Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet

Hossain MS, Persicke M, ElSayed AI, Kalinowski J, Dietz K-J (2017)
Journal of Experimental Botany 68(21-22): 5961-5976.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
Sugar beet is among the most salt-tolerant crops. This study aimed to investigate the metabolic adaptation of sugar beet to salt stress at the cellular and subcellular levels. Seedlings were grown hydroponically and subjected to stepwise increases in salt stress up to 300 mM NaCl. Highly enriched fractions of chloroplasts were obtained by nonaqueous fractionation using organic solvents. Total leaf metabolites and metabolites in chloroplasts were profiled at 3 h and 14 d after reaching the maximum salinity stress of 300 mM NaCl. Metabolite profiling by gas chromatography- mass spectrometry (GC-MS) resulted in the identification of a total of 83 metabolites in leaves and chloroplasts under control and stress conditions. There was a lower abundance of Calvin cycle metabolites under salinity whereas there was a higher abundance of oxidative pentose phosphate cycle metabolites such as 6-phosphogluconate. Accumulation of ribose-5-phosphate and ribulose-5-phosphate coincided with limitation of carbon fixation by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). Increases in glycolate and serine levels indicated that photorespiratory metabolism was stimulated in salt-stressed sugar beet. Compatible solutes such as proline, mannitol, and putrescine accumulated mostly outside the chloroplasts. Within the chloroplast, putrescine had the highest relative level and probably assisted in the acclimation of sugar beet to high salinity stress. The results provide new information on the contribution of chloroplasts and the extra-chloroplast space to salinity tolerance via metabolic adjustment in sugar beet.
Erscheinungsjahr
Zeitschriftentitel
Journal of Experimental Botany
Band
68
Ausgabe
21-22
Seite(n)
5961-5976
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Hossain MS, Persicke M, ElSayed AI, Kalinowski J, Dietz K-J. Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany. 2017;68(21-22):5961-5976.
Hossain, M. S., Persicke, M., ElSayed, A. I., Kalinowski, J., & Dietz, K. - J. (2017). Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany, 68(21-22), 5961-5976. doi:10.1093/jxb/erx388
Hossain, M. S., Persicke, M., ElSayed, A. I., Kalinowski, J., and Dietz, K. - J. (2017). Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany 68, 5961-5976.
Hossain, M.S., et al., 2017. Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany, 68(21-22), p 5961-5976.
M.S. Hossain, et al., “Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet”, Journal of Experimental Botany, vol. 68, 2017, pp. 5961-5976.
Hossain, M.S., Persicke, M., ElSayed, A.I., Kalinowski, J., Dietz, K.-J.: Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany. 68, 5961-5976 (2017).
Hossain, M. Sazzad, Persicke, Marcus, ElSayed, Abdelaleim Ismail, Kalinowski, Jörn, and Dietz, Karl-Josef. “Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet”. Journal of Experimental Botany 68.21-22 (2017): 5961-5976.

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Mishra P, Jain A, Takabe T, Tanaka Y, Negi M, Singh N, Jain N, Mishra V, Maniraj R, Krishnamurthy SL, Sreevathsa R, Singh NK, Rai V., Front Plant Sci 10(), 2019
PMID: 30941150
Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.
Zinta G, AbdElgawad H, Peshev D, Weedon JT, Van den Ende W, Nijs I, Janssens IA, Beemster GTS, Asard H., J Exp Bot 69(8), 2018
PMID: 29462345

92 References

Daten bereitgestellt von Europe PubMed Central.

Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity.
Abebe T, Guenzi AC, Martin B, Cushman JC., Plant Physiol. 131(4), 2003
PMID: 12692333
Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses
Ahmad R, Lim CJ, Kwon SY., 2013
Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene.
Alcazar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrian M, Tiburcio AF, Altabella T., Plant Physiol. Biochem. 48(7), 2010
PMID: 20206537
Synthesis and Use of Stable-Isotope-Labeled Internal Standards for Quantification of Phosphorylated Metabolites by LC-MS/MS.
Arrivault S, Guenther M, Fry SC, Fuenfgeld MM, Veyel D, Mettler-Altmann T, Stitt M, Lunn JE., Anal. Chem. 87(13), 2015
PMID: 26010726
Sucrose regulated enhanced induction of anthra-quinone, phenolics, flavonoids biosynthesis and activities of antioxidant enzymes in adventitious root suspension cultures of Morinda citrifolia (L.)
Baque MA, Elgirban A, Lee E, Paek K., 2012
Drought and salt tolerance in plants
Bartels D, Sunkar R., 2005
Purification and compartmentation of α-mannosidase isoenzymes of barley leaves
Betz M, Martinoia E, Hincha DK, Schmidt JM, Dietz KJ., 1992
Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes.
Bose J, Munns R, Shabala S, Gilliham M, Pogson B, Tyerman SD., J. Exp. Bot. 68(12), 2017
PMID: 28472512
Natural products (secondary metabolites)
Croteau R, Kutchan TM, Lewis NG., 2000
A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis of leaves
Dietz KJ., 1985
Alleviation of changes in protein metabolism in NaCl-stressed wheat seedlings by thiamine
El-Shintinawy F, El-Shourbagy MN., 2001
Silicon-induced reversibility of cadmium toxicity in rice.
Farooq MA, Detterbeck A, Clemens S, Dietz KJ., J. Exp. Bot. 67(11), 2016
PMID: 27122572
Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants.
Feng L, Wang K, Li Y, Tan Y, Kong J, Li H, Li Y, Zhu Y., Plant Cell Rep. 26(9), 2007
PMID: 17458549
Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management
Flexas J, Bota J, Cifre J, Mariano J., 2004
Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity
Gao Z, Sagi M, Lips SH., 1998
Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars
Ghoulam C, Foursy A, Fares K., 2002
Polyamines and abiotic stress: recent advances.
Groppa MD, Benavides MP., Amino Acids 34(1), 2007
PMID: 17356805
Proteome analysis of sugar beet leaves under drought stress.
Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Salekdeh GH., Proteomics 5(4), 2005
PMID: 15712235
Über die Lokalisation yon löslichen Zuckern in der Pflanzenzelle
Heber U., 1957
Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight
Heber U, Bligny R, Streb P, Douce R., 1996
Effect of NaCl stress on growth, water relations, organic and inorganic osmolytes accumulation in sunflower (Helianthus annuus L.) lines
Heidari A, Toorchi M, Bandehagh A, Shakiba MR., 2011
Redox and Reactive Oxygen Species Network in Acclimation for Salinity Tolerance in Sugar Beet.
Hossain MS, ElSayed AI, Moore M, Dietz KJ., J. Exp. Bot. 68(5), 2017
PMID: 28338762
Salt-regulated mannitol metabolism in algae.
Iwamoto K, Shiraiwa Y., Mar. Biotechnol. 7(5), 2005
PMID: 16088352
Cold stress and acclimation - what is important for metabolic adjustment?
Janska A, Marsik P, Zelenkova S, Ovesna J., Plant Biol (Stuttg) 12(3), 2010
PMID: 20522175
Exploring the temperature-stress metabolome of Arabidopsis.
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL., Plant Physiol. 136(4), 2004
PMID: 15557093
Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana.
Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler F, Peterhansel C., Nat. Biotechnol. 25(5), 2007
PMID: 17435746
A central role of abscisic acid in stress-regulated carbohydrate metabolism.
Kempa S, Krasensky J, Dal Santo S, Kopka J, Jonak C., PLoS ONE 3(12), 2008
PMID: 19081841
FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry.
Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O., Anal. Chem. 81(24), 2009
PMID: 19928838
Metabolite profiling in plant biology: platforms and destinations.
Kopka J, Fernie A, Weckwerth W, Gibon Y, Stitt M., Genome Biol. 5(6), 2004
PMID: 15186482
A topological map of the compartmentalized Arabidopsis thaliana leaf metabolome.
Krueger S, Giavalisco P, Krall L, Steinhauser MC, Bussis D, Usadel B, Flugge UI, Fernie AR, Willmitzer L, Steinhauser D., PLoS ONE 6(3), 2011
PMID: 21423574
Proteomic analysis of sugar beet apomictic monosomic addition line M14.
Li H, Cao H, Wang Y, Pang Q, Ma C, Chen S., J Proteomics 73(2), 2009
PMID: 19782777
Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana.
Liebminger E, Huttner S, Vavra U, Fischl R, Schoberer J, Grass J, Blaukopf C, Seifert GJ, Altmann F, Mach L, Strasser R., Plant Cell 21(12), 2009
PMID: 20023195
Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte.
Lugan R, Niogret MF, Leport L, Guegan JP, Larher FR, Savoure A, Kopka J, Bouchereau A., Plant J. 64(2), 2010
PMID: 21070405
Vacuoles as storage compartments for nitrate in barley leaves
Martinoia E, Heck U, Wiemken A., 1981
Spreading the news: subcellular and organellar reactive oxygen species production and signalling.
Mignolet-Spruyt L, Xu E, Idanheimo N, Hoeberichts FA, Muhlenbock P, Brosche M, Van Breusegem F, Kangasjarvi J., J. Exp. Bot. 67(13), 2016
PMID: 26976816
Mechanisms of salinity tolerance
Munns R, Tester M., 2008
Salt tolerance and salinity effects on plants: a review.
Parida AK, Das AB., Ecotoxicol. Environ. Saf. 60(3), 2005
PMID: 15590011
Investigations on the antioxidative defence responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes
Parida AK, Das AB, Mohanty P., 2004
Rubisco activity: effects of drought stress.
Parry MA, Andralojc PJ, Khan S, Lea PJ, Keys AJ., Ann. Bot. 89 Spec No(), 2002
PMID: 12102509
Trehalose metabolism and signaling.
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y., Annu Rev Plant Biol 59(), 2008
PMID: 18257709
A demonstration of carboxylase enzyme activity in pea pod and seed tissues
Price DN, Donkin ME., 1982
Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance.
Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, Dupont-Gillain CC, Lutts S., J. Exp. Bot. 61(10), 2010
PMID: 20472577
Physiology and molecular biology of salinity stress tolerance in plants
Sairam RK, Tyagi A., 2004
Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis.
Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J., Plant Cell Environ. 34(4), 2011
PMID: 21251019
Plant metabolomics reveals conserved and divergent metabolic responses to salinity.
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J., Physiol Plant 132(2), 2008
PMID: 18251862
Osmoprotectants: potential for crop improvement under adverse conditions
Saxena SC, Kaur H, Verma P., 2013
Plant metabolomics: towards biological function and mechanism.
Schauer N, Fernie AR., Trends Plant Sci. 11(10), 2006
PMID: 16949327
Strategies to maintain redox homeostasis during photosynthesis under changing conditions.
Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S., J. Exp. Bot. 56(416), 2005
PMID: 15851411
Mannitol Protects against Oxidation by Hydroxyl Radicals.
Shen B, Jensen RG, Bohnert HJ., Plant Physiol. 115(2), 1997
PMID: 12223821
Increased Salt and Drought Tolerance by D-Ononitol Production in Transgenic Nicotiana tabacum L.
Sheveleva E, Chmara W, Bohnert HJ, Jensen RG., Plant Physiol. 115(3), 1997
PMID: 12223867
The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress.
Shu S, Yuan Y, Chen J, Sun J, Zhang W, Tang Y, Zhong M, Guo S., Sci Rep 5(), 2015
PMID: 26435404
Metabolomics for plant stress response.
Shulaev V, Cortes D, Miller G, Mittler R., Physiol Plant 132(2), 2008
PMID: 18251861
The physiology and biochemistry of polyamines in plants.
Slocum RD, Kaur-Sawhney R, Galston AW., Arch. Biochem. Biophys. 235(2), 1984
PMID: 6393877
Chloroplast Isolation in Nonaqueous Media.
Stocking CR., Plant Physiol. 34(1), 1959
PMID: 16655175
Proline: a multifunctional amino acid.
Szabados L, Savoure A., Trends Plant Sci. 15(2), 2009
PMID: 20036181
Water stress enhances beta-amylase activity in cucumber cotyledons.
Todaka D, Matsushima H, Morohashi Y., J. Exp. Bot. 51(345), 2000
PMID: 10938866
Understanding regulatory networks and engineering for enhanced drought tolerance in plants.
Valliyodan B, Nguyen HT., Curr. Opin. Plant Biol. 9(2), 2006
PMID: 16483835
Proline accumulation in plants: a review.
Verbruggen N, Hermans C., Amino Acids 35(4), 2008
PMID: 18379856
Emerging concept for the role of photorespiration as an important part of abiotic stress response.
Voss I, Sunil B, Scheibe R, Raghavendra AS., Plant Biol (Stuttg) 15(4), 2013
PMID: 23452019
Osmotic adjustment of young sugar beets (Beta vulgaris) under progressive drought stress and subsequent rewatering assessed by metabolite analysis and infrared thermography
Wedeking R, Mahlein A-K, Steiner U, Oerke E-Ch, Goldbach HE, Wimmer MA., 2017
Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance.
Widodo , Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U., J. Exp. Bot. 60(14), 2009
PMID: 19666960
Targeted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analyses.
Wienkoop S, Weiss J, May P, Kempa S, Irgang S, Recuenco-Munoz L, Pietzke M, Schwemmer T, Rupprecht J, Egelhofer V, Weckwerth W., Mol Biosyst 6(6), 2010
PMID: 20358043
Subcellular volumes and metabolite concentrations in barley leaves
Winter H, Robinson DG, Heldt HW., 1993
Subcellular volumes and metabolite concentrations in spinach leaves
Winter H, Robinson DG, Heldt HW., 1994
Tissue metabolic responses to salt stress in wild and cultivated barley.
Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G., PLoS ONE 8(1), 2013
PMID: 23383190
Photorespiration is more effective than the Mehler reaction in protecting the photosynthetic apparatus against photoinhibition
Wu J, Neimanis S, Heber U., 1991
Salt stress induced proteome and transcriptome changes in sugar beet monosomic addition line M14.
Yang L, Ma C, Wang L, Chen S, Li H., J. Plant Physiol. 169(9), 2012
PMID: 22498239
Molecular biology of salt tolerance in the context of whole-plant physiology
Yeo AR., 1998
Comparative metabolome analysis of the salt response in breeding cultivars of rice
Zuther E, Koehl K, Kopka J., 2007

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