DOI":"10.1021\/bi9712450","volume":"36","author":"E Zhang","year":"1997","unstructured":"Zhang, E., Brewer, J. M., Minor, W., Carreira, L. A. & Lebioda, L. Mechanism of enolase: The crystal structure of asymmetric dimer enolase- 2-phospho-D-glycerate\/enolase-phosphoenolpyruvate at 2.0 \u00c5 resolution. Biochemistry 36, 12526\u201312534. https:\/\/doi.org\/10.1021\/bi9712450 (1997).","journal-title":"Biochemistry"},{"key":"56477_CR56","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep45910","volume":"7","author":"RH Wilbers","year":"2017","unstructured":"Wilbers, R. H. et al. Production and glyco-engineering of immunomodulatory helminth glycoproteins in plants. Sci. Rep. 7, 1\u201310. https:\/\/doi.org\/10.1038\/srep45910 (2017).","journal-title":"Sci. Rep."},{"key":"56477_CR57","doi-asserted-by":"publisher","first-page":"944","DOI":"10.2741\/4526","volume":"22","author":"P Cappello","year":"2017","unstructured":"Cappello, P., Principe, M., Bulfamante, S. & Novelli, F. Alpha-Enolase (ENO1), a potential target in novel immunotherapies. Front. Biosci. Landmark 22, 944\u2013959. https:\/\/doi.org\/10.2741\/4526 (2017).","journal-title":"Front. Biosci. Landmark"},{"key":"56477_CR58","doi-asserted-by":"publisher","first-page":"3981","DOI":"10.7150\/ijbs.63556","volume":"17","author":"G Qiao","year":"2021","unstructured":"Qiao, G., Wu, A., Chen, X., Tian, Y. & Lin, X. Enolase 1, a moonlighting protein, as a potential target for cancer treatment. Int. J. Biol. Sci. 17, 3981\u20133992. https:\/\/doi.org\/10.7150\/ijbs.63556 (2021).","journal-title":"Int. J. Biol. Sci."},{"key":"56477_CR59","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1038\/nature05286","volume":"444","author":"JD Jones","year":"2006","unstructured":"Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323\u2013329. https:\/\/doi.org\/10.1038\/nature05286 (2006).","journal-title":"Nature"},{"key":"56477_CR60","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1038\/s41586-021-03315-7","volume":"592","author":"BPM Ngou","year":"2021","unstructured":"Ngou, B. P. M., Ahn, H. K., Ding, P. & Jones, J. D. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110\u2013115. https:\/\/doi.org\/10.1038\/s41586-021-03315-7 (2021).","journal-title":"Nature"},{"key":"56477_CR61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep23796","volume":"6","author":"C Guillou","year":"2016","unstructured":"Guillou, C. et al. Soluble alpha-enolase activates monocytes by CD14-dependent TLR4 signalling pathway and exhibits a dual function. Sci. Rep. 6, 1\u201312. https:\/\/doi.org\/10.1038\/srep23796 (2016).","journal-title":"Sci. Rep."},{"key":"56477_CR62","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1007\/s00436-007-0668-7","volume":"101","author":"G Vanegas","year":"2007","unstructured":"Vanegas, G. et al. Enolase as a plasminogen binding protein in Leishmania mexicana. Parasitol. Res. 101, 1511\u20131516. https:\/\/doi.org\/10.1007\/s00436-007-0668-7 (2007).","journal-title":"Parasitol. Res."},{"key":"56477_CR63","doi-asserted-by":"publisher","first-page":"986","DOI":"10.1016\/j.bbapap.2008.03.017","volume":"1784","author":"S Agarwal","year":"2008","unstructured":"Agarwal, S., Kulshreshtha, P., Bambah Mukku, D. & Bhatnagar, R. $$\\alpha$$-Enolase binds to human plasminogen on the surface of Bacillus anthracis. Biochim. Biophys. Acta Proteins Proteom. 1784, 986\u2013994. https:\/\/doi.org\/10.1016\/j.bbapap.2008.03.017 (2008).","journal-title":"Biochim. Biophys. Acta Proteins Proteom."},{"key":"56477_CR64","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1111\/boc.201500095","volume":"108","author":"G Grossi","year":"2016","unstructured":"Grossi, G. et al. Extracellular matrix degradation via enolase\/plasminogen interaction: Evidence for a mechanism conserved in Metazoa. Biol. Cell 108, 161\u2013178. https:\/\/doi.org\/10.1111\/boc.201500095 (2016).","journal-title":"Biol. Cell"},{"key":"56477_CR65","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pntd.0012069","volume":"18","author":"E O\u2019Kelly","year":"2024","unstructured":"O\u2019Kelly, E. et al. Moonlighting on the Fasciola hepatica tegument: Enolase, a glycolytic enzyme, interacts with the extracellular matrix and fibrinolytic system of the host. PLoS Negl. Trop. Dis. 18, 1\u201324. https:\/\/doi.org\/10.1371\/journal.pntd.0012069 (2024).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"56477_CR66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2017.01760","volume":"8","author":"L Stavolone","year":"2017","unstructured":"Stavolone, L. & Lionetti, V. Extracellular matrix in plants and animals: Hooks and locks for viruses. Front. Microbiol. 8, 1\u20138. https:\/\/doi.org\/10.3389\/fmicb.2017.01760 (2017).","journal-title":"Front. Microbiol."},{"key":"56477_CR67","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.1016\/S0020-7519(02)00178-9","volume":"32","author":"L Fioretti","year":"2002","unstructured":"Fioretti, L., Porter, A., Haydock, P. & Curtis, R. Monoclonal antibodies reactive with secreted\u2013excreted products from the amphids and the cuticle surface of Globodera pallida affect nematode movement and delay invasion of potato roots. Int. J. Parasitol. 32, 1709\u20131718. https:\/\/doi.org\/10.1016\/S0020-7519(02)00178-9 (2002).","journal-title":"Int. J. Parasitol."},{"key":"56477_CR68","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1093\/bfgp\/elm006","volume":"6","author":"RHC Curtis","year":"2007","unstructured":"Curtis, R. H. C. Plant parasitic nematode proteins and the host parasite interaction. Brief. Funct. Genom. Proteom. 6, 50\u201358. https:\/\/doi.org\/10.1093\/bfgp\/elm006 (2007).","journal-title":"Brief. Funct. Genom. Proteom."},{"key":"56477_CR69","doi-asserted-by":"publisher","first-page":"1289","DOI":"10.1094\/PHYTO-04-10-0109","volume":"100","author":"R Shinya","year":"2010","unstructured":"Shinya, R., Morisaka, H., Takeuchi, Y., Ueda, M. & Futai, K. Comparison of the surface coat proteins of the pine wood nematode appeared during host pine infection and in vitro culture by a proteomic approach. Phytopathology 100, 1289\u20131297. https:\/\/doi.org\/10.1094\/PHYTO-04-10-0109 (2010).","journal-title":"Phytopathology"},{"key":"56477_CR70","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-04185-8","volume":"7","author":"G Perconti","year":"2017","unstructured":"Perconti, G. et al. Pro-invasive stimuli and the interacting protein Hsp70 favour the route of alpha-enolase to the cell surface. Sci. Rep. 7, 1\u201312. https:\/\/doi.org\/10.1038\/s41598-017-04185-8 (2017).","journal-title":"Sci. Rep."},{"key":"56477_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.ppat.1012395","volume":"20","author":"B Molloy","year":"2024","unstructured":"Molloy, B. et al. The origin, deployment, and evolution of a plant-parasitic nematode effectorome. PLoS Pathog. 20, 1\u201322. https:\/\/doi.org\/10.1371\/journal.ppat.1012395 (2024).","journal-title":"PLoS Pathog."},{"key":"56477_CR72","first-page":"153","volume":"9","author":"U Wyss","year":"1986","unstructured":"Wyss, U. & Zunke, U. Observation of the behaviour of second stage juveniles of Heterodera schachtii inside host roots. Revue .N\u00e9matol. 9, 153\u2013166 (1986).","journal-title":"Revue .N\u00e9matol."},{"key":"56477_CR73","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1093\/molbev\/msab120","volume":"38","author":"K Tamura","year":"2021","unstructured":"Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022\u20133027. https:\/\/doi.org\/10.1093\/molbev\/msab120 (2021).","journal-title":"Mol. Biol. Evol."},{"key":"56477_CR74","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1093\/oxfordjournals.molbev.a040454","volume":"4","author":"N Saitou","year":"1987","unstructured":"Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406\u2013425. https:\/\/doi.org\/10.1093\/oxfordjournals.molbev.a040454 (1987).","journal-title":"Mol. Biol. Evol."},{"key":"56477_CR75","doi-asserted-by":"publisher","first-page":"783","DOI":"10.2307\/2408678","volume":"39","author":"J Felsenstein","year":"1985","unstructured":"Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783. https:\/\/doi.org\/10.2307\/2408678 (1985).","journal-title":"Evolution"},{"key":"56477_CR76","doi-asserted-by":"publisher","first-page":"1351","DOI":"10.1006\/jmbi.1999.3310","volume":"294","author":"N Blom","year":"1999","unstructured":"Blom, N., Gammeltoft, S. & Brunak, S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351\u20131362. https:\/\/doi.org\/10.1006\/jmbi.1999.3310 (1999).","journal-title":"J. Mol. Biol."},{"key":"56477_CR77","first-page":"310","volume":"7","author":"R Gupta","year":"2002","unstructured":"Gupta, R. & Brunak, S. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac. Sympo. Biocomput. 7, 310\u2013322 (2002).","journal-title":"Pac. Sympo. Biocomput."},{"key":"56477_CR78","doi-asserted-by":"publisher","first-page":"45e","DOI":"10.1093\/nar\/29.9.e45","volume":"29","author":"MW Pfaffl","year":"2001","unstructured":"Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45e\u2013445. https:\/\/doi.org\/10.1093\/nar\/29.9.e45 (2001).","journal-title":"Nucleic Acids Res."},{"key":"56477_CR79","doi-asserted-by":"publisher","first-page":"2","DOI":"10.3732\/apps.1400033","volume":"2","author":"HM Easlon","year":"2014","unstructured":"Easlon, H. M. & Bloom, A. J. Easy Leaf Area: Automated digital image analysis for rapid and accurate measurement of leaf area. Appl. Plant Sci. 2, 2\u20135. https:\/\/doi.org\/10.3732\/apps.1400033 (2014).","journal-title":"Appl. Plant Sci."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-026-56477-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-026-56477-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-026-56477-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,8]],"date-time":"2026-06-08T13:29:09Z","timestamp":1780925349000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-026-56477-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,8]]},"references-count":79,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["56477"],"URL":"https:\/\/doi.org\/10.1038\/s41598-026-56477-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,8]]},"assertion":[{"value":"1 April 2026","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 June 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 June 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"17692"}}