{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T13:59:51Z","timestamp":1790171991076,"version":"4.1.0"},"reference-count":84,"publisher":"American Society for Microbiology","issue":"9","license":[{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"name":"CRIBIQ","award":["2022-031-C98"],"award-info":[{"award-number":["2022-031-C98"]}],"id":[{"id":"https:\/\/ror.org\/02ybbzx72","id-type":"ROR","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["ALLRP 583416-23"],"award-info":[{"award-number":["ALLRP 583416-23"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001804","name":"Canada Research Chairs","doi-asserted-by":"publisher","award":["CRC-2023-00119"],"award-info":[{"award-number":["CRC-2023-00119"]}],"id":[{"id":"10.13039\/501100001804","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Appl Environ Microbiol"],"published-print":{"date-parts":[[2026,9,23]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:sec>\n                    <jats:title\/>\n                    <jats:p>\n                      Bacterial canker of tomato, caused by\n                      <jats:italic toggle=\"yes\">Clavibacter michiganensis<\/jats:italic>\n                      (\n                      <jats:italic toggle=\"yes\">Cm<\/jats:italic>\n                      ), remains difficult to control due to lack of effective management options. In this study, a collection of over 500 bacterial isolates was screened\n                      <jats:italic toggle=\"yes\">in vitro<\/jats:italic>\n                      for antagonistic activity against\n                      <jats:italic toggle=\"yes\">Cm<\/jats:italic>\n                      and plant growth-promoting traits. Based on these results, 32 candidates were evaluated\n                      <jats:italic toggle=\"yes\">in planta<\/jats:italic>\n                      , leading to the identification of three highly effective strains:\n                      <jats:italic toggle=\"yes\">Pantoea agglomerans<\/jats:italic>\n                      SO16PY and two\n                      <jats:italic toggle=\"yes\">Pseudomonas marginalis sensu lato<\/jats:italic>\n                      strains, IRDA16 and SO16PC, which consistently enhanced tomato vegetative growth. Notably,\n                      <jats:italic toggle=\"yes\">P. agglomerans<\/jats:italic>\n                      SO16PY delayed disease onset in\n                      <jats:italic toggle=\"yes\">Cm<\/jats:italic>\n                      -inoculated plants by up to 7 days and significantly reduced wilting severity, lowering the disease severity score from 85% to 45%. Strains IRDA16 and SO16PC also restricted disease development, reducing severity scores to 67.5% and 57.5%, respectively. Whole-genome sequencing and comparative genomics revealed that strains IRDA16 and SO16PC form a distinct, specialized plant-associated lineage within the\n                      <jats:italic toggle=\"yes\">Pseudomonas marginalis<\/jats:italic>\n                      group, exhibiting average nucleotide identity \u2248 96% and digital DNA-DNA hybridization \u2248 69.5% values near species delineation thresholds. Genome mining identified diverse biosynthetic gene clusters encoding non-ribosomal peptide synthetases, the lipopeptide viscosin, and terpenes, which likely drive the biostimulant and antagonistic traits of this novel\n                      <jats:italic toggle=\"yes\">Pseudomonas<\/jats:italic>\n                      lineage. Together, these findings characterize promising bacterial candidates with dual biostimulant and biocontrol capacities while uncovering a genomically distinct\n                      <jats:italic toggle=\"yes\">Pseudomonas<\/jats:italic>\n                      lineage optimized for beneficial plant\u2013microbe interactions in sustainable agriculture.\n                    <\/jats:p>\n                    <jats:sec>\n                      <jats:title>IMPORTANCE<\/jats:title>\n                      <jats:p>\n                        <jats:italic toggle=\"yes\">Clavibacter michiganensis<\/jats:italic>\n                        (\n                        <jats:italic toggle=\"yes\">Cm<\/jats:italic>\n                        ) is a major bacterial pathogen of tomato and poses a significant economic threat to global production. It is classified as an A2 quarantine pathogen by the European and Mediterranean Plant Protection Organization (EPPO). Current management strategies rely largely on chemical control, including copper-based compounds (e.g., Bordeaux mixture, copper oxychloride), mancozeb, and antibiotics like streptomycin. However, these approaches raise increasing concerns related to environmental contamination, phytotoxicity, and the development of resistant pathogen populations. As a sustainable alternative, plant growth-promoting bacteria have emerged as promising biocontrol agents. In this study, we identified bacterial strains exhibiting antagonistic activity against\n                        <jats:italic toggle=\"yes\">Cm<\/jats:italic>\n                        both\n                        <jats:italic toggle=\"yes\">in vitro<\/jats:italic>\n                        and\n                        <jats:italic toggle=\"yes\">in planta<\/jats:italic>\n                        . Notably, these strains also enhanced tomato growth parameters, demonstrating their dual functionality. Given the environmental drawbacks associated with chemical inputs, the use of such beneficial microorganisms represents a promising strategy for advancing sustainable and eco-friendly tomato production systems.\n                      <\/jats:p>\n                    <\/jats:sec>\n                  <\/jats:sec>","DOI":"10.1128\/aem.01087-26","type":"journal-article","created":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T16:25:57Z","timestamp":1788366357000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":0,"title":["Identification of beneficial bacterial strains for tomato growth promotion and biocontrol of bacterial canker caused by\n                    <i>Clavibacter michiganensis<\/i>"],"prefix":"10.1128","volume":"92","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4193-8703","authenticated-orcid":true,"given":"Nasim","family":"Sedighian","sequence":"first","affiliation":[{"name":"Centre Armand-Frappier Sant\u00e9 Biotechnologie, Institut National de la Recherche Scientifique (INRS)","place":["Laval, Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4810-1030","authenticated-orcid":true,"given":"Marie-Christine","family":"Groleau","sequence":"additional","affiliation":[{"name":"Centre Armand-Frappier Sant\u00e9 Biotechnologie, Institut National de la Recherche Scientifique (INRS)","place":["Laval, Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4609-0115","authenticated-orcid":true,"given":"Eric","family":"D\u00e9ziel","sequence":"additional","affiliation":[{"name":"Centre Armand-Frappier Sant\u00e9 Biotechnologie, Institut National de la Recherche Scientifique (INRS)","place":["Laval, Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_4_2_2","unstructured":"FAO. 2023. FAOSTATS. Available from: https:\/\/www.fao.org\/faostat\/en\/#home"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1108\/BFJ-05-2019-0363"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS-09-24-1931-FE"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.3390\/app12031231"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.3390\/bacteria3020005"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.3390\/applmicrobiol5020044"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.923880"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cropro.2015.07.017"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1080\/17429145.2022.2029963"},{"key":"e_1_3_4_11_2","first-page":"11","article-title":"Review of antibacterial activity of plant extracts and growth-promoting microorganism (GPM) against phytopathogenic bacterial tomato crop","volume":"4","author":"Vald\u00e9s RA","year":"2017","unstructured":"Vald\u00e9s RA, Castillo FDH, Cabello JCA, Fuentes YMO, Morales GG, Cant\u00fa DJ, Aguilar CN. 2017. Review of antibacterial activity of plant extracts and growth-promoting microorganism (GPM) against phytopathogenic bacterial tomato crop. Eur J Biotechnol Genet Eng 4:11\u201336.","journal-title":"Eur J Biotechnol Genet Eng"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1111\/epp.12302"},{"key":"e_1_3_4_13_2","first-page":"794","article-title":"A new tomato disease of economic importance","volume":"31","author":"Smith E","year":"1910","unstructured":"Smith E. 1910. A new tomato disease of economic importance. Science 31:794\u2013796.","journal-title":"Science"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.70093"},{"key":"e_1_3_4_15_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10658-015-0738-0"},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS-09-10-0635"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS-08-20-1732-FE"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.heliyon.2020.e05222"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1111\/ppa.13690"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","unstructured":"Patz S Gautam A Becker M Ruppel S Rodr\u00edguez-Palenzuela P Huson D. 2021. PLaBAse: a comprehensive web resource for analyzing the plant growth-promoting potential of plant-associated bacteria. bioRxiv. doi:10.1101\/2021.12.13.472471","DOI":"10.1101\/2021.12.13.472471"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.3390\/jox14010021"},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkaf334"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2019.07.009"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.5424\/sjar\/2017151-9990"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jtemin.2025.100225"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms9061186"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2020.126672"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.48311\/jcp.2017.1351"},{"key":"e_1_3_4_29_2","first-page":"1481","article-title":"Potential of biological treatments for control of bacterial canker of tomato incited by Clavibacter michiganensis spp michiganensis in Morocco","volume":"13","author":"Moustaine M","year":"2019","unstructured":"Moustaine M, El Kahkahi R, Benbouazza A, Benkirane R. 2019. Potential of biological treatments for control of bacterial canker of tomato incited by Clavibacter michiganensis spp michiganensis in Morocco. Eurasia J Biosci 13:1481\u20131488.","journal-title":"Eurasia J Biosci"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbiotec.2014.07.440"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1186\/s41938-022-00643-2"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.3390\/plants14111621"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.1080\/09583150701309535"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1007\/s40009-022-01190-y"},{"key":"e_1_3_4_35_2","doi-asserted-by":"publisher","DOI":"10.1007\/s40009-024-01550-w"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11756-025-01969-6"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1080\/07060660609507322"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms8081166"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.14130"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/msphere.00294-24"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.12469"},{"key":"e_1_3_4_42_2","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.01706"},{"key":"e_1_3_4_43_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2180-13-111"},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1099\/ijsem.0.005424"},{"key":"e_1_3_4_45_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.149.1.381-383.1982"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1128\/aem.02405-21"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.14395"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-822919-4.00016-8"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1002\/9781118297674.ch31"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.48311\/jcp.2020.1488"},{"key":"e_1_3_4_51_2","doi-asserted-by":"publisher","DOI":"10.1007\/s42161-019-00461-w"},{"key":"e_1_3_4_52_2","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.970382"},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.micpath.2019.03.006"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1002\/mbo3.1202"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.3390\/applmicrobiol3030076"},{"key":"e_1_3_4_56_2","unstructured":"Dagher F. 2021. D\u00e9veloppement de pesticides biologiques actifs contre des bact\u00e9ries phytopathog\u00e8nes. Universit\u00e9 du Qu\u00e9bec Institut national de la recherche scientifique (INRS)"},{"key":"e_1_3_4_57_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6968.1999.tb13383.x"},{"key":"e_1_3_4_58_2","doi-asserted-by":"publisher","DOI":"10.1128\/aem.53.5.949-954.1987"},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.1128\/jmbe.v12i1.249"},{"key":"e_1_3_4_60_2","doi-asserted-by":"publisher","DOI":"10.1002\/pb.20054"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.3389\/fspas.2021.735834"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.75.5.592-603.1958"},{"key":"e_1_3_4_63_2","doi-asserted-by":"publisher","DOI":"10.1034\/j.1399-3054.2003.00086.x"},{"key":"e_1_3_4_64_2","doi-asserted-by":"publisher","DOI":"10.21769\/BioProtoc.3230"},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1104\/pp.26.1.192"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.3389\/fchem.2018.00265"},{"key":"e_1_3_4_67_2","doi-asserted-by":"publisher","DOI":"10.1099\/ijs.0.044875-0"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.2135\/cropsci1973.0011183X001300060013x"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.1186\/s41938-019-0152-6"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1080\/03235408.2021.1895477"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-03-20-0072-R"},{"key":"e_1_3_4_72_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btu170"},{"key":"e_1_3_4_73_2","doi-asserted-by":"publisher","DOI":"10.1089\/cmb.2012.0021"},{"key":"e_1_3_4_74_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btv351"},{"key":"e_1_3_4_75_2","doi-asserted-by":"publisher","DOI":"10.1099\/mgen.0.000685"},{"key":"e_1_3_4_76_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10482-017-0844-4"},{"key":"e_1_3_4_77_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkab902"},{"key":"e_1_3_4_78_2","doi-asserted-by":"publisher","DOI":"10.1099\/ijsem.0.002516"},{"key":"e_1_3_4_79_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-07641-9"},{"key":"e_1_3_4_80_2","doi-asserted-by":"publisher","DOI":"10.1099\/ijs.0.059774-0"},{"key":"e_1_3_4_81_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molp.2020.06.009"},{"key":"e_1_3_4_82_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btv421"},{"key":"e_1_3_4_83_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msu300"},{"key":"e_1_3_4_84_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv487"},{"key":"e_1_3_4_85_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkt1226"}],"container-title":["Applied and Environmental Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/aem.01087-26","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/aem.01087-26","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T13:03:16Z","timestamp":1790168596000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/aem.01087-26"}},"subtitle":[],"editor":[{"given":"David A.","family":"Baltrus","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,9,23]]},"references-count":84,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2026,9,23]]}},"alternative-id":["10.1128\/aem.01087-26"],"URL":"https:\/\/doi.org\/10.1128\/aem.01087-26","relation":{},"ISSN":["0099-2240","1098-5336"],"issn-type":[{"value":"0099-2240","type":"print"},{"value":"1098-5336","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,23]]},"assertion":[{"value":"2026-05-29","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-07-31","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-02","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e01087-26"}}