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Metabolic analysis reveals temporal changes in C/N metabolites and senescence of flag leaf in wheat during grain filling

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Abstract

Flag leaves have been considered to be the first key organ contributing to higher yields in triticeae crops. Therefore, dynamical changes in physiological metabolisms in flag leaves are important to regulate senescence and provide reserves to the developing grains. In this study, the dynamic changes in contents of metabolites in flag leaves during grain filling of wheat (Triticum aestivum L.) were analyzed using non-targeted liquid chromatography–mass spectrometry. Metabolic profiling was conducted at Zadoks 69, Zadoks 75, Zadoks 83 and Zadoks 87 stages. In total, 126 metabolites were annotated over the grain-filling period. Metabolic analysis showed that the annotated metabolites were involved in the carbon and nitrogen metabolisms, regulation of senescence, antioxidant metabolism to resist mainly drought and hot stresses. In the metabolic pathway of carbohydrate metabolism, glucose, gluconic acid and pyruvate changed significantly during grain filling; in the amino acid (AA) metabolism, most AAs annotated showed the highest concentrations at the anthesis or Zadoks 75 stages and then gradually decreased; and α-Linolenic acid metabolism pathway may be involved in the modification of leaf mechanical strength, extension angle and light reception for photosynthesis; generally, the jasmonate content was gradually increased, showing the highest values at the Zadoks 87 stage; whereas the high content of phenols was observed at earlier two stages, followed by a gradually decrease. Based on the analysis on the functions of annotated metabolites, we conclude that these pathways might be of very importance for wheat to construct stress-resistant metabolism, regulate leaf senescence and remobilization of leaf reserves to filling grain.

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References

  • Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahmad I, Kamran M, Ali S, Bilegjargal B, Cai T, Ahmad S, Meng X, Su W, Liu T, Han Q (2018) Uniconazole application strategies to improve lignin biosynthesis, lodging resistance and production of maize in semiarid regions. Field Crops Res 222:66–77

    Article  Google Scholar 

  • Ahrar M, Doneva D, Koleva D, Romanod A, Rodeghiero M, Tsonev T, Biasioli F, Stefanova M, Peeva V, Wohlfahrt G, Loreto F, Varotto C, Velikova V (2015) Isoprene emission in the monocot Arundineae tribe in relation to functional and structural organization of the photosynthetic apparatus. Environ Exp Bot 119:87–95

    Article  CAS  Google Scholar 

  • Aidoo MK, Bdolach E, Fait A, Lazarovitch N, Rachmilevitch S (2016) Tolerance to high soil temperature in foxtail millet (Setaria italica L.) is related to shoot and root growth and metabolism. Plant Physiol Bioch 106:73–81

    Article  CAS  Google Scholar 

  • Akhter D, Qin R, Nath UK, Alamin M, Jin X, Shi C (2018) The brown midrib leaf (bml) mutation in rice (Oryza sativa L.) causes premature leaf senescence and the induction of defense responses. Genes 9:203

    Article  PubMed Central  Google Scholar 

  • Al-Reza SM, Rahman A, Sattar MA, Rahman MO, Fida HM (2010) Essential oil composition and antioxidant activities of Curcuma aromatica Salisb. Food Chem Toxicol 48:1757–1760

    Article  CAS  PubMed  Google Scholar 

  • Anjum SA, Wang L, Farooq M, Khan I, Xue L (2011) Methyl jasmonate-induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought. J Agron Crop Sci 197:296–301

    Article  CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Tung SA, Samad RA, Wang L, Khan I, ur Rehman N, Shah AN, Shahzad B (2016) Exogenously applied methyl jasmonate improves the drought tolerance in wheat imposed at early and late developmental stages. Acta Physiol Plant 38:25

  • Ansari MI, Lee RH, Chen SCG (2005) A novel senescence-associated gene encoding γ-aminobutyric acid (GABA):pyruvate transaminase is upregulated during rice leaf senescence. Physiol Plant 123:1–8

    Article  CAS  Google Scholar 

  • Barunawati N, Giehl RFH, Bauer B (2013) The influence of inorganic nitrogen fertilizer forms on micronutrient retranslocation and accumulation in grains of winter wheat. Front Plant Sci 4:320

    Article  PubMed  PubMed Central  Google Scholar 

  • Bollina V, Kumaraswamy G, Kushalappa AC, Choo TM, Dion Y, Rioux S, Faubert D, Hamzehzarghani H (2010) Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Mol Plant Pathol 11(6):769–782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brückner K, Božió D, Manzano D, Papaefthimiou D, Pateraki I, Scheler U, Ferrer A, de Vos RCH, Kanellis AK, Tissier A (2014) Characterization of two genes for the biosynthesis of abietane-type diterpenes in rosemary (Rosmarinus officinalis) glandular trichomes. Phytochemistry 101:52–64

    Article  PubMed  Google Scholar 

  • Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  Google Scholar 

  • Chen YT, Li XJ, Zao BL, Zheng RL, Xin WJ (1989) ESR study of the scavenging effect of natural products of rutin etc on superoxide and hydroxyl radical. Acta Bioph Sin 5:235–240

    Google Scholar 

  • Christiansen MW, Holm PB, Gregersen PL (2011) Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggests conserved functions compared to both monocots and dicots. BMC Res Notes 4:302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187

    Article  CAS  PubMed  Google Scholar 

  • Coruzzi G, Last R, Dudareva N, Amrhein N (2015) Amino Acids In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and Molecular Biology of Plants, 2nd edn, pp 289–337

  • Curci PL, Cigliano RA, Zuluaga DL, Janni M, Sanseverino W, Sonnante G (2017) Transcriptomic response of durum wheat to nitrogen starvation. Sci Rep 7:1176

    Article  PubMed  PubMed Central  Google Scholar 

  • Deshpande P, Dapkekar A, Oak M, Paknikar K, Rajwade J (2018) Nanocarrier-mediated foliar zinc fertilization influences expression of metal homeostasis related genes in flag leaves and enhances gluten content in durum wheat. PLoS One 13(1):e0191035

  • Díaz-Benito P, Banakar R, Rodríguez-Menéndez S, Capell T, Pereiro R, Christou P, Abadía J, Fernández B, Álvarez-Fernández A (2018) Iron and zinc in the embryo and endosperm of rice (Oryza sativa L.) seeds in contrasting 2’-deoxymugineic acid/nicotianamine scenarios. Front Plant Sci 9:1190

    Article  PubMed  PubMed Central  Google Scholar 

  • Dieumou FE, Teguia A, Kuiate JR, Tamokou JD, Fonge NB, Donogmo MC (2009) Effect of ginger (Zingiber officinale) and garlic (Allium sativum) essential oils on growth performance and gut microbial population of broiler chicks. Livestock Res Rural Dev 21:21–33

    Google Scholar 

  • Eagling T, Neal AL, McGrath SP, Fairweather-Tait S, Shewry PR, Zhao FJ (2014) Distribution and speciation of iron and zinc in grain of two wheat genotypes. J Agr Food Chem 62:708–716

    Article  CAS  Google Scholar 

  • Farooq M, Nawaz A, Chaudhry MAM, Indrasti R, Rehman A (2017a) Improving resistance against terminal drought in bread wheat by exogenous application of proline and gamma-aminobutyric acid. J Agron Crop Sci 203:464–472

    Article  CAS  Google Scholar 

  • Farooq M, Rizwan M, Nawaz A, Rehman A, Ahmad R (2017b) Application of natural plant extracts improves the tolerance against combined terminal heat and drought stresses in bread wheat. J Agron Crop Sci 203:528–538

    Article  CAS  Google Scholar 

  • Fourcroy P, Siso-Terraza P, Sudre D, Saviron M, Reyt G, Gaymard F, Abadía A, Abadia J, Álvarez-Fernández A, Briat J (2013) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–167

    Article  PubMed  Google Scholar 

  • Gao Z, Liang XG, Zhang L, Lin S, Zhao X, Zhou LL, Shen S, Zhou SL (2017) Spraying exogenous 6-benzyladenine and brassinolide at tasseling increases maize yield by enhancing source and sink capacity. Field Crops Res 211:1–9

    Article  Google Scholar 

  • Gladun I, Karpov E (1993) Distribution of assimilates from the flag leaf of rice during the reproductive period of development. Russia J Plant Physl 40:215–218

    Google Scholar 

  • Haworth M, Catola S, Marino G, Brunetti C, Michelozzi M, Riggi E, Avola G, Cosentino SL, Loreto F, Centritto M (2017a) Moderate drought stress induces increased foliar dimethylsulphoniopropionate (DMSP) concentration and isoprene emission in two contrasting ecotypes of Arundo donax. Front Plant Sci 8:1016

    Article  PubMed  PubMed Central  Google Scholar 

  • Haworth M, Cosentino SL, Marino G, Brunetti C, Scordia D, Testa G, Riggi E, Avola G, Centritto M (2017b) Physiological responses of Arundo donax ecotypes to drought: a common garden study. Gcb Bioenergy 9:132–143

    Article  CAS  Google Scholar 

  • He Y, Fukushige H, Hildebrand D, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hein JA, Sherrard ME, Manfredi KP, Abebe T (2016) The fifth leaf and spike organs of barley (Hordeum vulgare L.) display different physiological and metabolic responses to drought stress. BMC Plant Biol 16:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Heyneke E, Watanabe M, Erban A, Duan G, Buchner P, Walther D, Kopka J, Hawkesford MJ, Hoefgen R (2017) Characterization of the wheat leaf metabolome during grain filling and under varied N-supply. Front Plant Sci 8:2048

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu T, Liu SQ, Amombo E, Fu JM (2015) Stress memory induced rearrangements of HSP transcription, photosystem II photochemistry and metabolism of tall fescue (Festuca arundinacea Schreb) in response to high-temperature stress. Front Plant Sci 6:403

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu C, Tohge T, Chan SA, Song Y, Rao J, Cui B, Lin H, Wang L, Fernie AR, Zhang D, Shi J (2016) Identification of conserved and diverse metabolic shifts during rice grain development. Sci Rep 6:20942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang XH, Chen QX, Wang Q et al (2006) Inhibition of the activity of mushroom tyrosinase by alkylbenzoic acids. Food Chem 94:1–6

    Article  CAS  Google Scholar 

  • Huang S, Zhang J, Wang L, Song KK, Wang J, Sha L, Guana X (2013) Effect of abiotic stress on the abundance of different vitamin B6 vitamers in tobacco plants. Plant Physiol Biochem 66:63–67

    Article  CAS  PubMed  Google Scholar 

  • Hura T, Grzesiak S, Hura K, Thiemt E, Tokarz K, Wędzony M (2007) Physiological and biochemical tools in drought-tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann Bot 100:767–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • John RA (1995) Pyridoxal phosphate-dependent enzymes. Biochem Biophys Acta 1248:81–96

    PubMed  Google Scholar 

  • Jugran AK, Bahukhandi A, Bhatt ID, Rawal RS, Nandi SK (2017) Hydrogen peroxide induced deoxyribonucleic acid damage preventive activity of selected Valeriana species from west Himalaya. P Natl A Sci India 87:59–65

    CAS  Google Scholar 

  • Kamran M, Ahmad I, Wu X, Liu T, Ding R, Han Q (2018a) Application of paclobutrazol: a strategy for inducing lodging resistance of wheat through mediation of plant height, stem physical strength, and lignin biosynthesis. Environ Sci Pollut Res 25:29366–29378

    Article  CAS  Google Scholar 

  • Kamran M, Cui W, Ahmad I, Meng X, Zhang X, Su W, Chen J, Ahmad S, Fahad S, Han Q, Liu T (2018b) Effect of paclobutrazol, a potential growth regulator on stalk mechanical strength, lignin accumulation and its relation with lodging resistance of maize. Plant Growth Regul 84:317–332

    Article  CAS  Google Scholar 

  • Kang GZ, Li GZ, Liu GQ, Xu W, Peng XQ (2013) Wang CY Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. Biol Plant 57:718–724

    Article  CAS  Google Scholar 

  • Kikuzaki H, Nakatani N (1996) Cyclic diarylheptanoids from rhizomes of Zinnger officinale. Phytochemistry 43:273–277

    Article  CAS  Google Scholar 

  • Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ (2009) Kim JK Methyl Jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol 149:1751–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohl S, Hollmann J, Erban A, Kopka J, Riewe D, Weschke W, Weber H (2015) Metabolic and transcriptional transitions in barley glumes reveal a role as transitory resource buffers during endosperm filling. J Exp Bot 66:1397–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong LA, Sun MZ, Wang FH, Liu J, Feng B, Si JS, Zhang B, Li SD, Li HW (2014) Effects of high NH4+ on K+ uptake, culm mechanical strength and grain filling in wheat. Front Plant Sci 5:703

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong LA, Sun M, Xie Y, Wang F, Zhao Z (2015) Photochemical and antioxidative responses of the glume and flag leaf to seasonal senescence in wheat. Front Plant Sci 6:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong LA, Xie Y, Hu L, Feng B, Li SD (2016) Remobilization of vegetative nitrogen to developing grain in wheat (Triticum aestivum L). Field Crops Res 196:134–144

    Article  Google Scholar 

  • Kong LA, Xie Y, Hu L, Si J, Wang ZS (2017) Excessive nitrogen application dampens antioxidant capacity and grain filling in wheat as revealed by metabolic and physiological analyses. Sci Rep 7:43363

    Article  PubMed  PubMed Central  Google Scholar 

  • Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusaba M, Tanaka A, Tanaka R (2013) Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynth Res 117:221–234

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2016) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in creeping bentgrass (Agrostis stolonifera). Sci Rep 6:30338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2017) Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). Physiol Plant 159:42–58

    Article  CAS  PubMed  Google Scholar 

  • Li K, Wen W, Alseekh S, Yang X, Guo H, Li W, Wang L, Pan Q, Zhan W, Liu J, Li Y, Wu X, Brotman Y, Willmitzer L, Li J, Fernie AR, Yan J (2019) Large-scale metabolite quantitative trait locus analysis provides new insights for high-quality maize improvement. Plant J 99:216–230

    CAS  PubMed  Google Scholar 

  • Lim YY, Lim TT, Tee JJ (2007) Antioxidant properties of several tropical fruits: A comparative study. Food Chem 103:1003–1008

    Article  CAS  Google Scholar 

  • Liu L, Li H, Zeng H, Cai Q, Zhou X, Yin C (2016) Exogenous jasmonic acid and cytokinin antagonistically regulate rice flag leaf senescence by mediating chlorophyll degradation, membrane deterioration, and senescence-associated genes expression. J Plant Growth Regul 35:366–376

    Article  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. J Plant Physiol 127:1781–1787

    Article  CAS  Google Scholar 

  • Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–51

    Article  CAS  Google Scholar 

  • Masek A, Chrzescijanska E, Latos M, Zaborski M (2017) Influence of hydroxyl substitution on flavanone antioxidants properties. Food Chem 215:501–507

    Article  CAS  PubMed  Google Scholar 

  • McIntyre CL, Casu RE, Rattey A, Dreccer MF, Kam JW, van Herwaarden AF, Shorter R, Xue GP (2011) Linked gene networks involved in nitrogen and carbon metabolism and levels of water-soluble carbohydrate accumulation in wheat stems. Funct Integra Geno 11:585–597

    Article  CAS  Google Scholar 

  • Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B (2012) Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot 63:1315–1328

    Article  CAS  PubMed  Google Scholar 

  • Molnar M, Jerković I, Suknović D, Rajs BB, Aladić K, Šubarić D, Jokić S (2017) Screening of six medicinal plant extracts obtained by two conventional methods and supercritical CO2 extraction targeted on coumarin content, 2,2-Diphenyl-1-picrylhydrazyl radical scavenging capacity and total phenols content. Molecules 22:348

    Article  PubMed Central  Google Scholar 

  • Mori S, Nishizawa N, Hayashi H, Chino M, Yoshimura E, Ishihara J (1991) Why are young rice plants highly susceptible to iron deficiency. Iron nutrition and interactions in plants. Springer, Dordrecht, pp 175–188

    Chapter  Google Scholar 

  • Munné-Bosch S, Alegre L (2001) Subcellular compartmentation of the diterpene carnosic acid and its derivatives in the leaves of rosemary. Plant Physiol 125:1094–1102

    Article  PubMed  PubMed Central  Google Scholar 

  • Nam KH, Shin HJ, Pack IS, Park JH, Kim HB, Kim CG (2016) Metabolomic changes in grains of well-watered and drought-stressed transgenic rice. J Sci Food Agr 96:807–814

    Article  CAS  Google Scholar 

  • Narayanan S, Tamura PJ, Roth MR, Prasad PVV, Welti R (2016) Wheat leaf lipids during heat stress: I High day and night temperatures result in major lipid alterations. Plant Cell Environ 39:787–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishiyama R, Kato M, Nagata S, Yanagisawa S, Yoneyama T (2012) Identification of Zn-nicotianamine and Fe-2’-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L). Plant Cell Physiol 53:381–390

    Article  CAS  PubMed  Google Scholar 

  • Obata T, Witt S, Lisec Y, Palacios-Rojas N, Flores-Saraza I, Yousfi S, Araus JL, Cairns JE, Fernie AR (2015) Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 169:2665–2683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearce S, Tabbita F, Cantu D, Buffalo V, Avni R, Vazquez-Gross H, Zhao R, Conley CJ, Distelfeld A, Dubcovksy J (2014) Regulation of zinc and Fe transporters by the GpcB1 gene during early wheat monocarpic senescence. BMC Plant Biol 14:368

    Article  PubMed  PubMed Central  Google Scholar 

  • Pollastri S, Tsonev T, Loreto F (2014) Isoprene improves photochemical efficiency and enhances heat dissipation in plants at physiological temperatures. J Exp Bot 65:1565–1570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568

    Article  CAS  PubMed  Google Scholar 

  • Qi T, Wang J, Huang H, Liu B, Gao H, Liu Y (2015) Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis. Plant Cell 27:1634–1649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin X, Zeevaart JA (2002) Overexpression of a 9-cisepoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208

    Article  CAS  PubMed  Google Scholar 

  • Rao IS, Neeraja CN, Srikanth B, Subrahmanyam D, Swamy KN, Rajesh K, Vijayalakshmi P, Vishnu Kiran T, Sailaja N, Revathi P, Rao PR, Rao LVS, Surekha K, Babu VR, Voleti SR (2018) Identification of rice landraces with promising yield and the associated genomic regions under low nitrogen. Sci Rep 8:9200

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy KK, Ravinder T, Prasad RBN, Kanjilal S (2011) Evaluation of the antioxidant activity of capsiate analogues in polar, nonpolar, and micellar media. J Agr Food Chem 59:564–569

    Article  CAS  Google Scholar 

  • Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA (2018) Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind Crop Prod 112:741–748

    Article  CAS  Google Scholar 

  • Rossato L, Le Dantec C, Laine P, Ourry A (2002a) Nitrogen storage and remobilization in Brassica napus L during the growth cycle: identification, characterization and immunolocalization of a putative taproot storage glycoprotein. J Exp Bot 53:265–275

    Article  CAS  PubMed  Google Scholar 

  • Rossato L, MacDuff JH, Laine P, Le Deunff E, Ourry A (2002b) Nitrogen storage and remobilization in Brassica napus L during the growth cycle: effects of methyl jasmonate on nitrate uptake, senescence, growth, and VSP accumulation. J Exp Bot 53:1131–1141

    Article  CAS  PubMed  Google Scholar 

  • Rossi M, Bermudez L, Carrari F (2015) Crop yield: challenges from a metabolic perspective. Curr Opin Plant Biol 25:79–89

    Article  CAS  PubMed  Google Scholar 

  • Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD (2005) Effect of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277

    Article  CAS  Google Scholar 

  • Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769

    Article  CAS  Google Scholar 

  • Sharma M, Jain UK, Patel A, Gupta N (2010) A comprehensive pharmacognostic report on valerian. Int J Pharmaceuticul Sci Res 1:6–40

    Google Scholar 

  • Sharma M, Gupta SK, Majumder B, Maurya VK, Deeba F, Alam A, Pandey V (2017) Salicylic acid mediated growth, physiological and proteomic responses in two wheat varieties under drought stress. J Proteomics 163:28–51

    Article  CAS  PubMed  Google Scholar 

  • Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of glycine betaine in rice plants that over express choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98:565–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siddhuraju P, Becker K (2003) Antioxidant properties of various solvent extracts of total phenolic constituents from three different agroclimatic origins of drumstick tree (Moringa oleifera Lam) leaves. J Agr Food Chem 51:2144–2155

    Article  CAS  Google Scholar 

  • Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2008) Deoxymugineic acid increases Zn translocation in Zn deficient rice plants. Plant Mol Biol 66:609–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaki H, Reguera M, Abdel-Tawab YM, Takebayashi Y, Kasahara H, Blumwald E (2015) Targeting hormone-related pathways to improve grain yield in rice: a chemical approach. PLoS One 10(6): e0131213

  • Taylor IB, Burbidage A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51:1563–1574

    Article  CAS  PubMed  Google Scholar 

  • Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53

    Article  PubMed  Google Scholar 

  • Templer SE, Ammon A, Pscheidt D, Ciobotea O, Schuy C, McCollum C, Sonnewald U, Hanemann A, Föster J, Ordon F, von Korff M, Voll LM (2017) Metabolite profiling of barley flag leaves under drought and combined heat and drought stress reveals metabolic QTLs for metabolites associated with antioxidant defense. J Exp Bot 68(7):1697–1713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas H, Ougham H (2014) The stay-green trait. J Exp Bot 65:3889–3900

    Article  CAS  PubMed  Google Scholar 

  • Trijatmiko KR, Dueñas C, Tsakirpaloglou N, Torrizo L, Arines FM, Adeva C et al (2016) Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci Rep 6:19792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: Finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362–15367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda J, Kato J (1980) Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiol 66:246–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Saskia CM, Wees V, Pieterse CMJ (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761

    Article  PubMed  PubMed Central  Google Scholar 

  • Velikova V, Várkonyi Z, Szabó M, Maslenkova L, Nogues I, Kovács L, Peeva V, Busheva M, Garab G, Sharkey TD, Loreto F (2011) Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiol 157:905–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Peeva V, Busheva M, Garab G, Sharkey TD, Loreto F (2009) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531

    Article  CAS  PubMed  Google Scholar 

  • Wei H, Meng T, Li X, Dai Q, Zhang H, Yin X (2018) Sink-source relationship during rice grain filling is associated with grain nitrogen concentration. Field Crops Res 215:23–38

    Article  Google Scholar 

  • Woo HR, Kim HJ, Lim PO, Nam HG (2019) Leaf senescence: systems and dynamics aspects. Annu Rev Plant Biol 70:347–376

    Article  CAS  PubMed  Google Scholar 

  • Xue J, Balamurugan S, Li DW, Liu YH, Zeng H, Wang L, Yang WD, Liu JS, Li HY (2017) Glucose-6-phosphate dehydrogenase as a target for highly efficient fatty acid biosynthesis in microalgae by enhancing NADPH supply. Metab Eng 41:212–221

    Article  CAS  PubMed  Google Scholar 

  • Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51:795–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama T, Ishikawa S, Fujimaki S (2015) Route and regulation of Zinc, Cadmium, and iron transport in rice plants (Oryza sativa L) during vegetative growth and grain filling: metal transporters, metal speciation, grain Cd reduction and Zn and Fe biofortification. Int J Mol Sci 16:19111–19129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You J, Hu H, Xiong L (2012) An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci 197:59–69

    Article  CAS  PubMed  Google Scholar 

  • Yu SM, Lo SF, Ho THD (2015) Source-sink communication: regulated by hormone, nutrient, and stress cross-signaling. Trends Plant Sci 20:844–857

    Article  CAS  PubMed  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhang L, Zhang X, Fan S (2017a) Meta-analysis of salt-related gene expression profiles identifies common signatures of salt stress responses in Arabidopsis. Plant Syst Evol 303:757–774

    Article  CAS  Google Scholar 

  • Zhang Y, Ma X, Wang X, Liu J, Huang B, Guo X, Xiong S, La GX (2017b) UPLC-QTOF analysis reveals metabolomic changes in the flag leaf of wheat (Triticum aestivum L) under low-nitrogen stress. Plant Physiol Biochem 111:30–38

    Article  CAS  PubMed  Google Scholar 

  • Zhang CX, Feng BH, Chen TT, Fu WM, Li HB, Li GY, Jin QY, Tao LX, Fu GF (2018) Heat stress-reduced kernel weight in rice at anthesis is associated with impaired source-sink relationship and sugars allocation. Environ Exp Bot 155:718–733

    Article  CAS  Google Scholar 

  • Zhang L, Zhang Z, Zhang X, Yao Y, Wang R, Duan B, Fan SJ et al (2019) Comprehensive meta-analysis and co-expression network analysis identify candidate genes for salt stress response in Arabidopsis. Plant Biosyst 153:367–377

    Article  Google Scholar 

  • Zhen S, Dong K, Deng X, Zhou J, Xu X, Han C, Zhang W, Xu Y, Wang Z, Yan Y (2016) Dynamic metabolome profiling reveals significant metabolic changes during grain development of bread wheat (Triticum aestivum L.). J Sci Food Agri 96(11):3731–3740

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Key R & D Program of China (2017YFD03002), the National Natural Science Foundation of China (31801282), the Natural Science Foundation of Shandong Province (ZR2020MC087), and the Shandong Modern Agricultural Technology and Industry System (SDAIT-01-06). The authors would thank Shanghai Sensichip Infotech Co. Ltd. for their technological assistance with metabolic analysis.

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Zhang, Y., Du, W., Zhang, Y. et al. Metabolic analysis reveals temporal changes in C/N metabolites and senescence of flag leaf in wheat during grain filling. Acta Physiol Plant 43, 104 (2021). https://doi.org/10.1007/s11738-021-03272-8

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