{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T08:05:32Z","timestamp":1783929932611,"version":"3.55.0"},"reference-count":40,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T00:00:00Z","timestamp":1783900800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T00:00:00Z","timestamp":1783900800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Biotechnology Journal"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    <jats:styled-content style=\"fixed-case\">\n                      <jats:italic>Salmonella enterica<\/jats:italic>\n                    <\/jats:styled-content>\n                    serovars (\n                    <jats:italic>Salmonella<\/jats:italic>\n                    ) are common causes of bacterial gastroenteritis (salmonellosis) often associated with the consumption of poultry products. The control of\n                    <jats:italic>Salmonella<\/jats:italic>\n                    in broiler chickens is difficult because colonized birds may carry this pathogen undetected into the slaughterhouse and cause meat contamination. Poultry vaccines can mitigate colonization, and one promising production method is via plants. Iron is an essential nutrient for\n                    <jats:italic>Salmonella;<\/jats:italic>\n                    therefore, our goal was to exploit iron uptake systems as vaccine targets that could starve this pathogen of iron and thus prevent it from colonizing chickens. One challenge with this approach is that\n                    <jats:italic>Salmonella<\/jats:italic>\n                    possesses several iron acquisition proteins that are redundant in function. Therefore, we created nanoparticle\u2010based plant\u2010produced vaccine candidates against four different\n                    <jats:italic>Salmonella<\/jats:italic>\n                    iron acquisition proteins to create a multivalent vaccine that may be more effective than targeting a single protein. Extracellular antigenic peptides from each of these proteins were fused in tandem to the N\u2010terminus of the self\u2010assembling\n                    <jats:italic>Brucella<\/jats:italic>\n                    spp. lumazine synthase. These fusion constructs were then expressed in\n                    <jats:italic>Nicotiana benthamiana<\/jats:italic>\n                    plants. The resulting recombinant proteins were extracted, purified and characterized. The vaccine candidates administered individually or in combination elicited specific antibodies in mice and bound to the surface of\n                    <jats:italic>Salmonella,<\/jats:italic>\n                    indicating their potential in preventing\n                    <jats:italic>Salmonella<\/jats:italic>\n                    colonization in poultry.\n                  <\/jats:p>","DOI":"10.1111\/pbi.70717","type":"journal-article","created":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T07:07:13Z","timestamp":1783926433000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Design and Immunogenicity of a Nanoparticle Combination Vaccine for\n                    <i>Salmonella<\/i>\n                    in Poultry"],"prefix":"10.1111","author":[{"given":"Shabnam","family":"Shamriz","sequence":"first","affiliation":[{"name":"University of Western Ontario  London Ontario Canada"},{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angelo","family":"Kaldis","sequence":"additional","affiliation":[{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carly A.","family":"Charron","sequence":"additional","affiliation":[{"name":"University of Western Ontario  London Ontario Canada"},{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordan T.","family":"VanderBurgt","sequence":"additional","affiliation":[{"name":"University of Western Ontario  London Ontario Canada"},{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher P.","family":"Garnham","sequence":"additional","affiliation":[{"name":"University of Western Ontario  London Ontario Canada"},{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moussa S.","family":"Diarra","sequence":"additional","affiliation":[{"name":"Guelph Research and Development Centre AAFC  Guelph Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3536-0332","authenticated-orcid":false,"given":"Rima","family":"Menassa","sequence":"additional","affiliation":[{"name":"University of Western Ontario  London Ontario Canada"},{"name":"London Research and Development Centre Agriculture and Agri\u2010Food Canada (AAFC)  London Ontario Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,7,13]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2015.01170","article-title":"Expression of the Multimeric and Highly Immunogenic Brucella spp. Lumazine Synthase Fused to Bovine Rotavirus VP8d as a Scaffold for Antigen Production in Tobacco Chloroplasts","volume":"6","author":"Alfano E. F.","year":"2015","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_9_3_1","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1016\/S0021-9258(19)86223-3","article-title":"Riboflavin Synthases of \n                     Bacillus subtilis\n                  . Purification and Properties","volume":"255","author":"Bacher A.","year":"1980","journal-title":"Journal of Biological Chemistry"},{"key":"e_1_2_9_4_1","doi-asserted-by":"crossref","first-page":"1446","DOI":"10.1128\/JB.180.6.1446-1453.1998","article-title":"IroN, a Novel Outer Membrane Siderophore Receptor Characteristic of \n                     Salmonella enterica","volume":"180","author":"Baumler A. J.","year":"1998","journal-title":"Journal of Bacteriology"},{"key":"e_1_2_9_5_1","doi-asserted-by":"crossref","first-page":"2594","DOI":"10.1038\/sj.emboj.7601693","article-title":"Structure of Colicin I Receptor Bound to the R\u2010Domain of Colicin Ia: Implications for Protein Import","volume":"26","author":"Buchanan S. K.","year":"2007","journal-title":"EMBO Journal"},{"key":"e_1_2_9_6_1","doi-asserted-by":"crossref","unstructured":"Charron C. A. A.Kaldis S.Shamriz M. S.Diarra C. P.Garnham andR.Menassa.2026.\u201cSimultaneous Modification ofThermotoga maritimaEncapsulin Subunits to Produce Multivalent Nanoparticle Vaccines for Non\u2010TyphoidalSalmonella enterica.\u201dThe FEBS Journal ahead of print April 28.https:\/\/doi.org\/10.1111\/febs.70561.","DOI":"10.1111\/febs.70561"},{"key":"e_1_2_9_7_1","doi-asserted-by":"crossref","first-page":"1908","DOI":"10.1111\/febs.70340","article-title":"Plant\u2010Produced Encapsulin Displays Non\u2010Typhoidal \n                     Salmonella enterica\n                   Antigens and Assembles Into Mosaic Nanoparticles","volume":"293","author":"Charron C. A.","year":"2026","journal-title":"FEBS Journal"},{"key":"e_1_2_9_8_1","doi-asserted-by":"crossref","first-page":"548","DOI":"10.4315\/0362-028X.JFP-18-371","article-title":"Growth of \n                     Salmonella enterica\n                   Serovars Typhimurium and Enteritidis in Iron\u2010Poor Media and in Meat: Role of Catecholate and Hydroxamate Siderophore Transporters","volume":"82","author":"Chekabab S. M.","year":"2019","journal-title":"Journal of Food Protection"},{"key":"e_1_2_9_9_1","doi-asserted-by":"crossref","DOI":"10.1186\/1741-7007-7-48","article-title":"Induction of Protein Body Formation in Plant Leaves by Elastin\u2010Like Polypeptide Fusions","volume":"7","author":"Conley A. J.","year":"2009","journal-title":"BMC Biology"},{"key":"e_1_2_9_10_1","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1002\/prot.20635","article-title":"Multiple Display of a Protein Domain on a Bacterial Polymeric Scaffold","volume":"61","author":"Craig P. 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J.","year":"2010","journal-title":"Plant Physiology"},{"key":"e_1_2_9_18_1","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.csbj.2015.11.001","article-title":"Self\u2010Assembling Protein Nanoparticles in the Design of Vaccines","volume":"14","author":"Lopez\u2010Sagaseta J.","year":"2016","journal-title":"Computational and Structural Biotechnology Journal"},{"key":"e_1_2_9_19_1","first-page":"269","volume-title":"Methods in Molecular Biology","author":"Marillonnet S.","year":"2015"},{"key":"e_1_2_9_20_1","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1038\/s42003-025-08846-7","article-title":"Structural Insights Into Cir\u2010Mediated Killing by the Antimicrobial Protein Microcin V","volume":"8","author":"Maurakis S. A.","year":"2025","journal-title":"Communications Biology"},{"key":"e_1_2_9_21_1","doi-asserted-by":"crossref","DOI":"10.3390\/vaccines10091447","article-title":"Self\u2010Assembling Protein Nanoparticles in the Design of Vaccines: 2022 Update","volume":"10","author":"Morales\u2010Hernandez S.","year":"2022","journal-title":"Vaccine"},{"key":"e_1_2_9_22_1","first-page":"215","article-title":"Prevalence, Risks and Antibiotic Resistance of Salmonella in Poultry Production Chain","volume":"1","author":"Mouttotou N.","year":"2017","journal-title":"Current Topics in Salmonella and Salmonellosis"},{"key":"e_1_2_9_23_1","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1007\/s10534-009-9217-4","article-title":"Salmochelin, the Long\u2010Overlooked Catecholate Siderophore of Salmonella","volume":"22","author":"Muller S. I.","year":"2009","journal-title":"Biometals"},{"key":"e_1_2_9_24_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1472-6750-14-59","article-title":"Production and Characterization of In Planta Transiently Produced Polygalacturanase From Aspergillus Nigerand Its Fusions With Hydrophobin or ELP Tags","volume":"14","author":"Pereira E. O.","year":"2014","journal-title":"BMC Biotechnology"},{"key":"e_1_2_9_25_1","doi-asserted-by":"crossref","first-page":"227","DOI":"10.7774\/cevr.2014.3.2.227","article-title":"Lumazine Synthase Protein Cage Nanoparticles as Antigen Delivery Nanoplatforms for Dendritic Cell\u2010Based Vaccine Development","volume":"3","author":"Ra J. 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P.","year":"2010","journal-title":"Plant Biotechnology Journal"},{"key":"e_1_2_9_29_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s44383-025-00014-4","article-title":"Potential of Plant Chloroplast\u2010Based Recombinant Expression Systems to Express Bacterial Membrane Proteins as Vaccine Candidates for Salmonella in Poultry","volume":"2","author":"Shamriz S.","year":"2026","journal-title":"NPJ Science of Plants"},{"key":"e_1_2_9_30_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2026.1761000","article-title":"Protein Nanoparticle\u2010Based Vaccine Candidate Produced in Nicotiana Benthamiana Against Non\u2010Typhoidal \n                     Salmonella enterica\n                   in Poultry","volume":"17","author":"Shamriz S.","year":"2026","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_9_31_1","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2023.1125253","article-title":"Self\u2010Assembled Nanoparticles: A New Platform for Revolutionizing Therapeutic Cancer Vaccines","volume":"14","author":"Shi T.","year":"2023","journal-title":"Frontiers in Immunology"},{"key":"e_1_2_9_32_1","doi-asserted-by":"crossref","first-page":"3070","DOI":"10.1093\/emboj\/cdf312","article-title":"A Viral Protein Suppresses RNA Silencing and Binds Silencing\u2010Generated, 21\u2010 to 25\u2010Nucleotide Double\u2010Stranded RNAs","volume":"21","author":"Silhavy D.","year":"2002","journal-title":"EMBO Journal"},{"key":"e_1_2_9_33_1","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.biotechadv.2016.02.007","article-title":"The Case for Plant\u2010Made Veterinary Immunotherapeutics","volume":"34","author":"Topp E.","year":"2016","journal-title":"Biotechnology Advances"},{"key":"e_1_2_9_34_1","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1016\/j.vaccine.2009.01.024","article-title":"Importance of Subunit Vaccine Antigen of Major Fli C Antigenic Site of \n                     Salmonella enteritidis\n                   II: A Challenge Trial","volume":"27","author":"Toyota\u2010Hanatani Y.","year":"2009","journal-title":"Vaccine"},{"key":"e_1_2_9_35_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2023.1044675","article-title":"Plant Production of a Virus\u2010Like Particle\u2010Based Vaccine Candidate Against Porcine Reproductive and Respiratory Syndrome","volume":"14","author":"VanderBurgt J. T.","year":"2023","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_9_36_1","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2023.1043109","article-title":"New\u2010Age Vaccine Adjuvants, Their Development, and Future Perspective","volume":"14","author":"Verma S. 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