دورية أكاديمية

Glutamate decarboxylase-1 is essential for efficient acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation.

التفاصيل البيبلوغرافية
العنوان: Glutamate decarboxylase-1 is essential for efficient acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation.
المؤلفون: Benidickson KH; Department of Biology, Queen's University, Kingston, ON, K7L 3N6, Canada., Raytek LM; Department of Biology, Queen's University, Kingston, ON, K7L 3N6, Canada., Hoover GJ; Department of Plant Agriculture, University of Guelph, Guelph, ON, N1G 2W1, Canada., Flaherty EJ; Department of Plant Agriculture, University of Guelph, Guelph, ON, N1G 2W1, Canada., Shelp BJ; Department of Plant Agriculture, University of Guelph, Guelph, ON, N1G 2W1, Canada., Snedden WA; Department of Biology, Queen's University, Kingston, ON, K7L 3N6, Canada., Plaxton WC; Department of Biology, Queen's University, Kingston, ON, K7L 3N6, Canada.
المصدر: The New phytologist [New Phytol] 2023 Dec; Vol. 240 (6), pp. 2372-2385. Date of Electronic Publication: 2023 Oct 14.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE
أسماء مطبوعة: Publication: Oxford : Wiley on behalf of New Phytologist Trust
Original Publication: London, New York [etc.] Academic Press.
مواضيع طبية MeSH: Arabidopsis*/metabolism , Arabidopsis Proteins*/genetics , Arabidopsis Proteins*/metabolism, Phosphorus/metabolism ; Glutamate Decarboxylase/genetics ; Glutamate Decarboxylase/metabolism ; Acclimatization ; Aminobutyrates/metabolism ; gamma-Aminobutyric Acid/metabolism ; Plant Roots/metabolism ; Phosphates/metabolism ; Gene Expression Regulation, Plant
مستخلص: Glutamate decarboxylase (GAD) is a Ca 2+ -calmodulin-activated, cytosolic enzyme that produces γ-aminobutyrate (GABA) as the committed step of the GABA shunt. This pathway bypasses the 2-oxoglutarate to succinate reactions of the tricarboxylic acid (TCA) cycle. GABA also accumulates during many plant stresses. We tested the hypothesis that AtGAD1 (At5G17330) facilitates Arabidopsis acclimation to Pi deprivation. Quantitative RT-PCR and immunoblotting revealed that AtGAD1 transcript and protein expression is primarily root-specific, but inducible at lower levels in shoots of Pi-deprived (-Pi) plants. Pi deprivation reduced levels of the 2-oxoglutarate dehydrogenase (2-OGDH) cofactor thiamine diphosphate (ThDP) in shoots and roots by > 50%. Growth of -Pi atgad1 T-DNA mutants was significantly attenuated relative to wild-type plants. This was accompanied by: (i) an > 60% increase in shoot and root GABA levels of -Pi wild-type, but not atgad1 plants, and (ii) markedly elevated anthocyanin and reduced free and total Pi levels in leaves of -Pi atgad1 plants. Treatment with 10 mM GABA reversed the deleterious development of -Pi atgad1 plants. Our results indicate that AtGAD1 mediates GABA shunt upregulation during Pi deprivation. This bypass is hypothesized to circumvent ThDP-limited 2-OGDH activity to facilitate TCA cycle flux and respiration by -Pi Arabidopsis.
(© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.)
References: Abd El-Gawad HG, Mukherjee S, Farag R, Abd Elbar OH, Hikal M, Abou El-Yazied A, Abd Elhady SA, Helal N, ElKelish A, El Nahhas N et al. 2021. Exogenous γ-aminobutyric acid (GABA)-induced signaling events and field performance associated with mitigation of drought stress in Phaseolus vulgaris L. Plant Signaling & Behavior 16: 1853384.
Allan WL, Shelp BJ. 2006. Fluctuations of γ-aminobutyrate, γ-hydroxybutyrate, and related amino acids in Arabidopsis leaves as a function of the light-dark cycle, leaf age, and N stress. Canadian Journal of Botany 84: 1339-1346.
Arazi T, Baum G, Snedden WA, Shelp BJ, Fromm H. 1995. Molecular and biochemical analysis of calmodulin interactions with the calmodulin-binding domain of plant glutamate decarboxylase. Plant Physiology 108: 551-561.
Baum G, Chen Y, Arazi T, Takatsuji H, Fromm H. 1993. A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis. Journal of Biological Chemistry 268: 19610-19617.
Baum G, Lev-Yadun S, Fridmann Y, Arazi T, Katsnelson H, Zik M, Fromm H. 1996. Calmodulin binding to glutamate decarboxylase is required for regulation of glutamate and GABA metabolism and normal development in plants. EMBO Journal 15: 2988-2996.
Bocobza SE, Malitsky S, Araújo WL, Nunes-Nesi A, Meir S, Shapira M, Fernie AR, Aharoni A. 2013. Orchestration of thiamin biosynthesis and central metabolism by combined action of the thiamin pyrophosphate riboswitch and the circadian clock in Arabidopsis. Plant Cell 25: 288-307.
Bouché N, Fait A, Zik M, Fromm H. 2004. The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Molecular Biology 55: 315-325.
Bown AW, Shelp BJ. 2016. Plant GABA: not just a metabolite. Trends in Plant Science 21: 811-813.
Chen X, Tian Y, Xie Y, Liu Y, Liu Q, Ma F, Zhang W, Li C. 2023. GABA responds to low phosphorus stress by interfering with endogenous auxin levels in apple. Plant and Soil 490: 435-450.
Che-Othman MH, Jacoby RP, Millar AH, Taylor NL. 2020. Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytologist 225: 1166-1180.
Chevrot R, Rosen R, Haudecoeur E, Cirou A, Shelp BJ, Ron E, Faure D. 2006. GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, USA 103: 7460-7464.
Chien P-S, Chao Y-T, Chou C-H, Hsu Y-Y, Chiang S-F, Tung C-W, Chiou T-J. 2022. Phosphate transporter PHT1;1 is a key determinant of phosphorus acquisition in Arabidopsis natural accessions. Plant Physiology 190: 682-697.
DeFalco TA, Bender KW, Snedden WA. 2009. Breaking the code: Ca2+ sensors in plant signalling. Biochemical Journal 425: 27-40.
Deng X, Xu X, Liu Y, Zhang Y, Yang L, Zhang S, Xu J. 2020. Induction of γ-aminobutyric acid plays a positive role to Arabidopsis resistance against Pseudomonas syringae. Journal of Integrative Plant Biology 62: 1797-1812.
Dissanayaka DMSB, Ghahremani M, Siebers M, Wasaki J, Plaxton WC. 2021. Recent insights into the metabolic adaptations of phosphorus-deprived plants. Journal of Experimental Botany 72: 199-223.
Fixen PE, Johnston AM. 2012. World fertilizer nutrient reserves: a view to the future. Journal of the Science of Food and Agriculture 92: 1001-1005.
Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232: 51-68.
de la Fuente Cantó C, Simonin M, King E, Moulin L, Bennett MJ, Castrillo G, Laplaze L. 2020. An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. The Plant Journal 103: 951-964.
Gregory AL, Hurley BA, Tran HT, Valentine AJ, She YM, Knowles VL, Plaxton WC. 2009. In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. The Biochemical Journal 420: 57-65.
Hanson AD, Beaudoin GA, McCarty DR, Gregory JF III. 2016. Does abiotic stress cause functional B vitamin deficiency in plants? Plant Physiology 172: 2082-2097.
Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F et al. 2007. Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiology 144: 752-767.
Joshi J, Folz JS, Gregory JF III, McCarty DR, Fiehn O, Hanson AD. 2019. Rethinking the PDH bypass and GABA shunt as thiamin-deficiency workarounds. Plant Physiology 181: 389-393.
Kinnersley A, Lin F. 2000. Receptor modifiers indicate that 4-aminobutyric acid (GABA) is a potential modulator of ion transport in plants. Plant Growth Regulation 32: 65-76.
Knowles V, Plaxton WC. 2013. Quantification of total and soluble inorganic phosphate. Bio-Protocol 3: e890.
Lambers H, Plaxton WC. 2015. Phosphorus - back to the roots. In: Plaxton WC, Lambers H, eds. Phosphorus metabolism in plants. Annual plant reviews, vol. 48. Chichester, UK: John Wiley & Sons, 3-22.
Li L, Dou N, Zhang H, Wu C. 2021. The versatile GABA in plants. Plant Signaling & Behavior 16: 1862565.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene rxpression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25: 402-408.
Maruyama H, Sasaki T, Yamamoto Y, Wasaki J. 2019. AtALMT3 is involved in malate efflux induced by phosphorus deficiency in Arabidopsis thaliana root hairs. Plant and Cell Physiology 60: 107-115.
Mehta D, Ghahremani M, Pérez-Fernández M, Tan M, Schläpfer P, Plaxton WC, Uhrig RG. 2021. Phosphate and phosphite have a differential impact on the proteome and phosphoproteome of Arabidopsis suspension cell cultures. The Plant Journal 105: 924-941.
Mekonnen DW, Flügge UI, Ludewig F. 2016. Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Science 245: 25-34.
Micallef BJ, Shelp BJ. 1989. Arginine metabolism in developing soybean cotyledons: I. Relationship to nitrogen nutrition. Plant Physiology 90: 624-630.
Michaeli S, Fromm H. 2015. Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Frontiers in Plant Science 6: 419.
Miyashita Y, Good AG. 2008. Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant and Cell Physiology 49: 92-102.
O'Gallagher B, Ghahremani M, Stigter K, Walker EJL, Pyc M, Liu A-Y, MacIntosh GC, Mullen RT, Plaxton WC. 2021. Arabidopsis PAP17 is a dual-localized purple acid phosphatase up-regulated during phosphate deprivation, senescence, and oxidative stress. Journal of Experimental Botany 73: 382-399.
Pant BD, Pant P, Erban A, Huhman D, Kopka J, Scheible WR. 2015. Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant, Cell & Environment 38: 172-187.
Plaxton WC, Shane MW. 2015. The role of post-translational enzyme modifications in the metabolic adaptations of phosphorus-deprived plants. In: Plaxton WC, Lambers H, eds. Phosphorus metabolism in plants. Annual plant reviews, vol. 48. Chichester, UK: John Wiley & Sons, 99-123.
Poirier Y, Jung J-Y. 2015. Phosphate transporters. In: Plaxton WC, Lambers H, eds. Phosphorus metabolism in plants. Annual plant reviews, vol. 48. Chichester, UK: John Wiley & Sons, 125-158.
Rajani MS, Bedair MF, Li H, Duff SMG. 2021. Phenotypic effects from the expression of a deregulated AtGAD1 transgene and GABA pathway suppression mutants in maize. PLoS ONE 16: e0259365.
Raytek LM. 2022. What is the role of phosphorylation of the Ca2+/calmodulin-dependent glutamate decarboxylase isozyme AtGAD1 in response to phosphate nutrition of Arabidopsis thaliana? MSc thesis, Queen's University, Kingston, ON, Canada.
Robinson WD, Park J, Tran HT, Del Vecchio HA, Ying S, Zins JL, Patel K, McKnight TD, Plaxton WC. 2012. The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana. Journal of Experimental Botany 63: 6531-6542.
Schmidt R, Mohr H. 1981. Time-dependent changes in the responsiveness to light of phytochrome-mediated anthocyanin synthesis. Plant, Cell & Environment 4: 433-437.
Scholz SS, Reichelt M, Mekonnen DW, Ludewig F, Mithöfer A. 2015. Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Frontiers in Plant Science 6: 1128.
Seifikalhor M, Aliniaeifard S, Bernard F, Seif M, Latifi M, Hassani B, Didaran F, Bosacchi M, Rezadoost H, Li T. 2020. γ-Aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Scientific Reports 10: 3356.
Shelp BJ, Aghdam MS, Flaherty EJ. 2021. γ-aminobutyrate (GABA) regulated plant defense: mechanisms and opportunities. Plants 10: 1939.
Shelp BJ, Bown AW, McLean MD. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4: 446-452.
Shelp BJ, Bozzo GG, Trobacher CP, Chiu G, Bajwa VS. 2012. Strategies and tools for studying the metabolism and function of γ-aminobutyrate in plants. I. Pathway structure. Botany 90: 651-668.
Snedden WA, Arazi T, Fromm H, Shelp BJ. 1995. Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiology 108: 543-549.
Studart-Guimarães C, Fait A, Nunes-Nesi A, Carrari F, Usadel B, Fernie AR. 2007. Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiology 145: 626-639.
Su N, Wu Q, Chen J, Shabala L, Mithöfer A, Wang H, Qu M, Yu M, Cui J, Shabala S. 2019. GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion. Journal of Experimental Botany 70: 6349-6361.
Taylor SC, Nadeau K, Abbasi M, Lachance C, Nguyen M, Fenrich J. 2019. The ultimate qPCR experiment: producing publication quality, reproducible data the first time. Trends in Biotechnology 37: 761-774.
Turano FJ, Fang TK. 1998. Characterization of two glutamate decarboxylase cDNA clones from Arabidopsis. Plant Physiology 117: 1411-1421.
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ et al. 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195: 306-320.
Wang P, Lopes LD, Lopez-Guerrero MG, van Dijk K, Alvarez S, Riethoven JJ, Schachtman DP. 2022. Natural variation in root exudation of GABA and DIMBOA impacts the maize root endosphere and rhizosphere microbiomes. Journal of Experimental Botany 73: 5052-5066.
Wu Q, Su N, Huang X, Cui J, Shabala L, Zhou M, Yu M, Shabala S. 2021. Hypoxia-induced increase in GABA content is essential for restoration of membrane potential and preventing ROS-induced disturbance to ion homeostasis. Plant Communications 2: 100188.
Wu X, Jia Q, Ji S, Gong B, Li J, Lü G, Gao H. 2020. Gamma-aminobutyric acid (GABA) alleviates salt damage in tomato by modulating Na+ uptake, the GAD gene, amino acid synthesis and reactive oxygen species metabolism. BMC Plant Biology 20: 465.
Xu B, Sai N, Gilliham M. 2021. The emerging role of GABA as a transport regulator and physiological signal. Plant Physiology 187: 2005-2016.
Yin Y, Cheng C, Fang W. 2018. Effects of the inhibitor of glutamate decarboxylase on the development and GABA accumulation in germinating fava beans under hypoxia-NaCl stress. RSC Advances 8: 20456-20461.
Zarei A, Chiu GZ, Yu G, Trobacher CP, Shelp BJ. 2017. Salinity-regulated expression of genes involved in GABA metabolism and signaling. Botany 95: 621-627.
Zheng L, Karim MR, Hu Y-G, Shen R, Lan P. 2021. Greater morphological and primary metabolic adaptations in roots contribute to phosphate-deficiency tolerance in the bread wheat cultivar Kenong199. BMC Plant Biology 21: 381.
Zik M, Arazi T, Snedden WA, Fromm H. 1998. Two isoforms of glutamate decarboxylase in Arabidopsis are regulated by calcium/calmodulin and differ in organ distribution. Plant Molecular Biology 37: 967-975.
معلومات مُعتمدة: RGPIN/04476-2018 Natural Sciences and Engineering Research Council of Canada; RGPIN/03986-2020 Natural Sciences and Engineering Research Council of Canada; RGPIN/04928-2018 Natural Sciences and Engineering Research Council of Canada
فهرسة مساهمة: Keywords: Arabidopsis thaliana (thale cress); Pi starvation response; glutamate decarboxylase; metabolic bypasses; phosphorus nutrition; γ-aminobutyrate shunt
المشرفين على المادة: 27YLU75U4W (Phosphorus)
EC 4.1.1.15 (Glutamate Decarboxylase)
0 (Arabidopsis Proteins)
0 (Aminobutyrates)
56-12-2 (gamma-Aminobutyric Acid)
0 (Phosphates)
تواريخ الأحداث: Date Created: 20231014 Date Completed: 20231117 Latest Revision: 20231117
رمز التحديث: 20240628
DOI: 10.1111/nph.19300
PMID: 37837235
قاعدة البيانات: MEDLINE
الوصف
تدمد:1469-8137
DOI:10.1111/nph.19300