Abstract
Key message
During abiotic stress low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, darkness) and are degraded.
Abstract
Metabolic adaptation is crucial for abiotic stress resistance in plants, and accumulation of specific amino acids as well as secondary metabolites derived from amino acid metabolism has been implicated in increased tolerance to adverse environmental conditions. The role of proline, which is synthesized during Arabidopsis stress response to act as a compatible osmolyte, has been well established. However, conclusions drawn about potential functions of other amino acids such as leucine, valine, and isoleucine are not entirely consistent. This study reevaluates published datasets with a special emphasis on changes in the free amino acid pool and transcriptional regulation of the associated anabolic and catabolic pathways. In order to gain a comprehensive overview about the general direction of amino acid metabolism under abiotic stress conditions a complete map of all currently known enzymatic steps involved in amino acid synthesis and degradation was assembled including also the initial steps leading to the synthesis of secondary metabolites. Microarray datasets and amino acid profiles of Arabidopsis plants exposed to dehydration, high salinity, extended darkness, cold, and heat were systematically analyzed to identify trends in fluxes of amino acid metabolism. Some high abundant amino acids such as proline, arginine, asparagine, glutamine, and GABA are synthesized during abiotic stress to act as compatible osmolytes, precursors for secondary metabolites, or storage forms of organic nitrogen. In contrast, most of the low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, extended darkness) and are degraded.
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References
Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372
Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3
Amir R (2010) Current understanding of the factors regulating methionine content in vegetative tissues of higher plants. Amino Acids 39:917–931. https://doi.org/10.1007/s00726-010-0482-x
Angelovici R, Lipka AE, Deason N, Gonzalez-Jorge S, Lin H, Cepela J, Buell R, Gore MA, Dellapenna D (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25:4827–4843. https://doi.org/10.1105/tpc.113.119370
Araújo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22:1549–1563. https://doi.org/10.1105/tpc.110.075630
Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation—an alternative respiratory substrate for stressed plants. Trends Plant Sci 16:489–498. https://doi.org/10.1016/j.tplants.2011.05.008
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58. https://doi.org/10.1080/07352680590910410
Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620. https://doi.org/10.1111/j.1469-8137.2009.02823.x
Bhaskara GB, Yang T, Verslues PE (2015) Dynamic proline metabolism: importance and regulation in water limited environments. Front Plant Sci 6:484. https://doi.org/10.3389/fpls.2015.00484
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115. https://doi.org/10.1016/j.tplants.2004.01.006
Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Ong Q, Paley S, Subhraveti P, Weaver DS, Karp PD (2016) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 44:D471–D480. https://doi.org/10.1093/nar/gkv1164
Chen Y, Holmes EC, Rajniak J, Kim J, Tang S, Fischer CR, Mudgett MB, Sattely ES (2018) N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. Proc Natl Acad Sci USA 115:E4920–E4929. https://doi.org/10.1073/pnas.1805291115
D’Auria JC, Gershenzon J (2005) The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 8:308–316. https://doi.org/10.1016/j.pbi.2005.03.012
Däschner K, Couée I, Binder S (2001) The mitochondrial isovaleryl-coenzyme a dehydrogenase of arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol 126:601–612
Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7:899–906. https://doi.org/10.1105/tpc.7.7.899
Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839. https://doi.org/10.1111/j.1365-313X.2005.02587.x
Gotor C, García I, Crespo JL, Romero LC (2013) Sulfide as a signaling molecule in autophagy. Autophagy 9:609–611. https://doi.org/10.4161/auto.23460
Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223. https://doi.org/10.1146/annurev.pp.41.060190.001155
Hannah MA, Caldana C, Steinhauser D, Balbo I, Fernie AR, Willmitzer L (2010) Combined transcript and metabolite profiling of Arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol 152:2120–2129. https://doi.org/10.1104/pp.109.147306
Hartmann M, Zeier T, Bernsdorff F, Reichel-Deland V, Kim D, Hohmann M, Scholten N, Schuck S, Bräutigam A, Hölzel T, Ganter C, Zeier J (2018) Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173:456–469.e16. https://doi.org/10.1016/j.cell.2018.02.049
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643
Hildebrandt TM, Nunes Nesi A, Araújo WL, Braun H (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579. https://doi.org/10.1016/j.molp.2015.09.005
Hong Z, Lakkineni K, Zhang Z, Verma DP (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747. https://doi.org/10.1155/2008/420747
Huang T, Jander G (2017) Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana. Planta. https://doi.org/10.1007/s00425-017-2727-3
Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17:2587–2600. https://doi.org/10.1105/tpc.105.035162
Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J 47:751–760. https://doi.org/10.1111/j.1365-313X.2006.02826.x
Izumi M, Wada S, Makino A, Ishida H (2010) The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154:1196–1209. https://doi.org/10.1104/pp.110.158519
Jacob C, Giles GI, Giles NM, Sies H (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Engl 42:4742–4758. https://doi.org/10.1002/anie.200300573
Joshi V, Jander G (2009) Arabidopsis methionine γ-lyase is regulated according to isoleucine biosynthesis needs but plays a subordinate role to threonine deaminase. Plant physiol 151:367–378
Joshi V, Joung J, Fei Z, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–947. https://doi.org/10.1007/s00726-010-0505-7
Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361. https://doi.org/10.1093/nar/gkw1092
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168. https://doi.org/10.1104/pp.104.052142
Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363. https://doi.org/10.1111/j.1365-313X.2007.03052.x
Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376. https://doi.org/10.1111/tpj.12205
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608. https://doi.org/10.1093/jxb/err460
Krüßel L, Junemann J, Wirtz M, Birke H, Thornton JD, Browning LW, Poschet G, Hell R, Balk J, Braun H, Hildebrandt TM (2014) The mitochondrial sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 is required for amino acid catabolism during carbohydrate starvation and embryo development in Arabidopsis. Plant Physiol 165:92–104. https://doi.org/10.1104/pp.114.239764
Lam H, Wong P, Chan H, Yam K, Chen L, Chow C, Coruzzi GM (2003) Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol 132:926–935. https://doi.org/10.1104/pp.103.020123
Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147:316–330. https://doi.org/10.1104/pp.108.115733
Ludwików A, Kierzek D, Gallois P, Zeef L, Sadowski J (2009) Gene expression profiling of ozone-treated Arabidopsis abi1td insertional mutant: protein phosphatase 2C ABI1 modulates biosynthesis ratio of ABA and ethylene. Planta 230:1003–1017. https://doi.org/10.1007/s00425-009-1001-8
Lugan R, Niogret M, Leport L, Guégan J, Larher FR, Savouré A, Kopka J, Bouchereau A (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant J 64:215–229. https://doi.org/10.1111/j.1365-313X.2010.04323.x
Lv W, Lin B, Zhang M, Hua X (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933. https://doi.org/10.1104/pp.111.175810
Maeda H, Song W, Sage T, Dellapenna D (2014) Role of callose synthases in transfer cell wall development in tocopherol deficient Arabidopsis mutants. Front Plant Sci 5:46. https://doi.org/10.3389/fpls.2014.00046
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158. https://doi.org/10.1016/j.abb.2005.10.018
Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243. https://doi.org/10.1007/s00018-012-1091-5
Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216. https://doi.org/10.1186/1471-2164-14-216
Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J Bacteriol 185:1942–1950
Perera IY, Hung C, Moore CD, Stevenson-Paulik J, Boss WF (2008) Transgenic Arabidopsis plants expressing the type 1 inositol 5-phosphatase exhibit increased drought tolerance and altered abscisic acid signaling. Plant Cell 20:2876–2893. https://doi.org/10.1105/tpc.108.061374
Pires MV, Pereira Júnior AA, Medeiros DB, Daloso DM, Pham PA, Barros KA, Engqvist MKM, Florian A, Krahnert I, Maurino VG, Araújo WL, Fernie AR (2016) The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis. Plant Cell Environ 39:1304–1319. https://doi.org/10.1111/pce.12682
Pratelli R, Pilot G (2014) Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot 65:5535–5556. https://doi.org/10.1093/jxb/eru320
Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:921–934. https://doi.org/10.1105/tpc.7.7.921
Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076. https://doi.org/10.1104/pp.114.245373
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, 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
Shedge V, Davila J, Arrieta-Montiel MP, Mohammed S, Mackenzie SA (2010) Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance. Plant Physiol 152:1960–1970. https://doi.org/10.1104/pp.109.152827
Shinde S, Villamor JG, Lin W, Sharma S, Verslues PE (2016) Proline coordination with fatty acid synthesis and redox metabolism of chloroplast and mitochondria. Plant Physiol 172:1074–1088. https://doi.org/10.1104/pp.16.01097
Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66:844–851. https://doi.org/10.1111/j.1365-313X.2011.04550.x
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. https://doi.org/10.1016/j.tplants.2009.11.009
The UniProt Consortium (2017) UniProt: the universal protein knowledgebase. Nucleic Acids Res 45:D158–D169. https://doi.org/10.1093/nar/gkw1099
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x
Tzin V, Galili G (2010) New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol Plant 3:956–972. https://doi.org/10.1093/mp/ssq048
Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, 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
Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146:1834–1861. https://doi.org/10.1104/pp.107.115592
Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book 8:e0140. https://doi.org/10.1199/tab.0140
Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310. https://doi.org/10.1104/pp.113.217380
Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270
Zhu J (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324. https://doi.org/10.1016/j.cell.2016.08.029
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I thank Michael Senkler for helping me with the extraction of the expression data and Hans-Peter Braun for critically reading the manuscript.
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Hildebrandt, T.M. Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol Biol 98, 121–135 (2018). https://doi.org/10.1007/s11103-018-0767-0
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DOI: https://doi.org/10.1007/s11103-018-0767-0