{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T22:54:38Z","timestamp":1788476078046,"version":"build-2803163510"},"reference-count":44,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T00:00:00Z","timestamp":1661126400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p><jats:italic>Salmonella<\/jats:italic> capacity to colonize different environments depends on its ability to respond efficiently to fluctuations in micronutrient availability. Among micronutrients, Zn, besides playing an essential role in bacterial physiology, is a key element whose concentration can influence bacterial survival in a particular niche. Plant colonization by <jats:italic>Salmonella enterica<\/jats:italic> was described for several years, and some molecular determinants involved in this host-pathogen interaction have started to be characterized. However, it is still unclear if Zn plays a role in the outcome of this interaction, as well established for animal hosts that employ nutritional immunity strategies to counteract pathogens infections. In this study, we have investigated the involvement of <jats:italic>Salmonella<\/jats:italic> Typhimurium main effectors of zinc homeostasis in plant colonization, using <jats:italic>Arabidopsis thaliana<\/jats:italic> as a model host. The results show that to colonize plant tissues, <jats:italic>Salmonella<\/jats:italic> takes advantage of its ability to export excess metal through the efflux pumps ZntA and ZitB. In fact, the deletion of these Zn\/Cd detoxification systems can affect bacterial persistence in the shoots, depending on metal availability in the plant tissues. The importance of <jats:italic>Salmonella<\/jats:italic> ability to export excess metal was enhanced in the colonization of plants grown in high Zn conditions. On the contrary, the bacterial disadvantage related to Zn detoxification impairment can be abrogated if the plant cannot efficiently translocate Zn to the shoots. Overall, our work highlights the role of Zn in <jats:italic>Salmonella<\/jats:italic>-plant interaction and suggests that modulation of plant metal content through biofortification may be an efficient strategy to control pathogen colonization.<\/jats:p>","DOI":"10.3389\/fmicb.2022.975725","type":"journal-article","created":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T08:42:55Z","timestamp":1661157775000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Impairment of the Zn\/Cd detoxification systems affects the ability of Salmonella to colonize Arabidopsis thaliana"],"prefix":"10.3389","volume":"13","author":[{"given":"Sabina","family":"Visconti","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Luisa","family":"Astolfi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Battistoni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Serena","family":"Ammendola","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,8,22]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1007\/s10534-014-9763-2","article-title":"Deregulation of transition metals homeostasis is a key feature of cadmium toxicity in salmonella","volume":"27","author":"Ammendola","year":"2014","journal-title":"Biometals"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1039\/C6MT00108D","article-title":"Zinc is required to ensure the expression of flagella and the ability to form biofilms in Salmonella enterica sv Typhimurium","volume":"8","author":"Ammendola","year":"2016","journal-title":"Metallomics"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"5867","DOI":"10.1128\/IAI.00559-07","article-title":"High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica","volume":"75","author":"Ammendola","year":"2007","journal-title":"Infect. 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Physiol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1146\/ANNUREV-PHYTO-080516-035544","article-title":"Evolution of hormone signaling networks in plant defense","volume":"55","author":"Berens","year":"2017","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/J.PBI.2017.04.004","article-title":"Transcriptional events defining plant immune responses","volume":"38","author":"Birkenbihl","year":"2017","journal-title":"Curr. Opin. 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Plant Sci."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"108","DOI":"10.3389\/fcimb.2013.00108","article-title":"Competition for zinc binding in the host-pathogen interaction","volume":"3","author":"Cerasi","year":"2013","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1038\/NRMICRO.2017.15","article-title":"Metal homeostasis and resistance in bacteria","volume":"15","author":"Chandrangsu","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"2668","DOI":"10.3389\/fmicb.2017.02668","article-title":"Production of the plant hormone auxin by salmonella and its role in the interactions with plants and animals","volume":"8","author":"Cox","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"6640","DOI":"10.1073\/pnas.120163297","article-title":"One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products","volume":"97","author":"Datsenko","year":"2000","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"18954","DOI":"10.1074\/JBC.R115.647099","article-title":"The role of copper and zinc toxicity in innate immune defense against bacterial pathogens","volume":"290","author":"Djoko","year":"2015","journal-title":"J. Biol. Chem."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1093\/jxb\/erab400","article-title":"Arabidopsis thaliana Zn2+\u2212efflux ATPases HMA2 and HMA4 are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina BMM","volume":"73","author":"Escudero","year":"2022","journal-title":"J. Exp. 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Microbiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1105\/tpc.020487","article-title":"P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in arabidopsis","volume":"16","author":"Hussain","year":"2004","journal-title":"Plant Cell"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1901","DOI":"10.1096\/FJ.201500061","article-title":"Salmonella employs multiple mechanisms to subvert the TLR-inducible zinc-mediated antimicrobial response of human macrophages","volume":"30","author":"Kapetanovic","year":"2016","journal-title":"FASEB J."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"6076","DOI":"10.1128\/AEM.01084-09","article-title":"Internalization of salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata","volume":"75","author":"Kroupitski","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.chom.2012.01.017","article-title":"Zinc sequestration by the neutrophil protein calprotectin enhances salmonella growth in the inflamed gut","volume":"11","author":"Liu","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e0177321","DOI":"10.1128\/SPECTRUM.01773-21","article-title":"The role of ZntA in Klebsiella pneumoniae zinc homeostasis","volume":"10","author":"Maunders","year":"2022","journal-title":"Microbiol. 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Biochem."},{"key":"ref34","doi-asserted-by":"crossref","DOI":"10.1038\/s41579-022-00745-6","article-title":"Nutritional immunity: the battle for nutrient metals at the host-pathogen interface","volume-title":"Nat. Rev. Microbiol.","author":"Murdoch","year":"2022"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1094\/MPMI-07-14-0221-R","article-title":"Zinc detoxification is required for full virulence and modification of the host leaf ionome by Xylella fastidiosa","volume":"28","author":"Navarrete","year":"2015","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"11","DOI":"10.4049\/jimmunol.1800325","article-title":"Innate nutritional immunity","volume":"201","author":"N\u00fa\u00f1ez","year":"2018","journal-title":"J. Immunol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/s12870-019-2232-x","article-title":"Novel molecular components involved in callose-mediated Arabidopsis defense against salmonella enterica and Escherichia coli O157:H7","volume":"20","author":"Oblessuc","year":"2020","journal-title":"BMC Plant Biol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"3421","DOI":"10.1016\/j.vaccine.2008.04.036","article-title":"Attenuated salmonella enterica serovar Typhimurium lacking the ZnuABC transporter confers immune-based protection against challenge infections in mice","volume":"26","author":"Pasquali","year":"2008","journal-title":"Vaccine"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"e2279","DOI":"10.1371\/journal.pone.0002279","article-title":"The dark side of the salad: salmonella typhimurium overcomes the innate immune response of arabidopsis thaliana and shows an endopathogenic lifestyle","volume":"3","author":"Schikora","year":"2008","journal-title":"PLoS One"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/J.COI.2019.04.002","article-title":"Metals as phagocyte antimicrobial effectors","volume":"60","author":"Sheldon","year":"2019","journal-title":"Curr. 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Biochem."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"103833","DOI":"10.1016\/j.fm.2021.103833","article-title":"Mechanisms adopted by salmonella to colonize plant hosts","volume":"99","author":"Zarkani","year":"2021","journal-title":"Food Microbiol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"2494","DOI":"10.1128\/AEM.03704-12","article-title":"Colonization and internalization of salmonella enterica in tomato plants","volume":"79","author":"Zheng","year":"2013","journal-title":"Appl. Environ. 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