{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,5]],"date-time":"2025-11-05T14:35:17Z","timestamp":1762353317806,"version":"build-2065373602"},"reference-count":91,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,3,5]],"date-time":"2023-03-05T00:00:00Z","timestamp":1677974400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia (FCT)","award":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"],"award-info":[{"award-number":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"]}]},{"name":"national funds through FCT","award":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"],"award-info":[{"award-number":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"]}]},{"name":"Norte2020\u2014Sistema de Apoio \u00e0 Investiga\u00e7\u00e3o Cient\u00edfica e Tecnol\u00f3gica","award":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"],"award-info":[{"award-number":["SFRH\/BD\/116147\/2016","UIDB\/05748\/2020","UIDP\/05748\/2020","UIDB\/50016\/2020","NORTE-01-0145-FEDER-000041"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>This study aimed to understand the morphophysiological responses and primary metabolism of tomato seedlings subjected to mild levels of nitrogen and\/or water deficit (50% N and\/or 50% W). After 16 days of exposure, plants grown under the combined deficit showed similar behavior to the one found upon exposure to single N deficit. Both N deficit treatments resulted in a significantly lower dry weight, leaf area, chlorophyll content, and N accumulation but in a higher N use efficiency when compared to control (CTR) plants. Moreover, concerning plant metabolism, at the shoot level, these two treatments also responded in a similar way, inducing higher C\/N ratio, nitrate reductase (NR) and glutamine synthetase (GS) activity, expression of RuBisCO encoding genes as well as a downregulation of GS2.1 and GS2.2 transcripts. Interestingly, plant metabolic responses at the root level did not follow the same pattern, with plants under combined deficit behaving similarly to W deficit plants, resulting in enhanced nitrate and proline concentrations, NR activity, and an upregulation of GS1 and NR genes than in CTR plants. Overall, our data suggest that the N remobilization and osmoregulation strategies play a relevant role in plant acclimation to these abiotic stresses and highlight the complexity of plant responses under a combined N+W deficit.<\/jats:p>","DOI":"10.3390\/plants12051181","type":"journal-article","created":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T01:35:30Z","timestamp":1678066530000},"page":"1181","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Young Tomato Plants Respond Differently under Single or Combined Mild Nitrogen and Water Deficit: An Insight into Morphophysiological Responses and Primary Metabolism"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8222-7211","authenticated-orcid":false,"given":"Joana","family":"Machado","sequence":"first","affiliation":[{"name":"GreenUPorto\u2014Sustainable Agrifood Production Research Centre\/Inov4Agro, DGAOT, Faculty of Sciences, University of Porto, Campus de Vair\u00e3o, Rua da Agr\u00e1ria 747, 4485-646 Vair\u00e3o, Portugal"},{"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"},{"name":"Horticulture and Product Physiology Group, Department of Plant Sciences, Wageningen University, P.O. Box 16, 6700 AA Wageningen, The Netherlands"}]},{"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"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3330-2024","authenticated-orcid":false,"given":"Cristiano","family":"Soares","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Sustainable Agrifood Production Research Centre\/Inov4Agro, Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7756-5243","authenticated-orcid":false,"given":"Fernanda","family":"Fidalgo","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Sustainable Agrifood Production Research Centre\/Inov4Agro, Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8731-7195","authenticated-orcid":false,"given":"Ep","family":"Heuvelink","sequence":"additional","affiliation":[{"name":"Horticulture and Product Physiology Group, Department of Plant Sciences, Wageningen University, P.O. Box 16, 6700 AA Wageningen, The Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7157-1079","authenticated-orcid":false,"given":"Susana M. P.","family":"Carvalho","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Sustainable Agrifood Production Research Centre\/Inov4Agro, DGAOT, Faculty of Sciences, University of Porto, Campus de Vair\u00e3o, Rua da Agr\u00e1ria 747, 4485-646 Vair\u00e3o, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,5]]},"reference":[{"key":"ref_1","unstructured":"Fernandes, A., Machado, J., Fernandes, T., Vasconcelos, M., and Carvalho, S. (2022). Plant Nutrition and Food Security in the Era of Climate Change, Academic Press."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.plantsci.2016.04.008","article-title":"Review: Mechanisms of ammonium toxicity and the quest for tolerance","volume":"248","author":"Esteban","year":"2016","journal-title":"Plant Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.jclepro.2018.10.149","article-title":"Nitrogen footprint and nitrogen use efficiency of greenhouse tomato production in North China","volume":"208","author":"Liang","year":"2019","journal-title":"J. Clean. Prod."},{"key":"ref_4","unstructured":"Elbehri, A. (2015). Climate Change and Food Systems: Global Assessments and Implications for Food Security and Trade, Food and Agriculture Organization of the United Nations (FAO)."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/j.tplants.2017.05.004","article-title":"How plant root exudates shape the nitrogen cycle","volume":"22","author":"Coskun","year":"2017","journal-title":"Trends Plant Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1016\/j.scitotenv.2019.01.368","article-title":"N and P runoff losses in China\u2019s vegetable production systems: Loss characteristics, impact, and management practices","volume":"663","author":"Wang","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"17074","DOI":"10.1038\/nplants.2017.74","article-title":"Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition","volume":"3","author":"Coskun","year":"2017","journal-title":"Nat. Plants"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"30104","DOI":"10.1038\/srep30104","article-title":"Reducing human nitrogen use for food production","volume":"6","author":"Liu","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1038\/s43016-020-00166-9","article-title":"Game-changing potential of the EU\u2019s Farm to Fork Strategy","volume":"1","author":"Schebesta","year":"2020","journal-title":"Nat. Food"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Heuvelink, E., Okello, R.C., Peet, M., Giovannoni, J.J., and Dorais, M. (2020). Tomato, CABI International.","DOI":"10.1079\/9781786393777.0138"},{"key":"ref_11","unstructured":"De Cicco, A. (2019). The Fruit and Vegetable Sector in the EU\u2014A Statistical Overview Eurostat 2019."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"286","DOI":"10.21273\/HORTSCI15567-20","article-title":"Effect of planting density on the yield and growth of intercropped tomatoes and peppers in Florida","volume":"56","author":"Sandhu","year":"2021","journal-title":"HortScience"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.agwat.2018.08.035","article-title":"Water-and nitrogen-saving potentials in tomato production: A meta-analysis","volume":"210","author":"Du","year":"2018","journal-title":"Agric. Water Manag."},{"key":"ref_14","unstructured":"Machado, J., Fernandes, A., Fernandes, T., Heuvelink, E., Vasconcelos, M., and Carvalho, S. (2022). Plant Nutrition and Food Security in the Era of Climate Change, Academic Press."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1051\/agro\/2009059","article-title":"Water deficit and nitrogen nutrition of crops. A review","volume":"30","author":"Durand","year":"2010","journal-title":"Agron. Sustain. Dev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.3389\/fpls.2018.01143","article-title":"Is nitrogen a key determinant of water transport and photosynthesis in higher plants upon drought stress?","volume":"9","author":"Ding","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.tplants.2009.11.009","article-title":"Proline: A multifunctional amino acid","volume":"15","author":"Szabados","year":"2010","journal-title":"Trends Plant Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.4161\/psb.21949","article-title":"Role of proline under changing environments: A review","volume":"7","author":"Hayat","year":"2012","journal-title":"Plant Signal. Behav."},{"key":"ref_19","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_20","first-page":"75","article-title":"Analysis of nitrate reductase mRNA expression and nitrate reductase activity in response to nitrogen supply","volume":"3","author":"Kavoosi","year":"2014","journal-title":"Mol. Biol. Res. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1093\/pcp\/pcn081","article-title":"Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession","volume":"49","author":"Gaufichon","year":"2008","journal-title":"Plant Cell Physiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11104-013-1645-9","article-title":"Nitrogen acquisition by roots: Physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource","volume":"370","author":"Nacry","year":"2013","journal-title":"Plant Soil"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4452","DOI":"10.1093\/jxb\/eraa049","article-title":"The intersection of nitrogen nutrition and water use in plants: New paths toward improved crop productivity","volume":"71","author":"Plett","year":"2020","journal-title":"J. Exp. Bot."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.plaphy.2018.08.041","article-title":"Ammonium uptake and metabolism alleviate PEG-induced water stress in rice seedlings","volume":"132","author":"Cao","year":"2018","journal-title":"Plant Physiol. Biochem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/B978-0-444-89104-4.50024-4","article-title":"Effect of soil water and nutrient supply on root characteristics and nutrient uptake of plants","volume":"Volume 24","year":"1991","journal-title":"Developments in Agricultural and Managed Forest Ecology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1861","DOI":"10.1007\/s11738-011-0729-5","article-title":"Variation in the use efficiency of N under moderate water deficit in tomato plants (Solanum lycopersicum) differing in their tolerance to drought","volume":"33","author":"Blasco","year":"2011","journal-title":"Acta Physiol. Plant."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1016\/j.jplph.2010.11.018","article-title":"Ammonia production and assimilation: Its importance as a tolerance mechanism during moderate water deficit in tomato plants","volume":"168","author":"Blasco","year":"2011","journal-title":"J. Plant Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Zhou, R., Yu, X., Ottosen, C.-O., Rosenqvist, E., Zhao, L., Wang, Y., Yu, W., Zhao, T., and Wu, Z. (2017). Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol., 17.","DOI":"10.1186\/s12870-017-0974-x"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"393","DOI":"10.3389\/fpls.2018.00393","article-title":"Chilling and drought stresses in crop plants: Implications, cross talk, and potential management opportunities","volume":"9","author":"Hussain","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Sousa, B., Rodrigues, F., Soares, C., Martins, M., Azenha, M., Lino-Neto, T., Santos, C., Cunha, A., and Fidalgo, F. (2022). Impact of Combined Heat and Salt Stresses on Tomato Plants\u2014Insights into Nutrient Uptake and Redox Homeostasis. Antioxidants, 11.","DOI":"10.3390\/antiox11030478"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Machado, J., Vasconcelos, M.W., Soares, C., Fidalgo, F., Heuvelink, E., and Carvalho, S.M.P. (2023). Enzymatic and Non-Enzymatic Antioxidant Responses of Young Tomato Plants (cv. Micro-Tom) to Single and Combined Mild Nitrogen and Water Deficit: Not the Sum of the Parts. Antioxidants, 12.","DOI":"10.3390\/antiox12020375"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"974048","DOI":"10.3389\/fpls.2022.974048","article-title":"Transcriptomic and splicing changes underlying tomato responses to combined water and nutrient stress","volume":"13","author":"Ruggiero","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.crvi.2008.01.002","article-title":"Water-deficit stress-induced anatomical changes in higher plants","volume":"331","author":"Shao","year":"2008","journal-title":"Comptes Rendus Biol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Nemesk\u00e9ri, E., Nem\u00e9nyi, A., B\u0151cs, A., P\u00e9k, Z., and Helyes, L. (2019). Physiological Factors and their Relationship with the Productivity of Processing Tomato under Different Water Supplies. Water, 11.","DOI":"10.3390\/w11030586"},{"key":"ref_35","first-page":"319","article-title":"Effect of different nitrogen doses and deficit irrigation on nitrogen use efficiency and growth parameters of tomato crop under drip irrigation system","volume":"36","author":"Khan","year":"2020","journal-title":"Sarhad J. Agric."},{"key":"ref_36","first-page":"461","article-title":"Water stress affects growth and yield of container grown tomato (Lycopersicon esculentum Mill) plants","volume":"2","author":"Sibomana","year":"2013","journal-title":"GJBB"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"465","DOI":"10.4172\/2157-7110.1000465","article-title":"Effect of drought stress on tomato cv. Bombino","volume":"6","author":"Khan","year":"2015","journal-title":"J. Food Process. Technol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.plaphy.2018.05.008","article-title":"Drought induced changes of leaf-to-root relationships in two tomato genotypes","volume":"128","author":"Moles","year":"2018","journal-title":"Plant Physiol. Biochem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.actaastro.2011.05.025","article-title":"Physio-anatomical responses of drought stressed tomato plants to magnetic field","volume":"69","author":"Selim","year":"2011","journal-title":"Acta Astronaut."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"131","DOI":"10.11118\/actaun201058010131","article-title":"Effect of water stress on selected physiological characteristics of tomatoes","volume":"58","author":"Pokluda","year":"2010","journal-title":"Acta Univ. Agric. Silvic. Mendel. Brun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"159","DOI":"10.2134\/agronj2000.921159x","article-title":"Nitrogen stress effects on growth and nitrogen accumulation by field-grown tomato","volume":"92","author":"Scholberg","year":"2000","journal-title":"Agron. J."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.fcr.2004.09.013","article-title":"Effect of nitrogen supply on leaf appearance, leaf growth, leaf nitrogen economy and photosynthetic capacity in maize (Zea mays L.)","volume":"93","author":"Vos","year":"2005","journal-title":"Field Crops Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"11134","DOI":"10.1038\/ncomms11134","article-title":"Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme","volume":"7","author":"Cannella","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1007\/s00468-006-0084-0","article-title":"Comparative ecophysiological effects of drought on seedlings of the Mediterranean water-saver Pinus halepensis and water-spenders Quercus coccifera and Quercus ilex","volume":"20","author":"Baquedano","year":"2006","journal-title":"Trees"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2327","DOI":"10.1038\/s41598-018-20653-1","article-title":"Nitrogen supply influences photosynthesis establishment along the sugarcane leaf","volume":"8","author":"Bassi","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s11099-013-0021-6","article-title":"Photosynthesis under stressful environments: An overview","volume":"51","author":"Ashraf","year":"2013","journal-title":"Photosynthetica"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Tamburino, R., Vitale, M., Ruggiero, A., Sassi, M., Sannino, L., Arena, S., Costa, A., Batelli, G., Zambrano, N., and Scaloni, A. (2017). Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol., 17.","DOI":"10.1186\/s12870-017-0971-0"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1081\/PLN-120014065","article-title":"Tomato leaf chlorophyll meter readings as affected by variety, nitrogen form, and nighttime nutrient solution strength","volume":"25","author":"Wood","year":"2002","journal-title":"J. Plant Nutr."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fpls.2018.00048","article-title":"Divergent N deficiency-dependent senescence and transcriptome response in developmentally old and young Brassica napus leaves","volume":"9","author":"Franzaring","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1186\/s43141-021-00275-3","article-title":"Nitrogen deficiency regulates premature senescence by modulating flag leaf function, ROS homeostasis, and intercellular sugar concentration in rice during grain filling","volume":"19","author":"Zakari","year":"2021","journal-title":"J. Genet. Eng. Biotechnol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1016\/j.phytochem.2011.02.011","article-title":"Differential responses of five cherry tomato varieties to water stress: Changes on phenolic metabolites and related enzymes","volume":"72","author":"Moreno","year":"2011","journal-title":"Phytochemistry"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.scienta.2019.01.006","article-title":"Deficit irrigation in tomato: Agronomical and physio-biochemical implications","volume":"248","author":"Khapte","year":"2019","journal-title":"Sci. Hortic."},{"key":"ref_53","unstructured":"Taiz, L., Zeiger, E., M\u00f8ller, I.M., and Murphy, A. (2015). Plant Physiology and Development, Sinauer Associates Incorporated."},{"key":"ref_54","first-page":"24","article-title":"Stomatal responses to drought stress","volume":"1","author":"Pakniyat","year":"2016","journal-title":"Water Stress Crop Plants Sustain. Approach"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1111\/pce.12800","article-title":"Osmotic adjustment is a prime drought stress adaptive engine in support of plant production","volume":"40","author":"Blum","year":"2017","journal-title":"Plant Cell Environ."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1","DOI":"10.9734\/AJSSPN\/2017\/36861","article-title":"Fruit Quality and Osmotic Adjustment of Four Tomato Cultivars under Drought Stress","volume":"2","author":"Nahar","year":"2017","journal-title":"Asian J. Soil Sci. Plant Nutr."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"122","DOI":"10.3389\/fpls.2018.00122","article-title":"Plant abiotic stress proteomics: The major factors determining alterations in cellular proteome","volume":"9","author":"Urban","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_58","unstructured":"Qazi, H.A., Jan, N., Ramazan, S., and John, R. (2019). Protein Modificomics, Elsevier."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1093\/jexbot\/53.372.1331","article-title":"Role of superoxide dismutases (SODs) in controlling oxidative stress in plants","volume":"53","author":"Alscher","year":"2002","journal-title":"J. Exp. Bot."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s40659-018-0152-0","article-title":"Regulation of aquaporins in plants under stress","volume":"51","author":"Kapilan","year":"2018","journal-title":"Biol. Res."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Afzal, Z., Howton, T., Sun, Y., and Mukhtar, M.S. (2016). The roles of aquaporins in plant stress responses. J. Dev. Biol., 4.","DOI":"10.3390\/jdb4010009"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Yang, X., Lu, M., Wang, Y., Wang, Y., Liu, Z., and Chen, S. (2021). Response Mechanism of Plants to Drought Stress. Horticulturae, 7.","DOI":"10.20944\/preprints202102.0466.v1"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1093\/jxb\/eri059","article-title":"Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants","volume":"56","author":"Fernie","year":"2005","journal-title":"J. Exp. Bot."},{"key":"ref_64","first-page":"209","article-title":"Diverse responses of tomato to N and P deficiency","volume":"11","author":"Najafi","year":"2009","journal-title":"Int. J. Agric. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/S1369-5266(00)00168-0","article-title":"Carbon and nitrogen sensing and signaling in plants: Emerging \u2018matrix effects\u2019","volume":"4","author":"Coruzzi","year":"2001","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1104\/pp.010475","article-title":"Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: Nitrogen availability","volume":"128","author":"Martin","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1093\/pcp\/pcu002","article-title":"Ubiquitin ligase ATL31 functions in leaf senescence in response to the balance between atmospheric CO2 and nitrogen availability in Arabidopsis","volume":"55","author":"Aoyama","year":"2014","journal-title":"Plant Cell Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1104\/pp.117.1.283","article-title":"Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves","volume":"117","author":"Foyer","year":"1998","journal-title":"Plant Physiol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Chen, D., Wang, S., Xiong, B., Cao, B., and Deng, X. (2015). Carbon\/nitrogen imbalance associated with drought-induced leaf senescence in Sorghum bicolor. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0137026"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1104\/pp.117.1.293","article-title":"Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA","volume":"117","author":"Valadier","year":"1998","journal-title":"Plant Physiol."},{"key":"ref_71","first-page":"399","article-title":"Elevated CO2 reduces the drought effect on nitrogen metabolism in barley plants during drought and subsequent recovery","volume":"71","author":"Robredo","year":"2011","journal-title":"Environ. Exp. Bot."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1111\/j.1399-3054.1984.tb05180.x","article-title":"Sources of proline-nitrogen in water-stressed soybean (Glycine max). II. Fate of 15N-labelled protein","volume":"61","author":"Fukutoku","year":"1984","journal-title":"Physiol. Plant."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1981","DOI":"10.1093\/jexbot\/52.363.1981","article-title":"Post-translational regulation of nitrate reductase: Mechanism, physiological relevance and environmental triggers","volume":"52","author":"Kaiser","year":"2001","journal-title":"J. Exp. Bot."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1093\/aob\/mcaa155","article-title":"Regulation of sugar metabolism genes in the nitrogen-dependent susceptibility of tomato stems to Botrytis cinerea","volume":"127","author":"Lacrampe","year":"2020","journal-title":"Ann. Bot."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1104\/pp.88.2.383","article-title":"Expression of leaf nitrate reductase genes from tomato and tobacco in relation to light-dark regimes and nitrate supply","volume":"88","author":"Galangau","year":"1988","journal-title":"Plant Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1111\/j.1438-8677.2008.00097.x","article-title":"Leaf nitrogen remobilisation for plant development and grain filling","volume":"10","author":"Orsel","year":"2008","journal-title":"Plant Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1104\/pp.108.119040","article-title":"Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition","volume":"147","author":"Diaz","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1187","DOI":"10.1093\/aob\/mci131","article-title":"Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus) from stem extension to harvest. II. An 15N-labelling-based simulation model of N partitioning between vegetative and reproductive tissues","volume":"95","author":"Malagoli","year":"2005","journal-title":"Ann. Bot."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2097","DOI":"10.1104\/pp.105.060673","article-title":"Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways","volume":"138","author":"Thompson","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1111\/j.1438-8677.2008.00086.x","article-title":"Metabolic regulation of leaf senescence: Interactions of sugar signalling with biotic and abiotic stress responses","volume":"10","author":"Wingler","year":"2008","journal-title":"Plant Biol."},{"key":"ref_81","unstructured":"Hunt, R. (2012). Basic Growth Analysis: Plant Growth Analysis for Beginners, Springer Science & Business Media."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.envexpbot.2017.07.018","article-title":"Moderate salinity improves stomatal functioning in rose plants grown at high relative air humidity","volume":"143","author":"Carvalho","year":"2017","journal-title":"Environ. Exp. Bot."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/BF00018060","article-title":"Rapid determination of free proline for water-stress studies","volume":"39","author":"Bates","year":"1973","journal-title":"Plant Soil"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.envexpbot.2011.04.007","article-title":"Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and posttranslationally in Cd-induced stress","volume":"72","author":"Fidalgo","year":"2011","journal-title":"Environ. Exp. Bot."},{"key":"ref_85","unstructured":"Mills, H., and Jones, J.B. (1996). Plant Analysis Handbook II, MicroMacro Publishing."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1104\/pp.96.2.363","article-title":"Rapid modulation of spinach leaf nitrate reductase activity by photosynthesis: I. Modulation in vivo by CO2 availability","volume":"96","author":"Kaiser","year":"1991","journal-title":"Plant Physiol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1016\/0076-6879(71)17305-3","article-title":"[130] Glutamine synthetase (Escherichia coli)","volume":"Volume 17","author":"Shapiro","year":"1970","journal-title":"Methods in Enzymology"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Mariz-Ponte, N., Mendes, R.J., Sario, S., Correia, C.V., Correia, C.M., Moutinho-Pereira, J., Melo, P., Dias, M.C., and Santos, C. (2021). Physiological, biochemical and molecular assessment of UV-A and UV-B supplementation in Solanum lycopersicum. Plants, 10.","DOI":"10.3390\/plants10050918"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/aob\/mcp087","article-title":"Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum)","volume":"104","author":"Jin","year":"2009","journal-title":"Ann. Bot."},{"key":"ref_90","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"},{"key":"ref_91","first-page":"212","article-title":"Evaluation of real-time PCR data","volume":"18","author":"Vaerman","year":"2004","journal-title":"J. Biol. Regul. Homeost. Agents"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/5\/1181\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:48:11Z","timestamp":1760122091000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/5\/1181"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,5]]},"references-count":91,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["plants12051181"],"URL":"https:\/\/doi.org\/10.3390\/plants12051181","relation":{},"ISSN":["2223-7747"],"issn-type":[{"type":"electronic","value":"2223-7747"}],"subject":[],"published":{"date-parts":[[2023,3,5]]}}}