{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T04:41:01Z","timestamp":1760244061107,"version":"build-2065373602"},"reference-count":51,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2022,11,7]],"date-time":"2022-11-07T00:00:00Z","timestamp":1667779200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"National Funds from FCT\u2014Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"],"award-info":[{"award-number":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Portuguese Mass Spectrometry Network","award":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"],"award-info":[{"award-number":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"]}]},{"name":"International Ph.D. Program in Biotechnology, Portugal, for providing Ph.D. scholarship","award":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"],"award-info":[{"award-number":["UIDB\/50016\/2020","PTDC\/AGR-PRO\/3972\/2014","ROTEIRO\/0028\/2013","LISBOA-01-0145-FEDER-022125","NORTE-08-5369-FSE-000007"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Elevated atmospheric CO2 (eCO2) and iron (Fe) availability are important factors affecting plant growth that may impact the proteomic profile of crop plants. In this study, soybean plants treated under Fe-limited (0.5 mM) and Fe-sufficient (20 mM) conditions were grown at ambient (400 \u03bcmol mol\u22121) and eCO2 (800 \u03bcmol mol\u22121) in hydroponic solutions. Elevated CO2 increased biomass from 2.14 to 3.14 g plant\u22121 and from 1.18 to 2.91 g plant\u22121 under Fe-sufficient and Fe-limited conditions, respectively, but did not affect leaf photosynthesis. Sugar concentration increased from 10.92 to 26.17 \u03bcmol g FW\u22121 in roots of Fe-sufficient plants and from 8.75 to 19.89 \u03bcmol g FW\u22121 of Fe-limited plants after exposure to eCO2. In leaves, sugar concentration increased from 33.62 to 52.22 \u03bcmol g FW\u22121 and from 34.80 to 46.70 \u03bcmol g FW\u22121 in Fe-sufficient and Fe-limited conditions, respectively, under eCO2. However, Fe-limitation decreases photosynthesis and biomass. Pathway enrichment analysis showed that cell wall organization, glutathione metabolism, photosynthesis, stress-related proteins, and biosynthesis of secondary compounds changed in root tissues to cope with Fe-stress. Moreover, under eCO2, at sufficient or limited Fe supply, it was shown an increase in the abundance of proteins involved in glycolysis, starch and sucrose metabolism, biosynthesis of plant hormones gibberellins, and decreased levels of protein biosynthesis. Our results revealed that proteins and metabolic pathways related to Fe-limitation changed the effects of eCO2 and negatively impacted soybean production.<\/jats:p>","DOI":"10.3390\/ijms232113632","type":"journal-article","created":{"date-parts":[[2022,11,8]],"date-time":"2022-11-08T10:53:06Z","timestamp":1667904786000},"page":"13632","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Effect of the Interaction between Elevated Carbon Dioxide and Iron Limitation on Proteomic Profiling of Soybean"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7241-8719","authenticated-orcid":false,"given":"Jos\u00e9 C.","family":"Soares","sequence":"first","affiliation":[{"name":"CBQF\u2014Centro de Biotecnologia e Qu\u00edmica Fina\u2014Laborat\u00f3rio Associado, Escola Superior de Biotecnologia, Universidade Cat\u00f3lica Portuguesa, Rua Diogo Botelho 1327, 4169-005 Porto, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6362-8255","authenticated-orcid":false,"given":"Hugo","family":"Os\u00f3rio","sequence":"additional","affiliation":[{"name":"i3S\u2014Instituto de Investiga\u00e7\u00e3o e Inova\u00e7\u00e3o em Sa\u00fade, Universidade do Porto, 4200-135 Porto, Portugal"},{"name":"Ipatimup\u2014Institute of Molecular Pathology and Immunology of the University of Porto, University of Porto, 4200-135 Porto, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manuela","family":"Pintado","sequence":"additional","affiliation":[{"name":"CBQF\u2014Centro de Biotecnologia e Qu\u00edmica Fina\u2014Laborat\u00f3rio Associado, Escola Superior de Biotecnologia, Universidade Cat\u00f3lica Portuguesa, Rua Diogo Botelho 1327, 4169-005 Porto, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marta W.","family":"Vasconcelos","sequence":"additional","affiliation":[{"name":"CBQF\u2014Centro de Biotecnologia e Qu\u00edmica Fina\u2014Laborat\u00f3rio Associado, Escola Superior de Biotecnologia, Universidade Cat\u00f3lica Portuguesa, Rua Diogo Botelho 1327, 4169-005 Porto, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1175\/JCLI3746.1","article-title":"Climate Change Projections for the Twenty-First Century and Climate Change Commitment in the CCSM3","volume":"19","author":"Meehl","year":"2006","journal-title":"J. Clim."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2446","DOI":"10.1021\/acs.jproteome.8b00951","article-title":"Proteomic Profiling for Metabolic Pathways Involved in Interactive Effects of Elevated Carbon Dioxide and Nitrogen on Leaf Growth in a Perennial Grass Species","volume":"18","author":"Yu","year":"2019","journal-title":"J. Proteome Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.pld.2019.09.004","article-title":"Impacts of CO2 elevation on the physiology and seed quality of soybean","volume":"42","author":"Zheng","year":"2020","journal-title":"Plant Divers."},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1104\/pp.109.136721","article-title":"Elevated Carbon Dioxide Improves Plant Iron Nutrition through Enhancing the Iron-Deficiency-Induced Responses under Iron-Limited Conditions in Tomato","volume":"150","author":"Jin","year":"2009","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2188","DOI":"10.1016\/j.foodchem.2012.12.025","article-title":"Mild Fe-deficiency improves biomass production and quality of hydroponic-cultivated spinach plants (Spinacia oleracea L.)","volume":"138","author":"Jin","year":"2013","journal-title":"Food Chem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1038\/88143","article-title":"Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes","volume":"19","author":"Takahashi","year":"2001","journal-title":"Nat. Biotechnol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nature13179","article-title":"Increasing CO2 threatens human nutrition","volume":"510","author":"Myers","year":"2014","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"85","DOI":"10.21273\/JASHS.141.1.85","article-title":"Leaf protein abundance associated with improved drought tolerance by elevated carbon dioxide in creeping bentgrass","volume":"141","author":"Burgess","year":"2016","journal-title":"J. Am. Soc. Hortic. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.fcr.2014.05.003","article-title":"Root protein metabolism in association with improved root growth and drought tolerance by elevated carbon dioxide in creeping bentgrass","volume":"165","author":"Burgess","year":"2014","journal-title":"Field Crops Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.3389\/fpls.2017.01506","article-title":"Metabolic pathways involved in carbon dioxide enhanced heat tolerance in bermudagrass","volume":"8","author":"Yu","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/S0065-2113(08)00404-5","article-title":"Chapter 4 Iron Dynamics in the Rhizosphere: Consequences for Plant Health and Nutrition","volume":"Volume 99","author":"Robin","year":"2008","journal-title":"Advances in Agronomy"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.2134\/jeq2006.0136","article-title":"Responses to Iron Limitation in Hordeum vulgare L. as Affected by the Atmospheric CO2 Concentration","volume":"37","author":"Haase","year":"2008","journal-title":"J. Environ. Qual."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2229-10-268","article-title":"Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots","volume":"10","author":"Donnini","year":"2010","journal-title":"BMC Plant Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.jprot.2016.03.024","article-title":"Long-term iron deficiency: Tracing changes in the proteome of different pea (Pisum sativum L.) cultivars","volume":"140","author":"Meisrimler","year":"2016","journal-title":"J. Proteom."},{"key":"ref_16","first-page":"254","article-title":"Iron deficiency in plants: An insight from proteomic approaches","volume":"4","author":"Grusak","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_17","first-page":"1","article-title":"Effects of Elevated Carbon Dioxide on Photosynthesis and Carbon Partitioning: A Perspective on Root Sugar Sensing and Hormonal Crosstalk","volume":"578","author":"Thompson","year":"2017","journal-title":"Front. Physiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1104\/pp.15.01598","article-title":"Increased Sucrose Accumulation Regulates Iron-Deficiency Responses by Promoting Auxin Signaling in Arabidopsis Plants","volume":"170","author":"Lin","year":"2016","journal-title":"Plant Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Chen, T., Zhang, L., Shang, H., Liu, S., Peng, J., Gong, W., Shi, Y., Zhang, S., Li, J., and Gong, J. (2016). iTRAQ-based quantitative proteomic analysis of cotton roots and leaves reveals pathways associated with salt stress. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0148487"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1104\/pp.106.086256","article-title":"The Effects of Elevated CO2 Concentration on Soybean Gene Expression. An Analysis of Growing and Mature Leaves","volume":"142","author":"Ainsworth","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1105\/tpc.111.092254","article-title":"Regulation of root greening by light and auxin\/cytokinin signaling in Arabidopsis","volume":"24","author":"Kobayashi","year":"2012","journal-title":"Plant Cell"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"6141","DOI":"10.1093\/jxb\/erz358","article-title":"Integrative analysis of hexaploid wheat roots identifies signature components during iron starvation","volume":"70","author":"Kaur","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_23","first-page":"53","article-title":"Effects of iron deficiency on photosynthesis and photosystem II function in soybean leaf","volume":"33","author":"Jiang","year":"2007","journal-title":"J. Plant Physiol. Mol. Biol."},{"key":"ref_24","first-page":"502","article-title":"Mineral nutrient signaling controls photosynthesis: Focus on iron deficiency-induced chlorosis","volume":"27","author":"Lacombe","year":"2021","journal-title":"Trends Plant Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/s11120-006-9092-6","article-title":"Proteomic profiles of thylakoid membranes and changes in response to iron deficiency","volume":"89","author":"Andaluz","year":"2006","journal-title":"Photosynth. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.3389\/fpls.2019.01463","article-title":"The Regulation of Plant Secondary Metabolism in Response to Abiotic Stress: Interactions Between Heat Shock and Elevated CO2","volume":"10","author":"Austen","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.4161\/psb.6.11.17613","article-title":"Influence of abiotic stress signals on secondary metabolites in plants","volume":"6","author":"Ramakrishna","year":"2011","journal-title":"Plant Signal. Behav."},{"key":"ref_28","first-page":"222","article-title":"Flavonoids: Biosynthesis, biological functions, and biotechnological applications","volume":"3","author":"Rius","year":"2012","journal-title":"Front. Plant Sci."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Ahmed, U., Rao, M.J., Qi, C., Xie, Q., Noushahi, H.A., Yaseen, M., Shi, X., and Zheng, B. (2021). Expression Profiling of Flavonoid Biosynthesis Genes and Secondary Metabolites Accumulation in Populus under Drought Stress. Molecules, 26.","DOI":"10.3390\/molecules26185546"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1104\/pp.110.169508","article-title":"iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis","volume":"155","author":"Lan","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Perkowska, I., Potrykus, M., Siwinska, J., Siudem, D., Lojkowska, E., and Ihnatowicz, A. (2021). Interplay between Coumarin Accumulation, Iron Deficiency and Plant Resistance to Dickeya spp.. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22126449"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/s41438-019-0172-0","article-title":"Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline\u2013alkali stress","volume":"6","author":"Jia","year":"2019","journal-title":"Hortic. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1800262","DOI":"10.1002\/pmic.201800262","article-title":"Physiological and proteomic evidence for the interactive effects of post-anthesis heat stress and elevated CO2 on wheat","volume":"18","author":"Zhang","year":"2018","journal-title":"Proteomics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"100182","DOI":"10.1016\/j.plgene.2019.100182","article-title":"Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS)","volume":"19","author":"Kapoor","year":"2019","journal-title":"Plant Gene"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1104\/pp.109.136630","article-title":"Physiological roles of glutathione S-transferases in soybean root nodules","volume":"150","author":"Dalton","year":"2009","journal-title":"Plant Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1007\/s13205-020-02312-3","article-title":"Glutathione S-transferase: A versatile protein family","volume":"10","author":"Vaish","year":"2020","journal-title":"3 Biotech."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2774","DOI":"10.1074\/mcp.M113.029991","article-title":"The metabolic status drives acclimation of iron deficiency responses in Chlamydomonas reinhardtii as revealed by proteomics based hierarchical clustering and reverse genetics","volume":"12","author":"Barth","year":"2013","journal-title":"Mol. Cell. Proteom."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1781","DOI":"10.1104\/pp.112.204842","article-title":"Action of gibberellins on growth and metabolism of Arabidopsis plants associated with high concentration of carbon dioxide","volume":"160","author":"Ribeiro","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1046\/j.0016-8025.2001.00818.x","article-title":"Responses of carboxylating enzymes, sucrose metabolizing enzymes and plant hormones in a tropical epiphytic CAM orchid to CO2 enrichment","volume":"25","author":"Li","year":"2002","journal-title":"Plant Cell Environ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1111\/j.1469-8137.2006.01818.x","article-title":"Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana","volume":"172","author":"Teng","year":"2006","journal-title":"New Phytol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Liu, J., Zhang, J., He, C., and Duan, A. (2014). Genes responsive to elevated CO2 concentrations in triploid white poplar and integrated gene network analysis. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0098300"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"627129","DOI":"10.3389\/fpls.2021.627129","article-title":"Proteomic Responses to Alkali Stress in Oats and the Alleviatory Effects of Exogenous Spermine Application","volume":"12","author":"Bai","year":"2021","journal-title":"Front. Plant Sci."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Soares, J., Deuchande, T., Valente, L.M.P., Pintado, M., and Vasconcelos, M.W. (2019). Growth and nutritional responses of bean and soybean genotypes to elevated CO2 in a controlled environment. Plants, 8.","DOI":"10.3390\/plants8110465"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.jplph.2008.06.011","article-title":"Metabolic responses in iron deficient tomato plants","volume":"166","author":"Morales","year":"2009","journal-title":"J. Plant Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/nprot.2014.022","article-title":"Universal sample preparation method integrating trichloroacetic acid\/acetone precipitation with phenol extraction for crop proteomic analysis","volume":"9","author":"Wu","year":"2014","journal-title":"Nat. Protoc."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Os\u00f3rio, H., Silva, C., Ferreira, M., Gullo, I., M\u00e1ximo, V., Barros, R., Mendon\u00e7a, F., Oliveira, C., and Carneiro, F. (2021). Proteomics Analysis of Gastric Cancer Patients with Diabetes Mellitus. J. Clin. Med., 10.","DOI":"10.3390\/jcm10030407"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1038\/s41536-021-00190-8","article-title":"Chondrogenic differentiation induced by extracellular vesicles bound to a nanofibrous substrate","volume":"6","author":"Casanova","year":"2021","journal-title":"NPJ Regen. Med."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1016\/j.molp.2019.01.003","article-title":"MapMan4: A Refined Protein Classification and Annotation Framework Applicable to Multi-Omics Data Analysis","volume":"12","author":"Schwacke","year":"2019","journal-title":"Mol. Plant"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1111\/j.1365-313X.2004.02016.x","article-title":"mapman: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes","volume":"37","author":"Thimm","year":"2004","journal-title":"Plant J."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1093\/nar\/gkw1041","article-title":"SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations","volume":"45","author":"Hooper","year":"2017","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/13632\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:11:47Z","timestamp":1760145107000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/13632"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,7]]},"references-count":51,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["ijms232113632"],"URL":"https:\/\/doi.org\/10.3390\/ijms232113632","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2022,11,7]]}}}