{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T11:56:23Z","timestamp":1785412583176,"version":"3.56.0"},"reference-count":48,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T00:00:00Z","timestamp":1782864000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32201445"],"award-info":[{"award-number":["32201445"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32201445"],"award-info":[{"award-number":["32201445"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"\u201cDouble First-Class\u201d Construction Program for Team Development","award":["561120232"],"award-info":[{"award-number":["561120232"]}]},{"DOI":"10.13039\/501100009620","name":"Gansu Provincial Science and Technology Major Projects","doi-asserted-by":"publisher","award":["23ZDNA009"],"award-info":[{"award-number":["23ZDNA009"]}],"id":[{"id":"10.13039\/501100009620","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Inner Mongolia Seed Industry Science and Technology Innovation Major Demonstration Project","award":["2022JBGS0040"],"award-info":[{"award-number":["2022JBGS0040"]}]},{"name":"Gansu Academy of Agricultural Sciences","award":["2025GAAS10"],"award-info":[{"award-number":["2025GAAS10"]}]},{"award":["2025GAAS10"],"award-info":[{"award-number":["2025GAAS10"]}],"id":[{"id":"https:\/\/ror.org\/001tdwk28","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Yunnan Laboratory Construction Special Project for the Shared Platform Construction of the Yuanmou R&D Center, Yunnan Seed Industry Joint Laboratory","award":["202405AR340001"],"award-info":[{"award-number":["202405AR340001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JoF"],"abstract":"<jats:p>Epichlo\u00eb endophytes enhance plant defense and biotic stress resistance through mutualistic interactions in natural hosts. However, whether these protective effects are retained in annual non-native hosts such as barley (Hordeum vulgare L.) remains unclear. An integrated multi-omics approach was used to characterize defense responses in Epichlo\u00eb bromicola-infected barley (LD1) and endophyte-free barley (CK) following pathogen challenge. The results show that LD1 had 20.0% lower disease incidence and 24.1% lower disease index than CK. LD1 also exhibited 21.1% lower malondialdehyde (MDA) content and higher antioxidant enzyme activities, indicating more effective control of oxidative damage and improved redox homeostasis. Integrated transcriptomic and metabolomic analyses revealed distinct defense responses between LD1 and CK. LD1 showed stronger activation of glutathione metabolism and antioxidant pathways than CK after 6 h of endophyte inoculation. This was consistent with more efficient control of early reactive oxygen species (ROS) dynamics. By 48 h, LD1 preferentially enriched phenylpropanoid biosynthesis and mitogen-activated protein kinase (MAPK) signaling, accompanied by increased accumulation of defense-related metabolites and enhanced structural and chemical defenses. Collectively, the study demonstrates that Epichlo\u00eb bromicola enhances disease resistance in barley by reprogramming host defense dynamics from early redox regulation to late structural and chemical reinforcement.<\/jats:p>","DOI":"10.3390\/jof12070484","type":"journal-article","created":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T10:41:01Z","timestamp":1782902461000},"page":"484","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Epichlo\u00eb bromicola Enhances Barley Disease Resistance Through Temporally Coordinated Defense Responses"],"prefix":"10.3390","volume":"12","author":[{"given":"Yufan","family":"Pang","sequence":"first","affiliation":[{"name":"College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China"},{"name":"State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Lanzhou University, Lanzhou 730020, China"},{"name":"Engineering Research Center of Grassland Industry, Ministry of Education, Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou University, Lanzhou 730020, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjing","family":"Zhi","sequence":"additional","affiliation":[{"name":"College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China"},{"name":"State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Lanzhou University, Lanzhou 730020, China"},{"name":"Engineering Research Center of Grassland Industry, Ministry of Education, Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou University, Lanzhou 730020, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenjiang","family":"Chen","sequence":"additional","affiliation":[{"name":"College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China"},{"name":"State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Lanzhou University, Lanzhou 730020, China"},{"name":"Engineering Research Center of Grassland Industry, Ministry of Education, Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou University, Lanzhou 730020, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3170-0483","authenticated-orcid":false,"given":"Kamran","family":"Malik","sequence":"additional","affiliation":[{"name":"College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China"},{"name":"State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Lanzhou University, Lanzhou 730020, China"},{"name":"Engineering Research Center of Grassland Industry, Ministry of Education, Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou University, Lanzhou 730020, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4785-9288","authenticated-orcid":false,"given":"Zhengfeng","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Economic Crops and Malt Barley Research, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueqin","family":"Han","sequence":"additional","affiliation":[{"name":"Institute of Tropical Eco-Agriculture, Yunnan Academy of Agricultural Sciences, Yuanmou County, Chuxiong 651399, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Jin","sequence":"additional","affiliation":[{"name":"Institute of Tropical Eco-Agriculture, Yunnan Academy of Agricultural Sciences, Yuanmou County, Chuxiong 651399, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongshan","family":"Deng","sequence":"additional","affiliation":[{"name":"Institute of Tropical Eco-Agriculture, Yunnan Academy of Agricultural Sciences, Yuanmou County, Chuxiong 651399, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3287-2140","authenticated-orcid":false,"given":"Chunjie","family":"Li","sequence":"additional","affiliation":[{"name":"College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China"},{"name":"State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Lanzhou University, Lanzhou 730020, China"},{"name":"Engineering Research Center of Grassland Industry, Ministry of Education, Gansu Tech Innovation Center of Western China Grassland Industry, Lanzhou University, Lanzhou 730020, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","article-title":"The global burden of pathogens and pests on major food crops","volume":"3","author":"Savary","year":"2019","journal-title":"Nat. Ecol. Evol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e2022239118","DOI":"10.1073\/pnas.2022239118","article-title":"The persistent threat of emerging plant disease pandemics to global food security","volume":"118","author":"Ristaino","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"99","DOI":"10.32782\/2226-0099.2025.145.2.12","article-title":"Major diseases of winter barley and selection for immunity in conditions of climate change","volume":"2","author":"Titov","year":"2025","journal-title":"Taurian Sci. Her."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1186\/s40168-020-00875-0","article-title":"Microbiome definition re-visited: Old concepts and new challenges","volume":"8","author":"Berg","year":"2020","journal-title":"Microbiome"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1038\/s41579-020-0412-1","article-title":"Plant\u2013microbiome interactions: From community assembly to plant health","volume":"18","author":"Trivedi","year":"2020","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1111\/nph.18160","article-title":"Fungal endophytes improve the performance of host plants but do not eliminate the growth\/defence trade-off","volume":"235","author":"Atala","year":"2022","journal-title":"New Phytol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Busby, P.E., Soman, C., Wagner, M.R., Friesen, M.L., Kremer, J., Bennett, A., Morsy, M., Eisen, J.A., Leach, J.E., and Dangl, J.L. (2017). Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol., 15.","DOI":"10.1371\/journal.pbio.2001793"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Fernando, K., Reddy, P., Spangenberg, G.C., Rochfort, S.J., and Guthridge, K.M. (2021). Metabolic Potential of Epichlo\u00eb Endophytes for Host Grass Fungal Disease Resistance. Microorganisms, 10.","DOI":"10.3390\/microorganisms10010064"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Decunta, F.A., P\u00e9rez, L.I., Malinowski, D.P., Molina-Montenegro, M.A., and Gundel, P.E. (2021). A Systematic Review on the Effects of Epichlo\u00eb Fungal Endophytes on Drought Tolerance in Cool-Season Grasses. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.644731"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1308","DOI":"10.1094\/PDIS-06-23-1044-RE","article-title":"High Diversity of Epicoccum Species Associated with Leaf Spot on Italian Ryegrass in Southwestern China: Six New Records and Three New Species","volume":"108","author":"Xu","year":"2024","journal-title":"Plant Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1111\/pce.12621","article-title":"Stress-triggered redox signalling: What\u2019s in pROSpect?","volume":"39","author":"Foyer","year":"2016","journal-title":"Plant Cell Environ."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2821","DOI":"10.1111\/pce.14787","article-title":"The redox code of plants","volume":"47","author":"Mittler","year":"2024","journal-title":"Plant Cell Environ."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Zhong, G., Wang, Z., Tang, D., and Wang, W. (2026). Decoding MAPK cascades in plant immunity: Activation, regulation, integration, and pathogen manipulation. J. Integr. Plant Biol., early view.","DOI":"10.1111\/jipb.70306"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1146\/annurev-arplant-042817-040322","article-title":"Reactive oxygen species in plant signaling","volume":"69","author":"Waszczak","year":"2018","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1111\/jipb.13054","article-title":"Contribution of phenylpropanoid metabolism to plant development and plant\u2013environment interactions","volume":"63","author":"Dong","year":"2021","journal-title":"J. Integr. Plant Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2955","DOI":"10.1007\/s00253-015-6487-3","article-title":"Plant-endophyte symbiosis, an ecological perspective","volume":"99","author":"Wani","year":"2015","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1146\/annurev.arplant.55.031903.141735","article-title":"Symbioses of Grasses with Seedborne Fungal Endophytes","volume":"55","author":"Schardl","year":"2004","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/0003-9861(68)90654-1","article-title":"Photoperoxidation in isolated chloroplasts","volume":"125","author":"Heath","year":"1968","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0168-9452(99)00197-1","article-title":"Oxidative stress and some antioxidant systems in acid rain-treated bean plants","volume":"151","author":"Velikova","year":"2000","journal-title":"Plant Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1104\/pp.59.2.309","article-title":"Superoxide dismutases: I. Occurrence in higher plants","volume":"59","author":"Giannopolitis","year":"1977","journal-title":"Plant Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1002\/9780470110171.ch14","article-title":"The assay of catalases and peroxidases","volume":"1","author":"Maehly","year":"1954","journal-title":"Methods Biochem. Anal."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: A fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: An efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"D587","DOI":"10.1093\/nar\/gkac963","article-title":"KEGG for taxonomy-based analysis of pathways and genomes","volume":"51","author":"Kanehisa","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.tplants.2016.08.002","article-title":"ROS are good","volume":"22","author":"Mittler","year":"2017","journal-title":"Trends Plant Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.pbi.2017.04.022","article-title":"Apoplastic ROS signaling in plant immunity","volume":"38","author":"Qi","year":"2017","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.semcdb.2017.07.013","article-title":"ROS-related redox regulation and signaling in plants","volume":"80","author":"Noctor","year":"2018","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1111\/tpj.14685","article-title":"Rapid systemic signaling during abiotic and biotic stresses: Is the ROS wave master of all trades","volume":"102","author":"Fichman","year":"2020","journal-title":"Plant J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1016\/j.molp.2019.06.003","article-title":"Whole-Plant Live Imaging of Reactive Oxygen Species","volume":"12","author":"Fichman","year":"2019","journal-title":"Mol. Plant"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1016\/j.tplants.2021.01.001","article-title":"The Induced Resistance Lexicon: Do\u2019s and Don\u2019ts","volume":"26","author":"Conrath","year":"2021","journal-title":"Trends Plant Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1146\/annurev-arplant-042916-041132","article-title":"Defense priming: An adaptive part of induced resistance","volume":"68","author":"Baccelli","year":"2017","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_33","first-page":"939","article-title":"Epichlo\u00eb fungal endophytes and plant defenses: Not just alkaloids","volume":"26","author":"Gundel","year":"2021","journal-title":"Trends Plant Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1146\/annurev-phyto-080516-035623","article-title":"Interplay between innate immunity and the plant microbiota","volume":"55","author":"Hacquard","year":"2017","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1126\/science.aaw9285","article-title":"Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome","volume":"366","author":"Cordovez","year":"2019","journal-title":"Science"},{"key":"ref_36","first-page":"713","article-title":"Regulation of primary plant metabolism during plant\u2013pathogen interactions and its contribution to plant defense","volume":"203","author":"Rojas","year":"2014","journal-title":"New Phytol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1094\/MPMI-22-5-0487","article-title":"Primary metabolism and plant defense\u2014Fuel for the fire","volume":"22","author":"Bolton","year":"2009","journal-title":"Mol. Plant. Microbe Interact."},{"key":"ref_38","first-page":"199","article-title":"Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses","volume":"34","author":"Foyer","year":"2011","journal-title":"Plant Cell Environ."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1104\/pp.20.00433","article-title":"Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy","volume":"184","author":"Erb","year":"2020","journal-title":"Plant Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1186\/s13059-017-1215-1","article-title":"Multi-omics approaches to disease","volume":"18","author":"Hasin","year":"2017","journal-title":"Genome Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"R21","DOI":"10.1530\/JME-18-0055","article-title":"Integrated omics: Tools, advances and future approaches","volume":"62","author":"Misra","year":"2019","journal-title":"J. Mol. Endocrinol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., and Zheng, B. (2019). Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress. Molecules, 24.","DOI":"10.3390\/molecules24132452"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Liu, Q., Luo, L., and Zheng, L. (2018). Lignins: Biosynthesis and Biological Functions in Plants. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19020335"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1093\/mp\/ssp106","article-title":"Phenylpropanoid biosynthesis","volume":"3","author":"Vogt","year":"2010","journal-title":"Mol. Plant"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.2307\/3870059","article-title":"Stress-induced phenylpropanoid metabolism","volume":"7","author":"Dixon","year":"1995","journal-title":"Plant Cell"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e0152","DOI":"10.1199\/tab.0152","article-title":"The phenylpropanoid pathway in Arabidopsis","volume":"9","author":"Fraser","year":"2011","journal-title":"Arab. Book"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1038\/s41586-021-03316-6","article-title":"Pattern-recognition receptors are required for NLR-mediated plant immunity","volume":"592","author":"Yuan","year":"2021","journal-title":"Nature"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"eaaw0759","DOI":"10.1126\/sciadv.aaw0759","article-title":"Initial soil microbiome composition and functioning predetermine future plant health","volume":"5","author":"Wei","year":"2019","journal-title":"Sci. Adv."}],"container-title":["Journal of Fungi"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2309-608X\/12\/7\/484\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T12:57:55Z","timestamp":1782910675000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2309-608X\/12\/7\/484"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,1]]},"references-count":48,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["jof12070484"],"URL":"https:\/\/doi.org\/10.3390\/jof12070484","relation":{},"ISSN":["2309-608X"],"issn-type":[{"value":"2309-608X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,1]]}}}