Abstract
Expression of Arabidopsis thaliana glutamate dehydrogenase genes is very low in the light and high in the dark. The molecular signals and mechanisms that provide the light-dependent glutamate dehydrogenase genes regulation remain unknown. The aim of this work was to study a role of redox signals which occur during light shifts in the regulation of the glutamate dehydrogenase genes expression. Using photosynthetic electron transport inhibitors 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) and 2,5-dibromo-3-methyl-6-isopropyl benzoquinone (DBMIB) we demonstrate that transcript levels of the GDH1 and GDH2 genes in Arabidopsis leaves change in accordance with a redox state of plastoquinone pool: they are low when it is highly reduced and high when it is oxidized. Hydrogen peroxide or high light treatment did not result in decreasing of GDH1 or GDH2 expression, so reactive oxygen species cannot be the signals that reduce expression of these genes during dark-to-light shifts. There was no significant difference between the glucose content in the leaves of plants treated with DCMU and the plants treated with DBMIB, so glucose is not the only or the main factor that regulates expression of the studied genes. We presume that expression of Arabidopsis GDH1 and GDH2 genes depends on the plastoquinone pool redox state.
Key Message
Expression of Arabidopsis glutamate dehydrogenase genes during light-to-dark and dark-to-light shifts depends on chloroplast electron transport chain redox state rather than reactive oxygen species or glucose content.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamiec M, Drath M, Jackowski G (2008) Redox state of plastoquionone pool regulates expression of Arabidopsis thaliana genes in response to elevated irradiance. Acta Biochim Pol 55(1):161–173
Akhtar TA, Lees HA, Lampi MA, Enstone D, Brain RA, Greenberg BM (2010) Photosynthetic redox imbalance influences flavonoid biosynthesis in Lemna gibbapce. Plant Cell Environ 33:1205–1219. https://doi.org/10.1111/j.1365-3040.2010.02140.x
Bode R, Ivanov AG, Huner NPA (2016) Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis. Photosynth Res 128:287–312. https://doi.org/10.1007/s11120-016-0245-y
Borisova-Mubarakshina MM, Vetoshkina DV, Rudenko NN, Shirshikova GN, Fedorchuk TP, Naydov IA, Ivanov BN (2014) The size of the light harvesting antenna of higher plant photosystem II is regulated by illumination intensity through transcription of antenna protein genes. Biochem Mosc 79(6):520–523. https://doi.org/10.1134/S0006297914060042
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510. https://doi.org/10.1105/tpc.010011
Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016) Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol 67:25–53. https://doi.org/10.1146/annurev-arplant-043015-111854
Degli Esposti M, Rotilio G, Lenaz G (1984) Effects of dibromothymoquinone on the structure and function of the mitochondrial bc1 complex. Biochim Biophys Acta 767(1):10–20. https://doi.org/10.1016/0005-2728(84)90074-4
Dietz K-J, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171(3):1541–1550. https://doi.org/10.1104/pp.16.00375
Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmuller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280(7):5318–5328. https://doi.org/10.1074/jbc.M406358200
Fontaine J-X, Terce-Laforgue T, Bouton S, Pageau K, Lea PJ, Dubois F, Hirel B (2013) Futher insights into the isoenzyme composition and activity of glutamate dehydrogenase in Arabidopsis thaliana. Plant Signal Behav 3:e23329. https://doi.org/10.4161/psb.23329
Garnik EYu, Belkov VI, Tarasenko VI, Potapova TV, Korzun MA, Konstantinov YuM (2013) The expression of Arabidopsis glutamate dehydrogenase gene GDH2 is induced under the influence of tetrapyrrole synthesis inhibitor norflurazon. J Stress Physiol Biochem 9(4):299–309
Garnik EYu, Belkov VI, Tarasenko VI, Konstantinov YuM (2014) The role of sugar-related regulation in the light-dependent alterations of Arabidopsis glutamate dehydrogenase genes expression. J Stress Physiol Biochem 10(4):67–76
Garnik EYu, Belkov VI, Tarasenko VI, Korzun MA, Konstantinov YuM (2016) Glutathione reductase gene expression depends on chloroplast signals in Arabidopsis thaliana. Biochem Mosc 81(4):364–372. https://doi.org/10.1134/S0006297916040064
Goel P, Singh AK (2015) Abiotic stresses downregulate key genes involved in nitrogen uptake and assimilation in Brassica juncea L. PLoS ONE 10(11):e0143645. https://doi.org/10.1371/journal.pone.0143645
Hong SM, Bahn SC, Lyu A, Jung HS, Ahn JH (2010) Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol 51:1694–1706. https://doi.org/10.1093/pcp/pcq128
Kim C, Apel K (2013) Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res 116(2–3):445–464. https://doi.org/10.1007/s11120-013-9876-4
Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55(404):1831–1842. https://doi.org/10.1093/jxb/erh203
Labboun S, Tercé-Laforgue T, Roscher A, Bedu M, Restivo FM, Velanis ChN, Skopelitis DS, Moshou PN, Roubelakis-Angelakis KA, Suzuki A, Hirel B (2009) Resolving the role of plant glutamate dehydrogenase. I. In vivo real time nuclear magnetic resonance spectroscopy experiments. Plant Cell Physiol 50(10):1761–1773. https://doi.org/10.1093/pcp/pcp118
Lee ChP, Eubel H, Millar AH (2010) Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis. Mol Cell Proteom 9(10):2125–2139. https://doi.org/10.1074/mcp.M110.001214
Lepetit B, Sturm S, Rogato A, Gruber A, Sachse M, Falciatore A, Lavaud J (2013) High light acclimation in the secondary plastids containing diatom Phaeodactylum tricornutum is triggered by the redox state of the plastoquinone pool. Plant Physiol 161(2):853–865. https://doi.org/10.1104/pp.112.207811
Li Yu, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance VectorMachine. Genome Res 16(3):414–427. https://doi.org/10.1101/gr.4237406
Magadlela A, Morcillo RJL, Kleinert A, Venter M, Steenkamp E, Valentine A (2019) Glutamate dehydrogenase is essential in the acclimation of Virgilia divaricata, a legume indigenous to the nutrient-poor Mediterranean-type ecosystems of the Cape Fynbos. J Plant Physiol 243:e153053. https://doi.org/10.1016/j.jplph.2019.153053
Marchi L, Degola F, Polverini E, Terce-Laforgque T, Dubois F, Restivo FM (2013) Glutamate dehydrogenase isoenzyme 3 (GDH3) of Arabidopsis thaliana is regulated by a combined effect of nitrogen and cytokinin. Plant Physiol Biochem 73:368–374. https://doi.org/10.1016/j.plaphy.2013.10.019
Miyashita Y, Good AG (2008) NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark induced carbon starvation. J Exp Bot 59(3):667–680. https://doi.org/10.1093/jxb/erm340
Mubarakshina MM, Ivanov BN (2010) The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes. Physiol Plant 140(2):103–110. https://doi.org/10.1111/j.1399-3054.2010.01391.x
Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397:625–628. https://doi.org/10.1038/17624
Pfannschmidt T, Shcutze K, Brost M, Oelmuller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276(39):36125–36130. https://doi.org/10.1074/jbc.m105701200
Rasmusson AG, Escobar MA (2007) Light and diurnal regulation of plant respiratory gene expression. Physiol Plant 129(1):57–67. https://doi.org/10.1111/j.1399-3054.2006.00797.x
Robinson SA, Stewart GR, Phillips R (1992) Regulation of glutamate dehydrogenase activity in relation to carbon imitation and protein catabolism in carrot cell suspension cultures. Plant Physiol 98:1190–1195. https://doi.org/10.1104/pp.98.3.1190
Saini G, Meskauskeine R, Pijacka W, Roszak P, Sjogren LL, Clarke AK, Straus M, Apel K (2011) «happy on norflurazon» (hon) mutations implicate perturbance of plastid homeostasis with activating stress acclimatization and changing nuclear gene expression in norflurazon-treated seedlings. Plant J 65(5):690–702. https://doi.org/10.1111/j.1365-313X.2010.04454.x
Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis CA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18(10):2767–2781. https://doi.org/10.1105/tpc.105.038323
Slesak I, Karpinska B, Surówka E, Miszalski Z, Karpinski S (2003) Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3–CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L. Plant Cell Physiol 44(6):573–581. https://doi.org/10.1093/pcp/pcg073
Sun M, Gao Z, Zhao W, Deng L, Deng Y, Zhao H, Ren A, Li G, Yang Z (2013) Effect of subsoiling in fallow period on soil water storage and grain protein accumulation of dryland wheat and its regulatory effect by nitrogen application. PLoS ONE 8(10):e75191. https://doi.org/10.1371/journal.pone.0075191
Surkov SA, Konstantinov A (1980) Dibromothymoquinone interaction with the CoQ-cytochrome b locus of the mitochondrial respiratory chain. FEBS Lett 109(2):283–288. https://doi.org/10.1016/0014-5793(80)81106-9
Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0145. https://doi.org/10.1199/tab.0145
Tarasenko VI, Garnik EYu, Shmakov VN, Konstantinov YuM (2009) Induction of Arabidopsis GDH2 gene expression during changes in redox state of the mitochondrial respiratory chain. Biochem Mosc 74(1):47–53. https://doi.org/10.1134/s0006297909010076
Tarasenko VI, Garnik EY, Shmakov VN, Konstantinov YM (2012) Modified alternative oxidase expression results in different reactive oxygen species contents in Arabidopsis cell culture but not in whole plants. Biol Plant 56:635–640. https://doi.org/10.1007/s10535-012-0115-1
Terce-Laforgue T, Clement G, Marchi L, Restivo FM, Lea PJ, Hirel B (2015) Resolving the role of plant NAD-glutamate dehydrogenase: III. Overexpressing individually or simultaneously the two enzyme subunits under salt stress induces changes in the leaf metabolic profile and increases plant biomass production. Plant Cell Physiol 56(10):1918–1929. https://doi.org/10.1093/pcp/pcv114
Tsai KJ, Lin CY, Ting CY, Shih MC (2016) Ethylene-regulated glutamate dehydrogenase fine-tunes metabolism during anoxia-reoxygenation. Plant Physiol 172(3):1548–1562. https://doi.org/10.1104/pp.16.00985
Turano F, Thakkar S, Fang T, Weisemann J (1997) Characterization and expression of NAD(H)- dependent glutamate dehydrogenase genes in Arabidopsis. Plant Physiol 113(3):1329–1341. https://doi.org/10.1104/pp.113.4.1329
Wang W-H, He E-M, Chen J, Guo Y, Chen J, Liu X, Zheng H-L (2016) The reduced state of the plastoquinone pool is required for chloroplast-mediated stomatal closure in response to calcium stimulation. Plant J 86(2):132–144. https://doi.org/10.1111/tpj.13154
Xiaochuang C, Meiyan W, Chunquan Zh, Chu Zh, Junhua Zh, Lianfeng Zh, Lianghuan W, Qianyu J (2020) Glutamate dehydrogenase mediated amino acid metabolism after ammonium uptake enhances rice growth under aeration condition. Plant Cell Rep 39(3):363–379. https://doi.org/10.1007/s00299-019-02496-w
Yabuta Y, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol 45(11):1586–1594. https://doi.org/10.1093/pcp/pch181
Acknowledgements
This work was financially supported by the RAS project VI.56.1.3. Equipment of the Bioanalitika Center for Collective Use, Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch of the Russian Academy of Sciences, Irkutsk, was used in this study. We would like to thank Prof. Ian Max Moller for his critical reading of this manuscript and his valuable comments helping to improve it.
Author information
Authors and Affiliations
Contributions
Conceptualization, Methodology, Writing—original draft preparation: EYG; Investigation, Validation, Data curation: VIB, AVR; Resources, Writing—reviewing and editing: VIT; Project administration: YMK. All authors discussed the results and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Informed consent
Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.
Research involving human and animal rights
This research did not involve experiments with human or animal participants.
Additional information
Communicated by Goetz Hensel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Garnik, E.Y., Belkov, V.I., Tarasenko, V.I. et al. Expression of glutamate dehydrogenase genes in Arabidopsis thaliana depends on the redox state of plastoquinone pool. Plant Cell Tiss Organ Cult 147, 107–116 (2021). https://doi.org/10.1007/s11240-021-02111-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-021-02111-5