{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,8]],"date-time":"2026-08-08T14:43:40Z","timestamp":1786200220940,"version":"build-2736575974"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"8","license":[{"start":{"date-parts":[[2026,4,16]],"date-time":"2026-04-16T00:00:00Z","timestamp":1776297600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"German Federal Ministry of Research and Education","award":["031B1070B"],"award-info":[{"award-number":["031B1070B"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Apple replant disease (ARD) is a soil-borne disease that arises from replanting apple trees on land previously used for apple cultivation. There is interest in biomarkers that can reliably assess the severity of ARD by quantifying how strongly apple plants react to the disease in soils of different agro-environments. Thus far, transcriptomic studies of ARD-affected plants have examined only a few soils at a time, revealing that expression patterns vary among different soils. Here, we analyzed the expression of 90 candidate genes in the roots of apple plants (rootstock genotype \u2018M.26\u2019) grown in ARD-affected soils from 151 sites across Germany to test whether a consistent pattern of gene expression under ARD-conditions exists. Additionally, the expression of the candidate genes was analyzed in the leaves of apple plants grown in 18 different ARD-affected soils. Most of the genes (72) showed significantly upregulated expression in roots under ARD conditions, while only 11 showed significantly upregulated expression in leaves, suggesting that these genes play a significant role in the ARD reaction in roots but only a limited or no role in leaves. The candidate genes were evaluated for their potential as ARD biomarkers, defined by their consistently increased expression under ARD conditions across different soils and correlation with ARD severity. The accordingly selected ARD biomarker genes in roots include genes involved in phytoalexin biosynthesis, lignin metabolism, ethylene metabolism, cyanogenesis, detoxification, programmed-cell-death, and plant defense. These biomarkers have the potential to assess the severity of ARD and open up new possibilities for disease diagnosis.<\/jats:p>","DOI":"10.1093\/hr\/uhag140","type":"journal-article","created":{"date-parts":[[2026,4,15]],"date-time":"2026-04-15T11:39:39Z","timestamp":1776253179000},"source":"Crossref","is-referenced-by-count":0,"title":["Establishing a biomarker set for the diagnosis of apple replant disease using qPCR"],"prefix":"10.1093","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0003-4241-6952","authenticated-orcid":false,"given":"Luisa","family":"Baader","sequence":"first","affiliation":[{"name":"Julius K\u00fchn Institute (JKI) \u2013 Federal Research Centre for Cultivated Plants, Institute for Breeding Research on Fruit Crops , 01326 Dresden-Pillnitz ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susan","family":"Schr\u00f6pfer","sequence":"additional","affiliation":[{"name":"Julius K\u00fchn Institute (JKI) \u2013 Federal Research Centre for Cultivated Plants, Institute for Breeding Research on Fruit Crops , 01326 Dresden-Pillnitz ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefanie","family":"Reim","sequence":"additional","affiliation":[{"name":"Julius K\u00fchn Institute (JKI) \u2013 Federal Research Centre for Cultivated Plants, Institute for Breeding Research on Fruit Crops , 01326 Dresden-Pillnitz ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2509-1418","authenticated-orcid":false,"given":"Traud","family":"Winkelmann","sequence":"additional","affiliation":[{"name":"Institute of Plant Genetics, Leibniz University Hannover , 30419 Hannover ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nils","family":"Orth","sequence":"additional","affiliation":[{"name":"Institute of Plant Genetics, Leibniz University Hannover , 30419 Hannover ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiem","family":"Krueger","sequence":"additional","affiliation":[{"name":"Institute of Earth System Sciences, Section Soil Science, Leibniz University Hannover , 30419 Hannover ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"Guggenberger","sequence":"additional","affiliation":[{"name":"Institute of Earth System Sciences, Section Soil Science, Leibniz University Hannover , 30419 Hannover ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jens","family":"Boy","sequence":"additional","affiliation":[{"name":"Institute of Earth System Sciences, Section Soil Science, Leibniz University Hannover , 30419 Hannover ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacqueline","family":"Kaldun","sequence":"additional","affiliation":[{"name":"Bayreuth Centre for Ecology and Environmental Research, University Bayreuth , 95448 Bayreuth ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Lehndorff","sequence":"additional","affiliation":[{"name":"Bayreuth Centre for Ecology and Environmental Research, University Bayreuth , 95448 Bayreuth ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nele","family":"Meyer","sequence":"additional","affiliation":[{"name":"Goethe University Frankfurt, Institute of Physical Geography , 60438 Frankfurt ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristin","family":"Hauschild","sequence":"additional","affiliation":[{"name":"Julius K\u00fchn Institute (JKI) \u2013 Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics , 38104 Braunschweig ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henryk","family":"Flachowsky","sequence":"additional","affiliation":[{"name":"Julius K\u00fchn Institute (JKI) \u2013 Federal Research Centre for Cultivated Plants, Institute for Breeding Research on Fruit Crops , 01326 Dresden-Pillnitz ,","place":["Germany"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,4,16]]},"reference":[{"key":"2026080810120461700_ref33","article-title":"Data from: ORDIAmur central experiment 12 (CE12) growth data","author":"Winkelmann","year":"2026","journal-title":"BonaRes Repository"},{"key":"2026080810120461700_ref32","article-title":"Data from: ORDIAmur central experiment 12 \u2013 gene expression data","author":"Baader","year":"2026","journal-title":"BonaRes Repository"},{"key":"2026080810120461700_ref1","doi-asserted-by":"crossref","first-page":"89","DOI":"10.21775\/cimb.030.089","article-title":"Apple replant disease: causes and mitigation strategies","volume":"30","author":"Winkelmann","year":"2019","journal-title":"Current Issues in Mol Biol"},{"key":"2026080810120461700_ref2","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1094\/PHYTO.1998.88.9.930","article-title":"Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington","volume":"88","author":"Mazzola","year":"1998","journal-title":"Phytopathology."},{"key":"2026080810120461700_ref3","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1146\/annurev-phyto-081211-173005","article-title":"Apple replant disease: role of microbial ecology in cause and control","volume":"50","author":"Mazzola","year":"2012","journal-title":"Annu Rev Phytopathol"},{"key":"2026080810120461700_ref4","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.scienta.2018.09.014","article-title":"Diagnosis of apple replant disease (ARD): microscopic evidence of early symptoms in fine roots of different apple rootstock genotypes","volume":"243","author":"Grunewaldt-St\u00f6cker","year":"2019","journal-title":"Sci Hortic"},{"key":"2026080810120461700_ref5","first-page":"11","article-title":"The Impact of Replant Problem on the Economics of High Density Apple Plantings","volume-title":"Acta Hortic.","author":"George","year":"1994"},{"key":"2026080810120461700_ref6","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1007\/s11104-012-1454-6","article-title":"Evaluation of apple replant problems based on different soil disinfection treatments\u2014links to soil microbial community structure?","volume":"366","author":"Yim","year":"2013","journal-title":"Plant Soil"},{"key":"2026080810120461700_ref7","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2022.949404","article-title":"Toward a holistic view of orchard ecosystem dynamics: a comprehensive review of the multiple factors governing development or suppression of apple replant disease","volume":"13","author":"Somera","year":"2022","journal-title":"Front Microbiol"},{"key":"2026080810120461700_ref8","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.hpj.2018.05.003","article-title":"Analysis of the fungal community in apple replanted soil around Bohai Gulf","volume":"4","author":"Wang","year":"2018","journal-title":"Horticultural Plant Journal"},{"key":"2026080810120461700_ref9","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/s41348-019-00236-6","article-title":"A soil-free method for assessing pathogenicity of fungal isolates from apple roots","volume":"126","author":"Popp","year":"2019","journal-title":"Journal of Plant Diseases and Protection"},{"key":"2026080810120461700_ref10","doi-asserted-by":"crossref","DOI":"10.1016\/j.rhisph.2020.100300","article-title":"Phytotoxins from dactylonectria torresensis involved in replant disease of fruit trees","volume":"17","author":"Manici","year":"2021","journal-title":"Rhizosphere."},{"key":"2026080810120461700_ref11","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1094\/PBIOMES-07-20-0053-R","article-title":"Molecular barcoding reveals the genus Streptomyces as associated root endophytes of apple (Malus domestica) plants grown in soils affected by apple replant disease","volume":"5","author":"Mahnkopp-Dirks","year":"2020","journal-title":"Phytobiomes Journal"},{"key":"2026080810120461700_ref12","first-page":"01224","article-title":"Different bacterial communities in heat and gamma irradiation treated replant disease soils revealed by 16S rRNA gene analysis\u2014contribution to improved aboveground apple plant growth?","volume":"6","author":"Yim","year":"2015","journal-title":"Original Research Frontiers in Microbiology"},{"key":"2026080810120461700_ref13","doi-asserted-by":"crossref","first-page":"fiab031","DOI":"10.1093\/femsec\/fiab031","article-title":"Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis","volume":"97","author":"Balb\u00edn-Su\u00e1rez","year":"2021","journal-title":"FEMS Microbiol Ecol"},{"key":"2026080810120461700_ref14","doi-asserted-by":"crossref","DOI":"10.1016\/j.scienta.2019.108809","article-title":"In-field heterogeneity of apple replant disease: relations to abiotic soil properties","volume":"259","author":"Simon","year":"2020","journal-title":"Sci Hortic"},{"key":"2026080810120461700_ref15","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s11104-024-07091-x","article-title":"Linking soil characteristics, rhizosphere microbiome composition, and plant defence reaction to apple replant disease severity","volume":"512","author":"Orth","year":"2024","journal-title":"Plant Soil"},{"key":"2026080810120461700_ref55","doi-asserted-by":"crossref","first-page":"fiaf055","DOI":"10.1093\/femsec\/fiaf055","article-title":"Catch crop amendments and microbial 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soil","volume":"192","author":"Busnena","year":"2021","journal-title":"Phytochemistry."},{"key":"2026080810120461700_ref24","doi-asserted-by":"crossref","DOI":"10.1016\/j.scienta.2024.112902","article-title":"Differential accumulation of phenolics and phytoalexins in seven Malus genotypes cultivated in apple replant disease-affected soil","volume":"328","author":"Siefen","year":"2024","journal-title":"Sci Hortic"},{"key":"2026080810120461700_ref25","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1080\/07060661.2016.1260640","article-title":"Genotype responses of two apple rootstocks to infection by Pythium ultimum causing apple replant disease","volume":"38","author":"Zhu","year":"2016","journal-title":"Can J Plant Pathol"},{"key":"2026080810120461700_ref26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/hortres.2014.53","article-title":"Transcriptional regulation of ethylene and jasmonate mediated defense response in apple (Malus domestica) root during Pythium ultimum infection","volume":"1","author":"Shin","year":"2014","journal-title":"Hortic Res"},{"key":"2026080810120461700_ref27","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.pmpp.2016.03.003","article-title":"Transcriptome changes specifically associated with apple (Malus domestica) root defense response during Pythium ultimum infection","volume":"94","author":"Shin","year":"2016","journal-title":"Physiol Mol Plant Pathol"},{"key":"2026080810120461700_ref28","doi-asserted-by":"crossref","DOI":"10.1016\/j.pmpp.2020.101567","article-title":"Transcriptome analysis Malus domestica \u2018M9T337\u2019 root molecular responses to Fusarium solani infection","volume":"113","author":"Xiang","year":"2021","journal-title":"Physiol Mol Plant Pathol"},{"key":"2026080810120461700_ref29","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1094\/PBIOMES-08-24-0082-R","article-title":"Apple genotypes and soil properties shape the soil microbiome and influence the plant response 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