{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T11:43:36Z","timestamp":1790768616778,"version":"4.1.0"},"reference-count":114,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2019,6,26]],"date-time":"2019-06-26T00:00:00Z","timestamp":1561507200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Key R&amp;D Program of China","award":["2017YFD0202000"],"award-info":[{"award-number":["2017YFD0202000"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31301740"],"award-info":[{"award-number":["31301740"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003392","name":"Natural Science Foundation of Fujian Province","doi-asserted-by":"publisher","award":["2014J05033"],"award-info":[{"award-number":["2014J05033"]}],"id":[{"id":"10.13039\/501100003392","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Magnesium (Mg) deficiency is one of the major constraining factors that limit the yield and quality of agricultural products. Uniform seedlings of the Citrus sinensis were irrigated with Mg deficient (0 mM MgSO4) and Mg sufficient (1 mM MgSO4) nutrient solutions for 16 weeks. CO2 assimilation, starch, soluble carbohydrates, TBARS content and H2O2 production were measured. Transcriptomic analysis of C. sinensis leaves was performed by Illumina sequencing. Our results showed that Mg deficiency decreased CO2 assimilation, but increased starch, sucrose, TBARS content and H2O2 production in C. sinensis leaves. A total of 4864 genes showed differential expression in response to Mg deficiency revealed by RNA-Seq and the transcriptomic data were further validated by real-time quantitative PCR (RT-qPCR). Gene ontology (GO) enrichment analysis indicated that the mechanisms underlying Mg deficiency tolerance in C. sinensis may be attributed to the following aspects: (a) enhanced microtubule-based movement and cell cycle regulation; (b) elevated signal transduction in response to biotic and abiotic stimuli; (c) alteration of biological processes by tightly controlling phosphorylation especially protein phosphorylation; (d) down-regulation of light harvesting and photosynthesis due to the accumulation of carbohydrates; (e) up-regulation of cell wall remodeling and antioxidant system. Our results provide a comprehensive insight into the transcriptomic profile of key components involved in the Mg deficiency tolerance in C. sinensis and enrich our understanding of the molecular mechanisms by which plants adapted to a Mg deficient condition.<\/jats:p>","DOI":"10.3390\/ijms20133129","type":"journal-article","created":{"date-parts":[[2019,6,27]],"date-time":"2019-06-27T02:50:15Z","timestamp":1561603815000},"page":"3129","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":53,"title":["Magnesium Deficiency Induced Global Transcriptome Change in Citrus sinensis Leaves Revealed by RNA-Seq"],"prefix":"10.3390","volume":"20","author":[{"given":"Lin-Tong","family":"Yang","sequence":"first","affiliation":[{"name":"Institute of Plant Nutritional Physiology and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang-Fei","family":"Zhou","sequence":"additional","affiliation":[{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan-Yu","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan-Mei","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Ye","sequence":"additional","affiliation":[{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7963-1328","authenticated-orcid":false,"given":"Jiu-Xin","family":"Guo","sequence":"additional","affiliation":[{"name":"Institute of Plant Nutritional Physiology and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8425-1306","authenticated-orcid":false,"given":"Li-Song","family":"Chen","sequence":"additional","affiliation":[{"name":"Institute of Plant Nutritional Physiology and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China"},{"name":"Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,6,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Peng, H.Y., Qi, Y.P., Lee, J., Yang, L.T., Guo, P., Jiang, H., and Chen, L.S. (2015). Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency. BMC Genom., 16.","DOI":"10.1186\/s12864-015-1462-z"},{"key":"ref_2","first-page":"263","article-title":"Soil chemical properties, \u2018Guanximiyou\u2019 pummelo leaf mineral nutrient status and fruit quality in the southern region of Fujian province, China","volume":"15","author":"Li","year":"2015","journal-title":"J. Soil Sci. Plant Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.cj.2015.11.003","article-title":"Magnesium deficiency in plants: An urgent problem","volume":"4","author":"Guo","year":"2016","journal-title":"Crop J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1023\/A:1016070614042","article-title":"Structural and catalytic roles for divalent magnesium in nucleic acid biochemistry","volume":"15","author":"Sreedhara","year":"2002","journal-title":"Biometals"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"6146","DOI":"10.1093\/emboj\/cdf624","article-title":"From chloroplasts to photosystems: In situ scanning force microscopy on intact thylakoid membranes","volume":"21","author":"Kaftan","year":"2002","journal-title":"EMBO J."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1038\/s41477-018-0191-0","article-title":"Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis","volume":"4","author":"Bloom","year":"2018","journal-title":"Nat. Plants"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Aro, E.M., and Anderson, B. (2001). Transport of metals: A key process in oxygenic photosynthesis. Regulation of Photosynthesis, Springer.","DOI":"10.1007\/0-306-48148-0"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1023\/A:1016022730880","article-title":"Structural and catalytic chemistry of magnesium-dependent enzymes","volume":"15","author":"Cowan","year":"2002","journal-title":"Biometals"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1007\/s00468-012-0699-2","article-title":"Physiological impacts of magnesium-deficiency in Citrus seedlings: Photosynthesis, antioxidant system and carbohydrates","volume":"26","author":"Yang","year":"2012","journal-title":"Trees"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1007\/s12011-012-9340-x","article-title":"Magnesium deficiency results in damage of nitrogen and carbon cross-talk of maize and improvement by cerium addition","volume":"148","author":"Zhao","year":"2012","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2091","DOI":"10.3389\/fpls.2017.02091","article-title":"Metabolomics reveals distinct carbon and nitrogen metabolic responses to magnesium deficiency in leaves and roots of soybean [Glycine max (Linn.) Merr.]","volume":"8","author":"Yang","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1093\/jxb\/45.9.1251","article-title":"Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants","volume":"45","author":"Cakmak","year":"1994","journal-title":"J. Exp. Bot."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/s00425-004-1376-5","article-title":"Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves","volume":"220","author":"Hermans","year":"2005","journal-title":"Planta"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1111\/j.1399-3054.2007.01042.x","article-title":"Role of magnesium in carbon partitioning and alleviating photooxidative damage","volume":"133","author":"Cakmak","year":"2008","journal-title":"Physiol. Plantarum"},{"key":"ref_15","first-page":"771","article-title":"Magnesium as a nutritional tool of nitrogen efficient management-plant production and environment","volume":"15","author":"Grzebisz","year":"2010","journal-title":"J. Elementol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2665","DOI":"10.1093\/nar\/11.9.2665","article-title":"Quantitation of cation binding to wheat germ ribosomes: Influences on subunit association equilibria and ribosome activity","volume":"11","author":"Sperrazza","year":"1983","journal-title":"Nucleic Acids Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1002\/jpln.201300127","article-title":"Increasing root and leaf growth and yield in Mg-deficient faba beans (Vicia faba) by MgSO4 foliar fertilization","volume":"177","author":"Neuhaus","year":"2014","journal-title":"J. Plant Nutr. Soil Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1564","DOI":"10.1093\/treephys\/tpx067","article-title":"Magnesium-deficiency-induced alterations of gas exchange, major metabolites and key enzymes differ among roots, and lower and upper leaves of Citrus sinensis seedlings","volume":"37","author":"Li","year":"2017","journal-title":"Tree Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.jplph.2016.04.011","article-title":"Alterations of physiology and gene expression due to long-term magnesium-deficiency differ between leaves and roots of Citrus reticulata","volume":"198","author":"Jin","year":"2016","journal-title":"J. Plant Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1146\/annurev-arplant-042817-040322","article-title":"Reactive Oxygen Species in Plant Signaling","volume":"69","author":"Waszczak","year":"2018","journal-title":"Ann. Rev. Plant Biol."},{"key":"ref_21","first-page":"23","article-title":"Magnesium: A forgotten element in crop production","volume":"94","author":"Cakmak","year":"2010","journal-title":"Better Crops"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.scienta.2005.12.006","article-title":"Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants","volume":"108","author":"Kumar","year":"2006","journal-title":"Sci. Hortic."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0981-9428(02)00006-2","article-title":"Relationship among chlorophyll-carotenoid content, antioxidant enzyme activities and lipid peroxidation levels by Mg2+ deficiency in the Mentha pulegium leaves","volume":"41","author":"Candan","year":"2003","journal-title":"Plant Physiol. Biochem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1016\/j.plantsci.2003.11.004","article-title":"Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize","volume":"166","author":"Kumar","year":"2004","journal-title":"Plant Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s10725-005-5466-6","article-title":"Suitability of the antioxidative system as marker of magnesium deficiency in Capsicum annuum L. plants under controlled conditions","volume":"46","author":"Riga","year":"2005","journal-title":"Plant Growth Regul."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/S1002-0160(08)60021-1","article-title":"High potassium aggravates the oxidative stress inducedy by magnesium deflciency in rice leaves","volume":"18","author":"Ding","year":"2008","journal-title":"Pedosphere"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1111\/j.1399-3054.2007.01025.x","article-title":"Metabolomics for plant stress response","volume":"132","author":"Shulaev","year":"2008","journal-title":"Physiol. Plantarum"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1111\/j.1469-8137.2010.03258.x","article-title":"Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes","volume":"187","author":"Hermans","year":"2010","journal-title":"New Phytol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1111\/j.1469-8137.2010.03257.x","article-title":"Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana","volume":"187","author":"Hermans","year":"2010","journal-title":"New Phytol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1080\/01904169209364307","article-title":"Ethylene evolution and ammonium accumulation by nutrient-stressed tomato plants","volume":"15","author":"Feng","year":"1992","journal-title":"J. Plant Nutr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1007\/s10535-013-0313-5","article-title":"Magnesium deficiency-induced changes in organic acid metabolism of Citrus sinensis roots and leaves","volume":"57","author":"Yang","year":"2013","journal-title":"Biol. Plantarum"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"330","DOI":"10.3389\/fpls.2017.00330","article-title":"Root adaptive responses to aluminum-treatment revealed by RNA-seq in two citrus species with different aluminum-tolerance","volume":"8","author":"Guo","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"R14","DOI":"10.1186\/gb-2010-11-2-r14","article-title":"Gene ontology analysis for RNA-seq: Accounting for selection bias","volume":"11","author":"Young","year":"2010","journal-title":"Genome Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1016\/j.tplants.2006.10.007","article-title":"How do plants respond to nutrient shortage by biomass allocation?","volume":"11","author":"Hermans","year":"2006","journal-title":"Trends Plant Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.bbabio.2003.09.005","article-title":"Membrane potential, adenylate levels and Mg2+ are interconnected via adenylate kinase equilibrium in plant cells","volume":"1607","author":"Igamberdiev","year":"2003","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1038\/380451a0","article-title":"Direct observation of single kinesin molecules moving along microtubules","volume":"380","author":"Vale","year":"1996","journal-title":"Nature"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.procbio.2005.03.071","article-title":"Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor","volume":"41","author":"Savitha","year":"2006","journal-title":"Process Biochem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1104\/pp.011028","article-title":"The cell wall-associated kinase (WAK) and WAK-like kinase gene family","volume":"129","author":"Verica","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"R139","DOI":"10.1186\/gb-2013-14-12-r139","article-title":"Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity","volume":"14","author":"Rosli","year":"2013","journal-title":"Genome Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"88","DOI":"10.3389\/fpls.2012.00088","article-title":"The cell wall-associated kinases, WAKs, as pectin receptors","volume":"3","author":"Kohorn","year":"2012","journal-title":"Front. Plant Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2256","DOI":"10.1104\/pp.103.022129","article-title":"Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis","volume":"132","author":"Sivaguru","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1093\/mp\/sst033","article-title":"Knights in action: Lectin receptor-like kinases in plant development and stress responses","volume":"6","author":"Vaid","year":"2013","journal-title":"Mol. Plant"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.plantsci.2012.12.019","article-title":"Overexpression of L-type lectin-like protein kinase 1 confers pathogen resistance and regulates salinity response in Arabidopsis thaliana","volume":"203","author":"Huang","year":"2013","journal-title":"Plant Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"28950","DOI":"10.1038\/srep28950","article-title":"Small glutamine-rich tetratricopeptide repeat-containing protein alpha (SGTA) ablation limits offspring viability and growth in mice","volume":"6","author":"Philp","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1007\/s11104-017-3436-1","article-title":"Identification of genome-wide single-nucleotide polymorphisms (SNPs) associated with tolerance to chromium toxicity in spring wheat (Triticum aestivum L.)","volume":"422","author":"Almas","year":"2018","journal-title":"Plant Soil"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1023\/A:1020687518999","article-title":"Plant lectins: Occurrence, biochemistry, functions and applications","volume":"18","author":"Gabius","year":"2001","journal-title":"Glycoconjugate J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1271\/bbb.90847","article-title":"Assimilation of formaldehyde in transgenic plants due to the introduction of the bacterial ribulose monophosphate pathway genes","volume":"74","author":"Chen","year":"2010","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1093\/mp\/ssp052","article-title":"Towards characterization of the chloroplast NAD(P)H dehydrogenase complex","volume":"2","author":"Suorsa","year":"2009","journal-title":"Mol. Plant"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1104\/pp.88.1.172","article-title":"Purification and properties of glucoamylase from sugar beet cells in suspension culture","volume":"88","author":"Masuda","year":"1988","journal-title":"Plant Physiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s11120-015-0076-2","article-title":"Genetic and genomic analysis of RNases in model cyanobacteria","volume":"126","author":"Cameron","year":"2015","journal-title":"Photosynth. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"dev151894","DOI":"10.1242\/dev.151894","article-title":"Brassinosteroid signaling in plant development and adaptation to stress","volume":"146","author":"Gupta","year":"2019","journal-title":"Development"},{"key":"ref_52","first-page":"86","article-title":"Phosphorylation of intrinsically disordered regions in remorin proteins","volume":"3","author":"Ott","year":"2012","journal-title":"Front. Plant Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/S0003-9861(03)00115-2","article-title":"Control of the phosphorylation of phosphoenolpyruvate carboxylase in higher plants","volume":"414","author":"Nimmo","year":"2003","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2127","DOI":"10.1002\/pmic.201400073","article-title":"Phosphorylation-dependent regulation of plant chromatin and chromatin-associated proteins","volume":"14","author":"Bigeard","year":"2014","journal-title":"Proteomics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2054","DOI":"10.1016\/j.biochi.2011.05.019","article-title":"Calcium decoding mechanisms in plants","volume":"93","author":"Hashimoto","year":"2011","journal-title":"Biochimie"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Zhai, Q., Yan, L., Tan, D., Chen, R., Sun, J., Gao, L., Dong, M.Q., Wang, Y., and Li, C. (2013). Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLoS Genet., 9.","DOI":"10.1371\/journal.pgen.1003422"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1111\/jipb.12096","article-title":"Phosphorylation-dependent trafficking of plasma membrane proteins in animal and plant cells","volume":"55","author":"Offringa","year":"2013","journal-title":"J. Integr. Plant Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1034\/j.1399-3054.1995.930125.x","article-title":"Stress-induced degradation of the photosynthetic apparatus is accompanied by changes in thylakoid protein turnover and phosphorylation","volume":"93","author":"Dannehl","year":"1995","journal-title":"Physiol. Plantarum"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/j.1399-3054.1994.tb02964.x","article-title":"The effect of phosphate deficiency on carbohydrate metabolism in bean roots","volume":"91","author":"Rychter","year":"1994","journal-title":"Physiol. Plantarum"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/j.tplants.2012.06.008","article-title":"Phosphorylation in the plant circadian system","volume":"17","author":"Kusakina","year":"2012","journal-title":"Trends Plant Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/S1360-1385(02)02255-0","article-title":"Towards genomic and proteomic studies of protein phosphorylation in plant\u2013pathogen interactions","volume":"7","author":"Xing","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.tplants.2014.10.001","article-title":"Mitogen-activated protein kinase cascades in signaling plant growth and development","volume":"20","author":"Xu","year":"2015","journal-title":"Trends Plant Sci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"585","DOI":"10.3389\/fpls.2015.00585","article-title":"Long-term boron-deficiency-responsive genes revealed by cDNA-AFLP differ between Citrus sinensis roots and leaves","volume":"6","author":"Lu","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1093\/pcp\/pcp179","article-title":"Boron nutrition of cultured tobacco BY-2 cells. VI. Calcium is involved in early responses to boron deprivation","volume":"51","author":"Koshiba","year":"2010","journal-title":"Plant Cell Physiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3207","DOI":"10.1007\/s11738-014-1687-5","article-title":"Transcriptome responses to phosphate deficiency in Poncirus trifoliata (L.) Raf","volume":"36","author":"Bai","year":"2014","journal-title":"Acta Physiol. Plant."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1007\/s11104-015-2657-4","article-title":"Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing","volume":"398","author":"Zeng","year":"2016","journal-title":"Plant Soil"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.ceca.2014.02.011","article-title":"Whole genome transcriptome analysis of rice seedling reveals alterations in Ca2+ ion signaling and homeostasis in response to Ca2+ deficiency","volume":"55","author":"Shankar","year":"2014","journal-title":"Cell Calcium"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.jplph.2012.11.017","article-title":"GsSRK, a G-type lectin S-receptor-like serine\/threonine protein kinase, is a positive regulator of plant tolerance to salt stress","volume":"170","author":"Sun","year":"2013","journal-title":"J. Plant Physiol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Zhao, J., Gao, Y., Zhang, Z., Chen, T., Guo, W., and Zhang, T. (2013). A receptor-like kinase gene (GbRLK) from Gossypium barbadense enhances salinity and drought-stress tolerance in Arabidopsis. BMC Plant Biol., 13.","DOI":"10.1186\/1471-2229-13-110"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1007\/s11103-012-9952-8","article-title":"Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice","volume":"80","author":"Vaid","year":"2012","journal-title":"Plant Mol. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.1105\/tpc.022574","article-title":"A multidrug resistance\u2013associated protein involved in anthocyanin transport in Zea mays","volume":"16","author":"Goodman","year":"2004","journal-title":"Plant Cell"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1146\/annurev.arplant.54.031902.135023","article-title":"Chloroplast movement","volume":"54","author":"Wada","year":"2003","journal-title":"Ann. Rev. Plant Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1105\/tpc.113.122358","article-title":"Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis","volume":"26","author":"Hao","year":"2014","journal-title":"Plant Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/s00425-010-1294-7","article-title":"Microarray analysis of Arabidopsis plants in response to allelochemical L-DOPA","volume":"233","author":"Golisz","year":"2011","journal-title":"Planta"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1104\/pp.107.1.1","article-title":"The biochemistry and molecular biology of isoprenoid metabolism","volume":"107","author":"Chappell","year":"1995","journal-title":"Plant Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1093\/mp\/sss088","article-title":"New insights into plant isoprenoid metabolism","volume":"5","author":"Pulido","year":"2012","journal-title":"Mol. Plant"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1111\/j.1399-3054.1997.tb01049.x","article-title":"Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants","volume":"101","author":"Lichtenthaler","year":"1997","journal-title":"Physiol. Plantarum"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1093\/mp\/sss015","article-title":"Structure and dynamics of the isoprenoid pathway network","volume":"5","author":"Coman","year":"2012","journal-title":"Mol. Plant"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1042\/bj1460223","article-title":"Role of glycerol 3-phosphate dehydrogenase in glyceride metabolism. Effect of diet on enzyme activities in chicken liver","volume":"146","author":"Harding","year":"1975","journal-title":"Biochem. J."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1111\/pce.12348","article-title":"UV-B mediated metabolic rearrangements in poplar revealed by non-targeted metabolomics","volume":"38","author":"Kaling","year":"2015","journal-title":"Plant Cell Environ."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.tplants.2009.12.006","article-title":"Abiotic stresses and induced BVOCs","volume":"15","author":"Loreto","year":"2010","journal-title":"Trends Plant Sci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1111\/pce.12666","article-title":"Lipid signalling in plant responses to abiotic stress","volume":"39","author":"Hou","year":"2016","journal-title":"Plant Cell Environ."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1887","DOI":"10.1105\/tpc.18.00347","article-title":"A lipase gene, HEAT INDUCIBLE LIPASE1, is involved in remodeling chloroplastic monogalactosyldiacylglycerol by liberating \u03b1-linolenic acid in Arabidopsis leaves under heat stress","volume":"30","author":"Higashi","year":"2018","journal-title":"Plant Cell"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.jplph.2015.12.002","article-title":"Legume nodules from nutrient-poor soils exhibit high plasticity of cellular phosphorus recycling and conservation during variable phosphorus supply","volume":"191","author":"Vardien","year":"2016","journal-title":"J. Plant Physiol."},{"key":"ref_85","first-page":"1154","article-title":"Proteomic response of Hordeum vulgare cv. Tadmor and Hordeum marinum to salinity stress: Similarities and differences between a glycophyte and a halophyte","volume":"7","author":"Hynek","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"An, D., Yang, J., and Zhang, P. (2012). Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genom., 13.","DOI":"10.1186\/1471-2164-13-64"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"11934","DOI":"10.1073\/pnas.0505266102","article-title":"A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation","volume":"102","author":"Misson","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"201","DOI":"10.3389\/fpls.2016.00201","article-title":"MicroRNA regulatory mechanisms on Citrus sinensis leaves to magnesium-deficiency","volume":"7","author":"Ma","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1104\/pp.006080","article-title":"Activation of phospholipases c and d is an early response to a cold exposure in Arabidopsis suspension cells","volume":"130","author":"Ruelland","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3903","DOI":"10.1073\/pnas.92.9.3903","article-title":"A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana","volume":"92","author":"Hirayama","year":"1995","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1111\/j.1365-313X.2010.04136.x","article-title":"Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance","volume":"62","author":"Vossen","year":"2010","journal-title":"Plant J."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1073\/pnas.0912930107","article-title":"Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation","volume":"107","author":"Sohlenkamp","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s00468-018-1766-0","article-title":"Magnesium deficiency affects secondary lignification of the vascular system in Citrus sinensis seedlings","volume":"33","author":"Huang","year":"2019","journal-title":"Trees"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1007\/s11105-010-0284-z","article-title":"Genome-wide analysis of fatty acid desaturases in soybean (Glycine max)","volume":"29","author":"Chi","year":"2011","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1104\/pp.112.210450","article-title":"Arabidopsis 3-ketoacyl-CoA synthase 9 is involved in the synthesis of tetracosanoic acids as precursors of cuticular waxes, suberins, sphingolipids, and phospholipids","volume":"162","author":"Kim","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1007\/s11104-018-3658-x","article-title":"Magnesium deficiency damages the youngest mature leaf in rice through tissue-specific iron toxicity","volume":"428","author":"Kobayashi","year":"2018","journal-title":"Plant Soil"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1105\/tpc.111.083485","article-title":"The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis","volume":"23","author":"Seo","year":"2011","journal-title":"Plant Cell"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.gene.2014.07.053","article-title":"Identification of differentially expressed genes in flax (Linum usitatissimum L.) under saline\u2013alkaline stress by digital gene expression","volume":"549","author":"Yu","year":"2014","journal-title":"Gene"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1111\/ppl.12353","article-title":"Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba","volume":"156","author":"Li","year":"2016","journal-title":"Physiol. Plantarum"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1038\/nature08122","article-title":"Recent advances and emerging trends in plant hormone signalling","volume":"459","author":"Santner","year":"2009","journal-title":"Nature"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.plaphy.2013.09.011","article-title":"Current understanding on ethylene signaling in plants: The influence of nutrient availability","volume":"73","author":"Iqbal","year":"2013","journal-title":"Plant Physiol. Biochem."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.3389\/fpls.2017.01358","article-title":"Transcriptional regulation of aluminum-tolerance genes in higher plants: Clarifying the underlying molecular mechanisms","volume":"8","author":"Daspute","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_103","doi-asserted-by":"crossref","unstructured":"Gui, J., Luo, L., Zhong, Y., Sun, J., Umezawa, T., and Li, L. (2019). Phosphorylation of LTF1, a MYB transcription factor in populus, acts as a sensory switch regulating lignin biosynthesis in wood cells. Mol. Plant.","DOI":"10.1016\/j.molp.2019.05.008"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1111\/j.1399-3054.2012.12003.x","article-title":"Leaf senescence in rice due to magnesium deficiency mediated defect in transpiration rate before sugar accumulation and chlorosis","volume":"148","author":"Kobayashi","year":"2013","journal-title":"Physiol. Plantarum"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.semcdb.2017.08.005","article-title":"Functional dissection and transport mechanism of magnesium in plants","volume":"74","author":"Chen","year":"2018","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"2234","DOI":"10.1105\/tpc.114.124628","article-title":"Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation","volume":"26","author":"Mao","year":"2014","journal-title":"Plant Cell"},{"key":"ref_107","first-page":"489","article-title":"An extraction procedure of plant materials for the rapid determination of Mn, Cu, Zn and Mg by the atomic absorption analysis","volume":"39","author":"Kushizaki","year":"1968","journal-title":"J. Sci. Soil Manure"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1104\/pp.60.3.379","article-title":"Enzymic assay of 10\u22127 to 10\u221214 moles of sucrose in plant tissues","volume":"60","author":"Jones","year":"1977","journal-title":"Plant Physiol."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.ecoenv.2018.07.028","article-title":"Proteome profile analysis of boron-induced alleviation of aluminum-toxicity in Citrus grandis roots","volume":"162","author":"Yang","year":"2018","journal-title":"Ecotox. Environ. Saf."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1007\/s004250050524","article-title":"Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds","volume":"207","author":"Hodges","year":"1999","journal-title":"Planta"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1002\/jsfa.2740230405","article-title":"A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops","volume":"23","author":"Morrison","year":"1972","journal-title":"J. Sci. Food Agric."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"R36","DOI":"10.1186\/gb-2013-14-4-r36","article-title":"TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions","volume":"14","author":"Kim","year":"2013","journal-title":"Genome Biol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/nmeth.1226","article-title":"Mapping and quantifying mammalian transcriptomes by RNA-Seq","volume":"5","author":"Mortazavi","year":"2008","journal-title":"Nat. Methods"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"D480","DOI":"10.1093\/nar\/gkm882","article-title":"KEGG for linking genomes to life and the environment","volume":"36","author":"Kanehisa","year":"2008","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/13\/3129\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:01:32Z","timestamp":1760187692000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/13\/3129"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,6,26]]},"references-count":114,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2019,7]]}},"alternative-id":["ijms20133129"],"URL":"https:\/\/doi.org\/10.3390\/ijms20133129","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,6,26]]}}}