{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T07:28:18Z","timestamp":1780385298379,"version":"3.54.1"},"reference-count":72,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,3,11]],"date-time":"2022-03-11T00:00:00Z","timestamp":1646956800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Fundamental Research Funds for the Central Universities","award":["2572020DY04"],"award-info":[{"award-number":["2572020DY04"]}]},{"name":"the Forestry Science and Technology Promotion Project","award":["12, 2020133122"],"award-info":[{"award-number":["12, 2020133122"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Phosphorus (P) deficiency affects plant yield and quality, yet at the same time, excessive phosphorus application does not necessarily promote the growth of plants. How to maintain a balance between biomass accumulation and phosphorus application is a problem. Therefore, the purpose of this research was to explore the relationship between yield and quality of Bupleurum and phosphorus fertilization, based on three phosphorus fertilization levels (20 kg\u2219ha\u22121; 10 kg\u2219ha\u22121; and 0 kg\u2219ha\u22121). We adopted gas chromatography-mass spectrometry to assess the response of primary metabolites of different plant tissues (flowers, main shoots, lateral shoots and roots) to phosphorus fertilization. At the same time, high-performance liquid chromatography was used to quantify saikosaponin A and saikosaponin D, the main active ingredients of Bupleurum. Our research showed that low phosphorus level application has a positive impact on the yield and quality of Bupleurum, especially the above-ground parts increasing the fresh weight of flowers and lateral shoots and the length of main shoots, and moreover, increasing the saikosaponins content in all above-ground parts while decreasing the content in roots which show no significance increase in fresh weight and length. However, high phosphorus level showed a negative impact as it decreases the saikosaponins content significantly in flowers and roots. Furthermore, phosphorus application changed the proportion of saikosaponins, promoting the content of saikosaponin A and inhibiting the content of saikosaponin D in most organs of Bupleurum. Therefore, we can say that high phosphorus application is not preferable to the yield and quality of Bupleurum. To identify the metabolic pathways and special key metabolites, a total of 73 metabolites were discovered, and four differential metabolites\u2014ether, glycerol, chlorogenic and L-rhamnose\u2014were considered to be the key metabolites of Bupleurum\u2019s response to phosphorus fertilization. Furthermore, Bupleurum\u2019s response to phosphorus fertilization was mainly related to metabolic pathways, such as starch and sucrose metabolism and galactose metabolism. Under the phosphorus level, the content of sugars, organic acids and their derivatives, polyols and their derivatives and alkyl were upregulated in flowers. Furthermore, the contents of compounds in the main shoot and lateral shoots showed the same upward trend, except glycosides and polyols and their derivatives.<\/jats:p>","DOI":"10.3390\/plants11060752","type":"journal-article","created":{"date-parts":[[2022,3,13]],"date-time":"2022-03-13T21:44:17Z","timestamp":1647207857000},"page":"752","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Metabolite Profiles Provide Insights into Underlying Mechanism in Bupleurum (Apiaceae) in Response to Three Levels of Phosphorus Fertilization"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3642-8055","authenticated-orcid":false,"given":"Jialin","family":"Sun","sequence":"first","affiliation":[{"name":"College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China"},{"name":"Biological Science and Technology Department, Heilongjiang Vocational College for Nationalities, Harbin 150066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zejia","family":"Duan","sequence":"additional","affiliation":[{"name":"College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ye","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sisi","family":"Cao","sequence":"additional","affiliation":[{"name":"Medical Department, Harbin Vocational & Technical College, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3278-5861","authenticated-orcid":false,"given":"Zhonghua","family":"Tang","sequence":"additional","affiliation":[{"name":"College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1282-0068","authenticated-orcid":false,"given":"Ann","family":"Abozeid","sequence":"additional","affiliation":[{"name":"Botany and Microbiology Department, Faculty of Science, Menoufia University, Shebin Elkoom 32511, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.phytochem.2012.02.004","article-title":"Influence of repeated short-term nitrogen limitations on leaf phenolics metabolism in tomato","volume":"77","author":"Larbat","year":"2012","journal-title":"Phytochemistry"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.17957\/IJAB\/15.0217","article-title":"Response of nitrogen, phosphorus and potassium fertilization on productivity and quality of winter rapeseed in Central China","volume":"18","author":"Yousaf","year":"2016","journal-title":"Int. J. Agric. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1046\/j.1469-8137.2003.00695.x","article-title":"Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource","volume":"157","author":"Vance","year":"2003","journal-title":"New Phytol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.plantsci.2015.06.018","article-title":"Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency","volume":"239","author":"Sulieman","year":"2015","journal-title":"Plant Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/j.plantsci.2018.11.011","article-title":"Review: Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved","volume":"280","author":"Ferrol","year":"2019","journal-title":"Plant Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1146\/annurev-arplant-042110-103849","article-title":"Signaling network in sensing phosphate availability in plants","volume":"62","author":"Chiou","year":"2011","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.devcel.2019.01.002","article-title":"Tackling plant phosphorus starvation by the roots","volume":"48","author":"Crombez","year":"2019","journal-title":"Dev. Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.plaphy.2021.05.043","article-title":"Comparative transcriptomic and metabolomic analyses reveal the protective effects of silicon against low phosphorus stress in tomato plants","volume":"166","author":"Zhang","year":"2021","journal-title":"Plant Physiol. Biochem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1093\/aob\/mcs285","article-title":"Responses of root architecture development to low phosphorus availability: A review","volume":"112","author":"Niu","year":"2013","journal-title":"Ann. Bot."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"995","DOI":"10.3389\/fpls.2019.00995","article-title":"Genotypic variation in the root and shoot metabolite profiles of wheat (Triticum aestivum L.) indicate sustained, preferential carbon allocation as a potential mechanism in phosphorus efficiency","volume":"10","author":"Nguyen","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s11104-020-04444-0","article-title":"Phosphorus uptake and partitioning in two durum wheat cultivars with contrasting biomass allocation as affected by different p supply during grain filling","volume":"449","author":"Mazlouzi","year":"2020","journal-title":"Plant Soil"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.jep.2015.12.061","article-title":"UHPLC\/Q-TOFMS-based metabolomics for the characterization of cold and hot properties of Chinese materiamedica","volume":"179","author":"Wang","year":"2016","journal-title":"J. Ethnopharmacol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.jchromb.2016.02.007","article-title":"Metabolomics approach to explore the effects of Kai-Xin-San on Alzheimer\u2019s disease using UPLC\/ESI-Q-TOF mass spectrometry","volume":"1015\u20131016","author":"Chu","year":"2016","journal-title":"J. Chromatogr. B Analyt. Technol. Biomed. Life Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.tibtech.2004.03.007","article-title":"Metabolomics by numbers: Acquiring and understanding global metabolite data","volume":"22","author":"Goodacre","year":"2004","journal-title":"Trends Biotechnol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.phymed.2018.04.004","article-title":"Identifying quality-markers from Shengmai San protects against transgenic mouse model of Alzheimer\u2019s disease using chinmedomics approach","volume":"45","author":"Zhang","year":"2018","journal-title":"Phytomedicine"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1616","DOI":"10.1111\/pbi.12899","article-title":"Deciphering drought-induced metabolic responses and regulation in developing maize kernels","volume":"16","author":"Yang","year":"2018","journal-title":"Plant Biotechnol. J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"8711","DOI":"10.1021\/jf402043m","article-title":"Comparative metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of their offspring","volume":"61","author":"Lu","year":"2013","journal-title":"J. Agric. Food Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"109280","DOI":"10.1016\/j.scienta.2020.109280","article-title":"UPLC-Triple TOF-MS\/MS based metabolomics approach to reveal the influence of nitrogen levels on Isatis indigotica seedling leaf","volume":"266","author":"Cao","year":"2020","journal-title":"Sci. Hortic."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.jpba.2017.04.009","article-title":"Nontargeted metabolomics approach for the differentiation of cultivation ages of mountain cultivated ginseng leaves using UHPLC\/QTOF-MS","volume":"141","author":"Chang","year":"2017","journal-title":"J. Pharm. Biomed. Anal."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Shi, Z., Wei, F., Wan, R., Li, Y., Wang, Y., An, W., Qin, K., Dai, G., Cao, Y., and Feng, J. (2019). Impact of nitrogenfertilizer levels on metabolite profiling of the Lyciumbarbarum L. fruit. Molecules, 24.","DOI":"10.3390\/molecules24213879"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"14656","DOI":"10.1038\/s41598-020-71492-y","article-title":"Impact of phosphorus fertilizer level on the yield and metabolome of goji fruit","volume":"10","author":"Wei","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s12038-020-00125-3","article-title":"Metabolite profiling of violet, white and pink flowers revealing flavonoids composition patterns in Rhododendron pulchrum Sweet","volume":"46","author":"Wang","year":"2021","journal-title":"J. Biosci."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Liu, J., Liu, Y., Wang, Y., Abozeid, A., Zu, Y.G., Zhang, X.N., and Tang, Z.H. (2017). GC-MS metabolomic analysis to reveal the metabolites and biological pathways involved in the developmental stages and tissue response of Panax ginseng. Molecules, 22.","DOI":"10.3390\/molecules22030496"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"11460","DOI":"10.1038\/s41598-021-90961-6","article-title":"Comparative analysis of tuberous root metabolites between cultivated and wild varieties of Rehmanniaglutinosa by widely targeted metabolomics","volume":"11","author":"Zhou","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Liu, Y., Liu, J., Abozeid, A., Wu, K.X., Guo, X.R., Mu, L.Q., and Tang, Z.H. (2020). UV-B radiation largely promoted the transformation of primary metabolites to phenols in Astragalusmongholicus seedlings. Biomolecules, 10.","DOI":"10.3390\/biom10040504"},{"key":"ref_26","unstructured":"Pimenov, M.G., and Leonov, M.V. (1993). The Genera of the Umbelliferae, Royal Botanic Gardens."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"424","DOI":"10.2179\/08-043R2.1","article-title":"Bupleurum gerardii All. (Apiaceae), an addition to the North American Flora, with comments onthe treatment of aliens in Floras","volume":"73","author":"Neves","year":"2009","journal-title":"Castanea"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.jpha.2020.06.006","article-title":"Comparative permeability of three saikosaponinsand corresponding saikogenins in Caco-2 model by a validated UHPLC-MS\/MS method","volume":"11","author":"Ren","year":"2021","journal-title":"J. Pharm. Anal."},{"key":"ref_29","first-page":"7597596","article-title":"Radix Bupleuri: A review of traditional uses, botany, phytochemistry, pharmacology, and toxicology","volume":"2017","author":"Yang","year":"2017","journal-title":"Biomed. Res. Int."},{"key":"ref_30","first-page":"e5133","article-title":"Comparison of chemical constituents of Bupleurummarginatum var","volume":"35","author":"Xia","year":"2021","journal-title":"stenophyllum and Bupleurumchinense DC. using UHPLC-Q-TOF-MS based on a metabonomics approach. Biomed. Chromatogr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"103929","DOI":"10.1016\/j.bse.2019.103929","article-title":"Chemical constituents from Bupleurumchinese and their chemotaxonomic significance","volume":"86","author":"Li","year":"2019","journal-title":"Biochem. Syst. Ecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1007\/s12272-011-0613-2","article-title":"Species classification and quality assessment of Chaihu (Radix Bupleuri) based on high-performance liquid chromatographic fingerprint and combined chemometrics methods","volume":"34","author":"Liu","year":"2011","journal-title":"Arch. Pharm. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.ijbiomac.2016.10.112","article-title":"Anti-tumor and immunomodulatoryactivitiesinduced by an alkali-extracted polysaccharide BCAP-1 from Bupleurumchinense via NF-\u03baB signaling pathway","volume":"95","author":"Song","year":"2017","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1594","DOI":"10.1016\/j.bmcl.2016.02.004","article-title":"Neuroprotectiveoleananetriterpenes from the roots of Bupleurumchinense","volume":"26","author":"Li","year":"2016","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1080\/13880209.2016.1262433","article-title":"A systematic review of the active saikosaponinsandextracts isolated from Radix Bupleuri and their applications","volume":"55","author":"Yuan","year":"2017","journal-title":"Pharm. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5272","DOI":"10.3748\/wjg.v26.i35.5272","article-title":"New approach of medicinal herbs and sulfasalazi.ne mixture on ulcerative colitis induced by dextran sodium sulfate","volume":"26","author":"Shin","year":"2020","journal-title":"World J. Gastroenterol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.apsb.2013.04.002","article-title":"Chemical profiling and histochemical analysis of Bupleurummarginatum roots from different growing areas of Hubei province","volume":"3","author":"Liang","year":"2013","journal-title":"Acta Pharm. Sin. B"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"192","DOI":"10.4161\/psb.6.2.14425","article-title":"The aspartate-family pathway of plants: Linking production of essential amino acids with energy and stress regulation","volume":"6","author":"Galili","year":"2011","journal-title":"Plant Signal. Behav."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.jpba.2014.08.030","article-title":"Qualitative and quantitative analysis on aroma characteristics of ginseng at different ages using E-nose and GC-MS combined with chemometrics","volume":"102","author":"Cui","year":"2015","journal-title":"J. Pharm. Biomed. Anal."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"18296","DOI":"10.1038\/srep18296","article-title":"Metabolomic analysis withGC-MS to reveal potential metabolites and biological pathways involved in Pb& Cd stress response ofradish roots","volume":"5","author":"Wang","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1457","DOI":"10.1038\/nprot0915-1457a","article-title":"Corrigendum: Gas chromatography massspectrometry-based metabolite profiling in plants","volume":"10","author":"Lisec","year":"2015","journal-title":"Nat. Protoc."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.phytochem.2006.10.023","article-title":"Metabolic profiling and systematic identification of flavonoids and isoflavonoids in roots and cell suspension cultures of Medicagotruncatula using HPLC-UV-ESI-MS and GC-MS","volume":"68","author":"Farag","year":"2007","journal-title":"Phytochemistry"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1007\/s11306-012-0470-0","article-title":"Grangercausality in integrated GC\u2013MS and LC\u2013MS metabolomics data reveals the interface of primary and secondarymetabolism","volume":"9","author":"Doerfler","year":"2013","journal-title":"Metabolomics"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.plaphy.2021.01.015","article-title":"Effects of phosphorus on fruit soluble sugar and citric acid accumulations in citrus","volume":"160","author":"Wu","year":"2021","journal-title":"Plant Physiol. Biochem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"104187","DOI":"10.1016\/j.envexpbot.2020.104187","article-title":"Characterization of COMT1-mediated low phosphorus resistance mechanism by metabolomics in tomato plants","volume":"179","author":"Xu","year":"2020","journal-title":"Environ. Exp. Bot."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1104\/pp.107.096958","article-title":"Phosphorus stress in common bean: Root transcript and metabolic responses","volume":"144","author":"Hernandez","year":"2007","journal-title":"Plant Physiol."},{"key":"ref_47","first-page":"108","article-title":"Study on effect of phosphorus on growth and flowering of marigold (tageteserecta)","volume":"1","author":"Dangi","year":"2019","journal-title":"JOJ Wildl. Biodivers."},{"key":"ref_48","first-page":"158","article-title":"Effect of nitrogen andphosphorus on flowering and yield of African marigold (Tagetes erecta Linn.)","volume":"10","author":"Sharma","year":"2010","journal-title":"Progress. Agric."},{"key":"ref_49","first-page":"153","article-title":"Effect of plant density, nitrogen and phosphorus levels on growth, yield and quality of AfricanMarigold","volume":"14","author":"Ahirwar","year":"2012","journal-title":"Ann. Plant Soil Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1104\/pp.111.175414","article-title":"Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops","volume":"156","author":"Lynch","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_51","first-page":"103827","article-title":"Phosphorus supply alters the root metabolism of Chinese flowering cabbage (Brassica campestris L. ssp. chinensis var","volume":"167","author":"Yang","year":"2019","journal-title":"utilis Tsenet Lee) and the mobilization of Cd bound to lepidocrocite in soil. Environ. Exp. Bot."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.3389\/fpls.2016.01664","article-title":"Rhizosphereorganicanions play a minor role in improving crop species\u2019 ability to take up residual phosphorus (P) in agricultural soils low in Pavailability","volume":"7","author":"Wang","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/00380768.2018.1476828","article-title":"Metabolite profiling of shoot extract, root extract, and root exudate of rice under nitrogen and phosphorus deficiency","volume":"64","author":"Tawaraya","year":"2018","journal-title":"Soil Sci. Plant Nutr."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1146\/annurev-arplant-050213-040251","article-title":"Sucrose metabolism: Gateway to diverse carbon use and sugar signaling","volume":"65","author":"Ruan","year":"2014","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"plv097","DOI":"10.1093\/aobpla\/plv097","article-title":"Contrasting responses of root morphology and root-exuded organic acids to low phosphorus availability in three important food crops with divergent root traits","volume":"7","author":"Wang","year":"2015","journal-title":"AoB Plants"},{"key":"ref_56","first-page":"3759","article-title":"Transcriptome and metabolome analyses provide insights into root and root-released organic anion responses to phosphorus deficiency in oat","volume":"69","author":"Wang","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1093\/pcp\/pcn044","article-title":"Metabolite profiling reveals distinct changes in carbon and nitrogenmetabolism in phosphate-deficient barley plants (Hordeum vulgare L.)","volume":"49","author":"Huang","year":"2008","journal-title":"Plant Cell Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Ganie, A.H., Ahmad, A., Pandey, R., Aref, I.M., Yousuf, P.Y., Ahmad, S., and Iqbal, M. (2015). Metabolite profiling of low-P tolerant and low-P sensitive maize genotypes under phosphorus starvation and restoration conditions. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0129520"},{"key":"ref_59","first-page":"1014","article-title":"Metabolic adaptations of white lupinroots and shoots under phosphorus deficiency","volume":"6","author":"Niehaus","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3906","DOI":"10.1002\/jsfa.7594","article-title":"Short-and long-term effects of carbohydrate limitation on sugar and organic acid accumulation during mandarin fruit growth","volume":"96","author":"Antoine","year":"2016","journal-title":"J. Sci. Food Agric."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.foodchem.2018.03.102","article-title":"Fruit sugar andorganic acid were significantly related to fruit Mg of six citrus cultivars","volume":"259","author":"Zhou","year":"2018","journal-title":"Food Chem."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.scienta.2015.05.008","article-title":"Soil application of calciumand magnesium fertilizer influences the fruit pulp mastication characteristics ofNanfeng tangerine (Citrus reticulata Blanco cv. Kinokuni)","volume":"191","author":"Zheng","year":"2015","journal-title":"Sci. Hortic."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2134\/agronj14.0122","article-title":"Soil application of Boron and Zinc influence fruit yield and quality of Satsuma Mandarin in acidic soils","volume":"107","author":"Zhang","year":"2015","journal-title":"Agron. J."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"125617","DOI":"10.1016\/j.foodchem.2019.125617","article-title":"Dynamic changes of enzymes involved in sugar and organic acid level modification during blueberry fruit maturation","volume":"309","author":"Li","year":"2020","journal-title":"Food Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.jplph.2010.09.017","article-title":"Root release and metabolism of organic acids in tea plants in response to phosphorus supply","volume":"168","author":"Lin","year":"2011","journal-title":"J. Plant Physiol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1007\/s11104-017-3214-0","article-title":"Maize responds to low shoot P concentration by altering rootmorphology rather than increasing root exudation","volume":"416","author":"Wen","year":"2017","journal-title":"Plant Soil."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.3389\/fpls.2016.01939","article-title":"Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply","volume":"7","author":"Lyu","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1590\/1678-4499.0408","article-title":"Determination of optimum levels of nitrogen, phosphorus and potassium of oil palm seedlings in solution culture","volume":"74","author":"Mohidin","year":"2015","journal-title":"Bragantia"},{"key":"ref_69","unstructured":"Chinese Pharmacopoeia Commission (2020). Pharmacopoeia of People\u2019s Republic of China, China Medical Sciences and Technology Press. (In Chinese)."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"110128","DOI":"10.1016\/j.foodres.2021.110128","article-title":"Widely targeted metabolomics analysis reveals new biomarkers and mechanistic insights on chestnut (Castaneamollissima Bl.) calcification process","volume":"141","author":"Xiao","year":"2021","journal-title":"Food Res. Int."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1007\/s00425-004-1446-8","article-title":"Amino acid contents and transport in oilseed rape (Brassica napus L.) under different nitrogen conditions","volume":"221","author":"Tilsner","year":"2005","journal-title":"Planta"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Sun, J., Li, W., Zhang, Y., Guo, Y., Duan, Z., Tang, Z., and Abozeid, A. (2021). Metabolomics analysis reveals potential mechanisms in Bupleurum L. (Apiaceae) induced by three levels of Nitrogen fertilization. Agronomy, 11.","DOI":"10.3390\/agronomy11112291"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/11\/6\/752\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:35:12Z","timestamp":1760135712000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/11\/6\/752"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,11]]},"references-count":72,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["plants11060752"],"URL":"https:\/\/doi.org\/10.3390\/plants11060752","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,11]]}}}