Metabolic signatures of Arabidopsis thaliana abiotic stress responses elucidate patterns in stress priming, acclimation, and recovery

Yuan Xu, Dana M. Freund, Adrian D. Hegeman, Jerry D. Cohen

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 11. DOI: 10.1007/s44154-022-00034-5
Original Paper

Metabolic signatures of Arabidopsis thaliana abiotic stress responses elucidate patterns in stress priming, acclimation, and recovery

Author information +
History +

Abstract

Temperature, water, and light are three abiotic stress factors that have major influences on plant growth, development, and reproduction. Plants can be primed by a prior mild stress to enhance their resistance to future stress. We used an untargeted metabolomics approach to examine Arabidopsis thaliana 11-day-old seedling’s abiotic stress responses including heat (with and without priming), cold (with and without priming), water-deficit and high-light before and after a 2-day-recovery period. Analysis of the physiological phenotypes showed that seedlings with stress treatment resulted in a reduction in fresh weight, hypocotyl and root length but remained viable. Several stress responsive metabolites were identified, confirmed with reference standards, quantified, and clustered. We identified shared and specific stress signatures for cold, heat, water-deficit, and high-light treatments. Central metabolism including amino acid metabolism, sugar metabolism, glycolysis, TCA cycle, GABA shunt, glutathione metabolism, purine metabolism, and urea cycle were found to undergo changes that are fundamentally different, although some shared commonalities in response to different treatments. Large increases in cysteine abundance and decreases in reduced glutathione were observed following multiple stress treatments highlighting the importance of oxidative stress as a general phenomenon in abiotic stress. Large fold increases in low-turnover amino acids and maltose demonstrate the critical role of protein and starch autolysis in early abiotic stress responses.

Keywords

Abiotic stress / Arabidopsis thaliana / LC-HRMS / Metabolomics / Plant stress acclimation / Priming / Recovery

Cite this article

Download citation ▾
Yuan Xu, Dana M. Freund, Adrian D. Hegeman, Jerry D. Cohen. Metabolic signatures of Arabidopsis thaliana abiotic stress responses elucidate patterns in stress priming, acclimation, and recovery. Stress Biology, 2022, 2(1): 11 https://doi.org/10.1007/s44154-022-00034-5

References

[1]
AlscherRG. Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant, 1989, 77: 457-464
CrossRef Google scholar
[2]
AvramovaZ. Transcriptional “memory” of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J, 2015, 83: 149-159
CrossRef Google scholar
[3]
BalmerA, PastorV, GamirJ, FlorsV, Mauch-ManiB. The “prime-ome”: towards a holistic approach to priming. Trends Plant Sci, 2015, 20(7):443-452
CrossRef Google scholar
[4]
Batista-SilvaW, HeinemannB, RugenN, Nunes-NesiA, AraújoWL, BraunmH-P, HildebrandtTM. The role of amino acid metabolism during abiotic stress release. Plant Cell Environ, 2019, 42: 1630-1644
CrossRef Google scholar
[5]
BoscaiuM, FitaA. Physiological and molecular characterization of crop resistance to abiotic stresses. Agron, 2020, 10: 1308
CrossRef Google scholar
[6]
CakmakI, MarschnerH. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol, 1992, 98: 1222-1227
CrossRef Google scholar
[7]
CaldanaC, DegenkolbeT, Cuadros-InostrozaA, KlieS, SulpiceR, LeisseA, SteinhauserD, FernieAR, WillmitzerL, HannahMA. High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant J, 2011, 67: 869-884
CrossRef Google scholar
[8]
CarreraFP, NocedaC, Maridueña-ZavalaMG, Cevallos-CevallosJM. Metabolomics, a powerful tool for understanding plant abiotic stress. Agronomy, 2021, 11(5):824
CrossRef Google scholar
[9]
ChambersMC, MacleanB, BurkeR, AmodeiD, RudermanDL, NeumannS, GattoL, FischerB, PrattB, EgertsonJ, HoffK, KessnerD, TasmanN, ShulmanN, FrewenB, BakerTA, BrusniakMY, PaulseC, CreasyD, FlashnerL, KaniK, MouldingC, SeymourSL, NuwaysirLM, LefebvreB, KuhlmannF, RoarkJ, RainerP, DetlevS, HemenwayT, HuhmerA, LangridgeJ, ConnollyB, ChadickT, HollyK, EckelsJ, DeutschEW, MoritzRL, KatzJE, AgusDB, MacCossM, TabbDL, MallickP. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol, 2012, 30: 918-920
CrossRef Google scholar
[10]
Chen W-P, Yang X-Y, Harms GL, Gray WM, Hegeman AD, Cohen JD (2011) An automated growth enclosure for metabolic labeling of Arabidopsis thaliana with 13C-carbon dioxide - an in vivo labeling system for proteomics and metabolomics research. Proteome Sci 9:–9. https://doi.org/10.1186/1477-5956-9-9
[11]
ChiangY, StushnoffC, McsayAE, JonesML, BohnertHJ. Overexpression of mannitol-1-phosphate dehydrogenase increases mannitol accumulation and adds protection against chilling injury in Petunia. J Am Soc Hort Sci, 2005, 130: 605-610
CrossRef Google scholar
[12]
ConrathU. Molecular aspects of defence priming. Trends Plant Sci, 2011, 16: 524-531
CrossRef Google scholar
[13]
CrispPA, GangulyD, EichtenSR, BorevitzJO, PogsonBJ. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv, 2016, 2: e1501340
CrossRef Google scholar
[14]
De OliveiraA. Abiotic and biotic stress in plants, 2019 London, UK IntechOpen
CrossRef Google scholar
[15]
Souza, D.P. De, Saunders, E.C., McConville, M.J. and Likić, V.A. (2006) Progressive peak clustering in GC-MS Metabolomic experiments applied to Leishmania parasites. Bioinformatics 22, 1391–1396. https://doi.org/10.1093/bioinformatics/btl085
[16]
DixonRA. Natural products and plant disease resistance. Nature, 2001, 411: 843-847
CrossRef Google scholar
[17]
DorionS, OuelletJC, RivoalJ. Glutathione metabolism in plants under stress: beyond reactive oxygen species detoxification. Metabolites, 2021, 11(9):641
CrossRef Google scholar
[18]
DreierW, SchnarrenbergerC, BörnerT. Light- and stress-dependent enhancement of amylolytic activities in white and green barley leaves: β-amylases are stress-induced proteins. J Plant Physiol, 1995, 145: 342-348
CrossRef Google scholar
[19]
EdelbrockC. Mixture model tests of hierarchical clustering algorithms: the problem of classifying everybody. Multivar Behav Res, 1979, 14: 367-384
CrossRef Google scholar
[20]
FanTW, ColmerTD, LaneAN, HigashiRM. Determination of metabolites by 1H NMR and GC: analysis for organic osmolytes in crude tissue extracts. Anal Biochem, 1993, 214: 260-271
CrossRef Google scholar
[21]
FirtzlaffV, OberländerJ, GeiselhardtS, HilkerM, KunzeR. Pre-exposure of Arabidopsis to the abiotic or biotic environmental stimuli “chilling” or “insect eggs” exhibits different transcriptomic responses to herbivory. Sci Rep, 2016, 6: 28544
CrossRef Google scholar
[22]
FosterJG, HessJL. Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol, 1980, 66: 482-487
CrossRef Google scholar
[23]
FoyerCH, LopezDelgadoH, DatJF, ScottIM. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant, 1997, 100: 241-254
CrossRef Google scholar
[24]
GamblePE, BurkeJJ. Effect of water-stress on the chloroplast antioxidant system .1. Alterations in glutathione-reductase activity. Plant Physiol, 1984, 76: 615-621
CrossRef Google scholar
[25]
GhatakA, ChaturvediP, WeckwerthW. Metabolomics in plant stress physiology. Adv Biochem Eng Biotechnol, 2018, 164: 187-236
CrossRef Google scholar
[26]
GiacomoniF, Le CorguilléG, MonsoorM, LandiM, PericardP, PétéraM, DuperierC, Tremblay-FrancoM, MartinJF, JacobD, GoulitquerS, ThévenotEA, CaronC. Workflow4Metabolomics: a collaborative research infrastructure for computational metabolomics. Bioinformatics, 2015, 31: 1493-1495
CrossRef Google scholar
[27]
GuoQ, LiX, NiuL, JamesonPE, ZhouW. Transcription-associated metabolomic adjustments in maize occur during combined drought and cold stress. Plant Physiol, 2021, 186(1):677-695
CrossRef Google scholar
[28]
GuyC. Molecular responses of plants to cold shock and cold acclimation. J Mol Microbiol Biotechnol, 1999, 1(2):231-242
[29]
GuyCL, HuberJL, HuberSC. Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol, 1992, 100: 502-508
CrossRef Google scholar
[30]
GuyCL, NiemiKJ, BramblR. Altered gene expression during cold acclimation of spinach. Proc Natl Acad Sci U S A, 1985, 82(11):3673-3677
CrossRef Google scholar
[31]
HallbergRL, KrausKW, HallbergEM. Induction of acquired thermotolerance in Tetrahymena thermophila: effects of protein synthesis inhibitors. Mol Cell Biol, 1985, 5: 2061-2069
CrossRef Google scholar
[32]
HasanuzzamanM, NaharK, AneeTI, FujitaM. Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants, 2017, 23: 249-268
CrossRef Google scholar
[33]
HernándezJA, AlmansaMS. Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiol Plant, 2002, 115(2):251-257
CrossRef Google scholar
[34]
Hildebrandt, T.M. (2018) Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol Biol. 98(1), 121-35. https://doi.org/10.1007/s11103-018-0767-0
[35]
Hipsch M., Lampl N., Zelinger E., Barda O., Waiger D., and Rosenwasser S. (2021) Sensing stress responses in potato with whole-plant redox imaging. Plant Physiol. 187(2), 618–631. https://doi.org/10.1093/plphys/kiab159
[36]
HoekstraFA, GolovinaEA, BuitinkJ. Mechanisms of plant desiccation tolerance. Trends Plant Sci, 2001, 6: 431-438
CrossRef Google scholar
[37]
HuangT, JanderG. Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana. Planta, 2017, 246: 737-747
CrossRef Google scholar
[38]
HunerN, ÖquistPAG, FatheyS. Energy balance and acclimation to light and cold. Trends Plant Sci, 1998, 3: 224-230
CrossRef Google scholar
[39]
KanehisaM, FurumichiM, TanabeM, SatoY, MorishimaK. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res, 2017, 45: D353-D361
CrossRef Google scholar
[40]
KanjariyaKG, PariharA. Prime-Ome: a molecular approach towards defence mechanisms. Int J Curr Microbiol App Sci, 2017, 6(8):3606-3610
CrossRef Google scholar
[41]
KaplanF, GuyCL. RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J, 2005, 44: 730-743
CrossRef Google scholar
[42]
KaplanF, KopkaJ, HaskellDW, ZhaoW, SchillerKC, GatzkeN, SungDY, GuyCL. Exploring the temperature-stress metabolome. Plant Physiol, 2004, 136: 4159-4168
CrossRef Google scholar
[43]
KaplanF, KopkaJ, SungDY, ZhaoW, PoppM, PoratR, GuyCL. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J, 2007, 50: 967-981
CrossRef Google scholar
[44]
KumarM, PatelMK, KumarN, BajpaiAB, SiddiqueK. Metabolomics and molecular approaches reveal drought stress tolerance in plants. Int J Mol Sci, 2021, 22(17):9108
CrossRef Google scholar
[45]
Kumar N, Singh H, Sharma SK (2020) Antioxidants: Responses and importance in plant defense system. In: Roychowdhury R, Choudhury S, Hasanuzzaman M, Srivastava S (eds) Sustainable agriculture in the era of climate change, Springer, Cham. https://doi.org/10.1007/978-3-030-45669-6_11
[46]
LarkindaleJ, HallJD, KnightMR, VierlingE. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol, 2005, 138(2):882-897
CrossRef Google scholar
[47]
Legris M, Klose C, Burgie ES, Rojas CC, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science:354, 897–900. https://doi.org/10.1126/science.aaf5656
[48]
LegrisM, NietoC, SellaroR, PratS, CasalJJ. Perception and signalling of light and temperature cues in plants. Plant J, 2017, 90: 683-697
CrossRef Google scholar
[49]
LeuendorfJE, FrankM, SchmüllingT. Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress. Sci Rep, 2020, 10: 689
CrossRef Google scholar
[50]
LevittJ. LevittJ. Responses of plants to environmental stresses, 1972 New York Academic Press 698 pp
[51]
LiWX, OonoY, ZhuJ, HeXJ, WuJM, IidaK, LuXY, CuiX, JinH, ZhuJK. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance. Plant Cell, 2008, 20(8):2238-2251
CrossRef Google scholar
[52]
LiX, BaoJ, WangJ, BlackmanC, TissueD. Antecedent drought condition affects responses of plant physiology and growth to drought and post-drought recovery. Frontiers in Forests and Global change, 2021 133
CrossRef Google scholar
[53]
LiX, LiuF, et al.. HossainMA, et al.. Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. Drought stress tolerance in plants, 2016 Switzerland Springer international publishing 17-44
CrossRef Google scholar
[54]
LiuQ, KasugaM, SakumaY, AbeH, MiuraS, Yamaguchi-ShinozakiK, ShinozakiK. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 1998, 10(8):1391-1406
CrossRef Google scholar
[55]
MarkleyJL, UlrichEL, BermanHM, HenrickK, NakamuraH, AkutsuH. BioMagResBank (BMRB) as a partner in the worldwide protein data Bank (wwPDB): new policies affecting biomolecular NMR depositions. J Biomol NMR, 2008, 40: 153-155
CrossRef Google scholar
[56]
Mauch-ManiB, BaccelliI, LunaE, FlorsV. Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol, 2017, 68: 485-512
CrossRef Google scholar
[57]
MaxwellDP, FalkS, HunerNP. Photosystem II excitation pressure and development of resistance to photoinhibition (I. light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris). Plant Physiol, 1995, 107(3):687-694
CrossRef Google scholar
[58]
NadarajahKK. ROS homeostasis in abiotic stress tolerance in plants. Int J Mol Sci, 2020, 21(15):5208
CrossRef Google scholar
[59]
NephaliL, PiaterLA, DuberyIA, PattersonV, HuyserJ, BurgessK, TugizimanaF. Biostimulants for plant growth and mitigation of abiotic stresses: a metabolomics perspective. Metabolites, 2020, 10(12):505
CrossRef Google scholar
[60]
Nieto-SoteloJ, KannanKB, MartínezLM, SegalC. Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/HSP 100 protein homologue. Gene, 1999, 230: 187-195
CrossRef Google scholar
[61]
NishizawaA, YabutaY, ShigeokaS. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol, 2008, 147: 1251-1263
CrossRef Google scholar
[62]
Olas, J.J., Apelt, F., Annunziata, M.G., John, S., Richard, S.I., Gupta, S., Kragler, F., Balazadeh, S. and Mueller-Roeber, B. (2021) Primary carbohydrate metabolism genes participate in heat-stress memory at the shoot apical meristem of Arabidopsis thaliana. Mol Plant 14(9), 1508-1524 https://doi.org/10.1016/j.molp.2021.05.024
[63]
PandeyP, IrulappanV, BagavathiannanMV, Senthil-KumarM. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci, 2017, 8: 537
CrossRef Google scholar
[64]
RajashekarCB, PandaM. Water stress is a component of cold acclimation process essential for inducing full freezing tolerance in strawberry. Sci Hortic, 2014, 174: 54-59
CrossRef Google scholar
[65]
RichlyE, DietzmannA, BiehlA, KurthJ, LaloiC, ApelK, SalaminiF, LeisterD. Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep, 2003, 4(5):491-498
CrossRef Google scholar
[66]
RizhskyL. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol, 2004, 134: 1683-1696
CrossRef Google scholar
[67]
RosselJB, WilsonIW, PogsonBJ. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol, 2002, 130(3):1109-1120
CrossRef Google scholar
[68]
RoxasVP, SmithRK, AllenER, AllenRD. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol, 1997, 15: 988-991
CrossRef Google scholar
[69]
SakumaY, MaruyamaK, OsakabeY, QinF, SekiM, ShinozakiK, Yamaguchi-ShinozakiK. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell, 2006, 18: 1292-1309
CrossRef Google scholar
[70]
SchneiderCA, RasbandWS, EliceiriKW. NIH image to ImageJ: 25 years of image analysis. Nat Methods, 2012, 9(7):671-675
CrossRef Google scholar
[71]
Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y., and Shinozaki K. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279–292. https://doi.org/10.1046/j.1365-313X.2002.01359.x
[72]
ShehuAA, AlsamadanyH, AlzahraniY. β-Aminobutyric acid (BABA) priming and abiotic stresses: a review. Int J Biosci, 2019, 14(5):450-459
CrossRef Google scholar
[73]
SmithA, O ‘MailleG, WantEJ, QinC, TraugerSA, BrandonTR, CustodioDE, AbagyanR, SiuzdakG. METLIN a metabolite mass spectral database. Ther Drug Monit, 2005, 27: 747-751
CrossRef Google scholar
[74]
StridÅ, ChowWS, AndersonJM. UV-B damage and protection at the molecular level in plants. Photosynth Res, 1994, 39: 475-489
CrossRef Google scholar
[75]
Strohm, M., Jouanin, L., Kunert, K.J., Pruvost, C., Polle, A., Foyer, C.H. and Rennenberg, H. (1995) Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula x P. alba) overexpressing glutathione synthetase. Plant J. 7, 141–145. https://doi.org/10.1046/j.1365-313X.1995.07010141.x
[76]
SzalaiG, KellősT, GalibaG, KocsyG. Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul, 2009, 28(1):66-80
CrossRef Google scholar
[77]
Szymańska, R., Ślesak, I., Orzechowska, A., and Kruk, J. (2017) Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot. 139, 165-77. https://doi.org/10.1016/j.envexpbot.2017.05.002
[78]
Tamburino, R., Vitale, M., Ruggiero, A., Sassi, M., Sannino, L., Arena, S., Costa A, Batelli G., Zambrano N., Scaloni A, Grillo S. and Scotti N. (2017). Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol. 17:40. https://doi.org/10.1186/s12870-017-0971-0
[79]
ThalmannM, SanteliaD. Starch as a determinant of plant fitness under abiotic stress. New Phytol, 2017, 214: 943-951
CrossRef Google scholar
[80]
ThomashowMF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol., 1999, 50: 571-599
CrossRef Google scholar
[81]
TivendaleND, HansonAD, HenryCS, HegemanAD, MillarAH. Enzymes as parts in need of replacement–and how to extend their working life. Trends Plant Sci, 2020, 25(7):661-669
CrossRef Google scholar
[82]
TugizimanaF, SteenkampPA, PiaterLA, LabuschagneN, DuberyIA. Unravelling the metabolic reconfiguration of the post-challenge primed state in sorghum bicolor responding to Colletotrichum sublineolum infection. Metabolites, 2019, 9(10):194
CrossRef Google scholar
[83]
Uemura M, Warren G, Steponkus PL (2003) Freezing sensitivity in the sfr4 mutant of Arabidopsis is due to low sugar content and is manifested by loss of osmotic responsiveness. Plant Physiol 131:1800–1807. https://doi.org/10.1104/pp.102.013227
[84]
Urano, K., Maruyama, K., Ogata, Y., Morishita, Y., Takeda, M., Sakurai, N., Suzuki, H., Saito, K., Shibata, D., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J. 57, 1065–1078. https://doi.org/10.1111/j.1365-313X.2008.03748.x
[85]
WangX, HouL, LuY, WuB, GongX, LiuM, WangJ, SunQ, VierlingE, XuS. Metabolic adaptation of wheat grain contributes to a stable filling rate under heat stress. J Exp Bot, 2018, 69(22):5531-5545
CrossRef Google scholar
[86]
WingateVPM, LawtonMA, LambCJ. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol, 1988, 87: 206-210
CrossRef Google scholar
[87]
WishartDS, JewisonT, GuoAC, WilsonM, KnoxC, LiuY, DjoumbouY, MandalR, AziatF, DongE, BouatraS, SinelnikovI, ArndtD, XiaJ, LiuP, YallouF, BjorndahlT, Perez-PineiroR, EisnerR, AllenF, NeveuV, GreinerR, ScalbertA. HMDB 3.0-the human metabolome database in 2013. Nucleic Acids Res, 2013, 41(database issue):D801-D807
CrossRef Google scholar
[88]
Wulff-Zottele C, Gatzke N, Kopka J, Orellana A, Hoefgen R, Fisahn J, Hesse H (2010) Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant Cell Environ 33:1974–1988. https://doi.org/10.1111/j.1365-3040.2010.02199.x
[89]
ZhangJZ, CreelmanRA, ZhuJK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol, 2004, 135(2):615-621
CrossRef Google scholar
[90]
ZhangT, WatsonDG. A short review of applications of liquid chromatography mass spectrometry-based metabolomics techniques to the analysis of human urine. Analyst, 2015, 140: 2907-2915 https://doi.org/10.1039/C4AN02294G
CrossRef Google scholar
Funding
Directorate for Biological Sciences(IOS-1400818); Minnesota Agricultural Experiment Station; Gordon and Margaret Bailey Endowment for Environmental Horticulture; University of Minnesota Informatics Institute

Accesses

Citations

Detail

Sections
Recommended

/