{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T21:06:22Z","timestamp":1792011982066,"version":"4.4.0"},"reference-count":38,"publisher":"MDPI AG","issue":"24","license":[{"start":{"date-parts":[[2024,12,22]],"date-time":"2024-12-22T00:00:00Z","timestamp":1734825600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>An alkaline pH in soils reduces Fe availability, limiting Fe uptake, compromising plant growth, and showing chlorosis due to a decrease in chlorophyll content. To achieve proper Fe homeostasis, dicotyledonous plants activate a battery of strategies involving not only Fe absorption mechanisms, but also releasing phyto-siderophores and recruiting siderophore-producing bacterial strains. A screening for siderophore-producing bacterial isolates from the rhizosphere of Pinus pinea was carried out, resulting in two Pseudomonas strains, Z8.8 and Z10.4, with an outstanding in vitro potential to solubilize Fe, Mn, and Co. The delivery of each strain to 4-week-old iron-starved tomatoes reverted chlorosis, consistent with enhanced Fe contents up to 40%. Photosynthesis performance was improved, revealing different strategies. While Z8.8 increased energy absorption together with enhanced chlorophyll \u201ca\u201d content, followed by enhanced energy dissipation, Z10.4 lowered pigment contents, indicating a better use of absorbed energy, leading to a better survival rate. The systemic reprogramming induced by both strains reveals a lower expression of Fe uptake-related genes, suggesting that both strains have activated plant metabolism to accelerate Fe absorption faster than controls, consistent with increased Fe content in leaves (47% by Z8.8 and 42% by Z10.4), with the difference probably due to the ability of Z8.8 to produce auxins affecting root structure. In view of these results, both strains are effective candidates to develop biofertilizers.<\/jats:p>","DOI":"10.3390\/plants13243585","type":"journal-article","created":{"date-parts":[[2024,12,23]],"date-time":"2024-12-23T08:16:07Z","timestamp":1734941767000},"page":"3585","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Iron Deficiency in Tomatoes Reversed by Pseudomonas Strains: A Synergistic Role of Siderophores and Plant Gene Activation"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9724-6792","authenticated-orcid":false,"given":"Bel\u00e9n","family":"Montero-Palmero","sequence":"first","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0086-957X","authenticated-orcid":false,"given":"Jose A.","family":"Lucas","sequence":"additional","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Blanca","family":"Montalb\u00e1n","sequence":"additional","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4081-5226","authenticated-orcid":false,"given":"Ana","family":"Garc\u00eda-Villaraco","sequence":"additional","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5230-6798","authenticated-orcid":false,"given":"Javier","family":"Gutierrez-Ma\u00f1ero","sequence":"additional","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0280-5198","authenticated-orcid":false,"given":"Beatriz","family":"Ramos-Solano","sequence":"additional","affiliation":[{"name":"Plant Physiology, Pharmaceutical and Health Sciences Department, Faculty of Pharmacy, San Pablo\u2014CEU Universities, 28668 Boadilla del Monte, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Li, M., Watanabe, S., Gao, F., and Dubos, C. (2023). Iron Nutrition in Plants: Towards a New Paradigm?. Plants, 12.","DOI":"10.3390\/plants12020384"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.tplants.2014.07.005","article-title":"Iron nutrition, biomass production, and plant product quality","volume":"20","author":"Briat","year":"2015","journal-title":"Trends Plant Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Montejano-Ram\u00edrez, V., and Valencia-Cantero, E. (2023). Cross-Talk between iron deficiency response and defense establishment in plants. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24076236"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Moln\u00e1r, Z., Solomon, W., Mutum, L., and Janda, T. (2023). Understanding the mechanisms of Fe deficiency in the rhizosphere to promote plant resilience. Plants, 12.","DOI":"10.3390\/plants12101945"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Timofeeva, A.M., Galyamova, M.R., and Sedykh, S.E. (2022). Bacterial siderophores: Classification, biosynthesis, perspectives of use in agriculture. Plants, 11.","DOI":"10.3390\/plants11223065"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Zhang, X., Zhang, D., Sun, W., and Wang, T. (2019). The adaptive mechanism of plants to iron deficiency via iron uptake, transport, and homeostasis. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20102424"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1007\/s003740050258","article-title":"Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.)","volume":"24","author":"Banerjee","year":"1997","journal-title":"Biol. Fert. Soils"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1139\/w97-141","article-title":"Antifungal activity of chitinolytic bacteria isolated from airtight stored cereal grain","volume":"44","year":"1998","journal-title":"Can. J. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Ilangumaran, G., and Smith, D.L. (2017). Plant growth promoting rhizobacteria in amelioration of salinity stress: A systems biology perspective. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.01768"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Lucas, J.A., Garcia-Villaraco, A., Montero-Palmero, M.B., Montalban, B., Ramos-Solano, B., and Gutierrez-Ma\u00f1ero, F.J. (2023). Physiological and genetic modifications induced by plant-growth-promoting rhizobacteria (PGPR) in tomato plants under moderate water stress. Biology, 12.","DOI":"10.3390\/biology12070901"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zhang, S., Deng, Z., Borham, A., Ma, Y., Wang, Y., Hu, J., Wang, J., and Bohu, T. (2023). Significance of soil siderophore-producing bacteria in evaluation and elevation of crop yield. Horticulturae, 9.","DOI":"10.3390\/horticulturae9030370"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.plaphy.2011.01.026","article-title":"Towards a knowledge-based correction of iron chlorosis","volume":"49","year":"2011","journal-title":"Plant Physiol. Biochem."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Orozco-Mosqueda, M.D.C., Flores, A., Rojas-S\u00e1nchez, B., Urtis-Flores, C.A., Morales-Cede\u00f1o, L.R., Valencia-Marin, M.F., Ch\u00e1vez-Avila, S., Rojas-Solis, D., and Santoyo, G. (2021). Plant growth-promoting bacteria as bioinoculants: Attributes and challenges for sustainable crop improvement. Agronomy, 11.","DOI":"10.3390\/agronomy11061167"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s11104-010-0371-9","article-title":"Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L","volume":"334","author":"Lucas","year":"2010","journal-title":"Plant Soil"},{"key":"ref_15","first-page":"e39973","article-title":"Peribacillus aracenensis sp.nov., a plant growth promoting bacteria for agriculture in water-scarce conditions isolated from Pinus pinaster rhizosphere","volume":"10","author":"Lucas","year":"2024","journal-title":"Helyon"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"773","DOI":"10.4236\/ajps.2020.116055","article-title":"Isolation, screening and molecular characterization of multifunctional plant growth promoting rhizobacteria for a sustainable agriculture","volume":"11","author":"Oo","year":"2020","journal-title":"Am. J. Plant Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.micres.2015.01.014","article-title":"Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting and disease suppressing effects on ginger","volume":"173","author":"Dinesh","year":"2015","journal-title":"Microbiol. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1111\/j.1467-7652.2008.00331.x","article-title":"Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria","volume":"6","author":"Barriuso","year":"2008","journal-title":"Plant Biotechnol. J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s42398-018-0005-3","article-title":"Modified chrome azurol S method for detection and estimation of siderophores having affinity for metal ions other than iron","volume":"1","author":"Patel","year":"2018","journal-title":"Environ. Sustain."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Park, S., Kim, A., Hong, Y., Shin, J., and Joo, S. (2021). A highly efficient auxin-producing bacterial strain and its effect on plant growth. J. Genet. Eng.Biotechnol., 19.","DOI":"10.1186\/s43141-021-00252-w"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1007\/s00374-015-1039-7","article-title":"Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants","volume":"51","author":"Bindraban","year":"2015","journal-title":"Biol. Fert. Soils"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1016\/j.bbamcr.2012.05.016","article-title":"The zinc homeostasis network of land plants","volume":"1823","author":"Sinclair","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Reed, L., and Glick, B.R. (2023). The recent use of plant-growth-promoting bacteria to promote the growth of agricultural food crops. Agriculture, 13.","DOI":"10.3390\/agriculture13051089"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1007\/s10482-013-9954-9","article-title":"Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture","volume":"104","author":"Radzki","year":"2013","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/s10725-020-00598-0","article-title":"The plant growth promoting bacteria Gluconacetobacter diazotrophicus and Azospirillum brasilense contribute to the iron nutrition of strawberry plants through siderophores production","volume":"91","author":"Lovaisa","year":"2020","journal-title":"J. Plant Growth Regul."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2141","DOI":"10.1080\/01904167.2018.1482910","article-title":"Effect of plant growth promoting rhizobacteria on Fe acquisition in peach (Prunus Persica L.) under calcareous soil conditions","volume":"41","author":"Arikan","year":"2018","journal-title":"J. Plant Nutr."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e312","DOI":"10.1002\/fes3.312","article-title":"Improving the yield potential in maize by constructing the ideal plant type and optimizing the maize canopy structure","volume":"10","author":"Li","year":"2021","journal-title":"Food Energy Secur."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1093\/pcp\/pcaa155","article-title":"The mechanism of non-photochemical quenching in plants: Localization and driving forces","volume":"62","author":"Ruban","year":"2021","journal-title":"Plant Cell Physiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"16225","DOI":"10.1038\/nplants.2016.225","article-title":"The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching","volume":"3","author":"Sacharz","year":"2017","journal-title":"Nat. Plants"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.tplants.2018.10.003","article-title":"Rapid responses to abiotic stress: Priming the landscape for the signal transduction network","volume":"24","author":"Kollist","year":"2019","journal-title":"Trends Plant Sci."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Kaleh, A.M., Singh, P., Chua, K.O., and Harikrishna, J.A. (2024). Modulation of plant transcription factors and priming of stress tolerance by plant growth-promoting bacteria: A systematic review. Ann. Bot., mcae166.","DOI":"10.1093\/aob\/mcae166"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Garcia-Villaraco, A., Ramos-Solano, B., Guti\u00e9rrez-Ma\u00f1ero, F.J., and Lucas, J.A. (2024). Deciphering the Structural and Functional Diversity of Rhizobacteria from Stone Pine Inoculated with Plant Growth Promoting Rhizobacteria (PGPR) before and after Transplanted into Degraded Agricultural Soil. Soil Syst., 8.","DOI":"10.3390\/soilsystems8020039"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1016\/S0038-0717(98)00006-6","article-title":"Role of maize root exudates in the production of auxins by Pseudomonas fluorescens M.3.1","volume":"30","author":"Benizri","year":"1998","journal-title":"Soil Biol. Biochem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/BF02178617","article-title":"The determination of soil chitinase activity: Conditions for assay and ecological studies","volume":"75","author":"Godoy","year":"1983","journal-title":"Plant Soil"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/0003-2697(87)90612-9","article-title":"Universal chemical assay for the detection and determination of siderophores","volume":"160","author":"Schwyn","year":"1987","journal-title":"Anal. Biochem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3233","DOI":"10.1128\/aem.63.8.3233-3241.1997","article-title":"Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients","volume":"63","author":"Heuer","year":"1997","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/S0005-2728(89)80347-0","article-title":"Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy","volume":"975","author":"Porra","year":"1989","journal-title":"Biochim. Et Biophys. Acta (BBA)- Bioenerg."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/24\/3585\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:58:00Z","timestamp":1760115480000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/24\/3585"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,22]]},"references-count":38,"journal-issue":{"issue":"24","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["plants13243585"],"URL":"https:\/\/doi.org\/10.3390\/plants13243585","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,22]]}}}