Overexpression of PtPEPCK1 gene promotes nitrogen metabolism in poplar

Lina Wang , Miao He , Song Chen , Kean Wang , Donghai Cui , Xin Huang , Lijie Liu

Journal of Forestry Research ›› 2019, Vol. 30 ›› Issue (6) : 2289 -2303.

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Journal of Forestry Research ›› 2019, Vol. 30 ›› Issue (6) : 2289 -2303. DOI: 10.1007/s11676-019-01042-4
Original Paper

Overexpression of PtPEPCK1 gene promotes nitrogen metabolism in poplar

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Abstract

To understand the function of phosphoenolpyruvate carboxylase kinase, we introduced PtPEPCK1 gene under the control of 35S promoter into 84K poplar (Populus alba ×  P. glandulosa). PtPEPCK1 gene is well-known for its role in gluconeogenesis. However, our data confirmed that it has significant effects on amino acid biosynthesis and nitrogen metabolism. Immunohistochemistry and fluorescence microscopy indicate that PtPEPCK1 is specifically expressed in the cytoplasm of the spongy and palisade tissues. Overexpression of PtPEPCK1 was characterized through transcriptomics and metabolomics. The metabolites concentration of the ornithine cycle and its precursors also increased, of which N-acetylornithine was up-regulated almost 50-fold and ornithine 33.7-fold. These were accompanied by a massive increase in levels of several amino acids. Therefore, overexpression of PtPEPCK1 increases amino acid levels with urea cycle disorder.

Keywords

Amino acid metabolism / Metabolome / Nitrogen metabolism / Phosphoenolpyruvate carboxylase kinase / Transcriptome / Urea cycle

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Lina Wang, Miao He, Song Chen, Kean Wang, Donghai Cui, Xin Huang, Lijie Liu. Overexpression of PtPEPCK1 gene promotes nitrogen metabolism in poplar. Journal of Forestry Research, 2019, 30(6): 2289-2303 DOI:10.1007/s11676-019-01042-4

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References

[1]

Azevedo RA, Arruda P, Turner WL, Peter JL. ChemInform abstract: biosynthesis and metabolism of the aspartate-derived amino acids in higher plants. Cheminform, 1998, 29(2): 395-419.

[2]

Bahrami AR, Chen ZH, Walker RP, Leegood R, Gray JE. Ripening-related occurrence of phosphoenolpyruvate carboxykinase in tomato fruit[J]. Plant Mol Biol, 2001, 47(4): 499-506.

[3]

Balint T, Rengel Z. Amino acid composition of xylem and phloem sap varies in canola genotypes differing in nitrogen- and sulfur-use efficiency. Crop Pasture Sci, 2011, 62(3): 198-207.

[4]

Chao YP, Liao JC. Metabolic responses to substrate futile cycling in Escherichia coli. J Biol Chem, 1994, 269(7): 5122-5126.

[5]

Chen ZH, Walker RP, Acheson R, Técsi LI, Wingler A, Lea PJ, Leegood R. Are isocitrate lyase and phosphoenolpyruvate carboxykinase involved in gluconeogenesis during senescence of barley leaves and cucumber cotyledons?. Plant Cell Physiol, 2000, 41(8): 960-967.

[6]

Chen ZH, Walker RP, Acheson RM, Leegood RC. Phosphoenolpyruvate carboxykinase assayed at physiological concentrations of metal ions has a high affinity for CO2. Plant Physiol, 2002, 128(1): 160-164.

[7]

Choi DS, Kim NH, Hwang BK. The pepper phosphoenolpyruvate carboxykinase capepck1 is involved in plant immunity against bacterial and oomycete pathogens. Plant Mol Biol, 2015, 89(1–2): 99-111.

[8]

Christian OB, Alexander S. The malate dehydrogenase of ralstonia eutropha and functionality of the C3/C4 metabolism in a Tn5-induced mdh mutant. FEMS Microbiol Lett, 2002, 212(2): 159-164.

[9]

Confalonieri M, Balestrazzi A, Bisoffi S. Genetic transformation of Populus nigra by Agrobacterium tumefaciens. Plant Cell Rep, 1994, 13(5): 256-261.

[10]

Delgado-Alvarado A, Walker RP, Leegood RC. Phosphoenolpyruvate carboxykinase in developing pea seeds is associated with tissues involved in solute transport and is nitrogen-responsive. Plant, Cell Environ, 2010, 30(2): 225-235.

[11]

Du SC, Kim NH, Hwang BK. The pepper phosphoenolpyruvate carboxykinase CaPEPCK1 is involved in plant immunity against bacterial and oomycete pathogens. Plant Mol Biol, 2015, 89(1–2): 99-111.

[12]

Edwards GE, Kanai R, Black CC. Phosphoenolpyruvate carboxykinase in leaves of certain plants which fix CO2 by the C4-dicarboxylic acid cycle of photosynthesis. Biochem Biophys Res Commun, 1971, 45(2): 278-285.

[13]

Famiani F, Paoletti A, Proietti P, Battistelli A, Moscatello S. The occurrence of phosphoenolpyruvate carboxykinase (PEPCK) in the pericarp of different grapevine genotypes and in grape leaves and developing seeds. J Hortic Sci Biotechnol, 2018, 23: 1-10.

[14]

Felice BD, Manfellotto F, Raffaella D, Olga DC, Antonietta DM, Marco T. Comparative transcriptional analysis reveals differential gene expression between Sand Daffodil tissues. Genetica, 2013, 141(10–12): 443-452.

[15]

Habash DZ, Bernard SM. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol, 2009, 182(3): 608-620.

[16]

Hu YB, Bellaloui N, Sun GY, Tigabu M, Wang JH. Exogenous sodium sulfide improves morphological and physiological responses of a hybrid Populus species to nitrogen dioxide. J Plant Physiol, 2014, 171(10): 868-875.

[17]

Huang YX, Yin YG, Sanuki A, Fukuda N, Ezura H, Matsukura C. Phosphoenolpyruvate carboxykinase (PEPCK) deficiency affects the germination, growth and fruit sugar content in tomato (Solanum lycopersicum L.). Plant Physiol Biochem, 2015, 96: 417-425.

[18]

Hussain SS, Kayani MA, Amjad M. Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol Prog, 2011, 27(2): 297-306.

[19]

Jiang F, Chen XP, Hu WS, Zheng SQ. Identification of differentially expressed genes implicated in peel color (red and green) of Dimocarpus confinis. SpringerPlus, 2016 5 1 1088

[20]

Lea PJ, Chen ZH, Leegood R, Walker RP. Does phosphoenolpyruvate carboxykinase have a role in both amino acid and carbohydrate metabolism?. Amino Acids, 2001, 20(3): 225-241.

[21]

Leegood RC, Ap RT. Identification of the regulatory steps in gluconeogenesis in cotyledons of Cucurbita pepo. Biochim Biophys Acta, 1978, 524(1): 1-11.

[22]

Leegood RC, Walker RP. Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Biochem Biophys, 2003, 414(2): 204-210.

[23]

Li TQ, Liu XF, Wan YM, Li ZH, Qi GH, Li YY, Liu XX, He R, Ma Y, Ma H. Transcriptome analysis for (plant species with extremely small populations) based on high throughput sequencing. Bull Bot Res, 2017, 37(6): 825-834.

[24]

Liu KY, Ba XL, Yu JZ, Li J, Wei KQ, Han GD, Li GP, Cui Y. The phosphoenolpyruvate carboxykinase of mycobacterium tuberculosis, induces strong cell-mediated immune responses in mice. Mol Cell Biochem, 2006, 288(1–2): 65-71.

[25]

Maciaga M, Paszkowski A. Genetic control of aspartate aminotransferase isoenzymes in Aegilops and Triticum species. J Appl Genet, 2004, 45(4): 411-417.

[26]

Majumdar R, Minocha R, Minocha SC, D’Mello JPF (2015) Ornithine: at the crossroads of multiple paths to amino acids and polyamines. CAB International, pp 156–172

[27]

Manzoor H, Kelloniemi J, Chiltz A, Wendehenne D, Alain P, Poinssot B, Garcia-Brugger A. Involvement of the glutamate receptor atglr3.3 in plant defense signaling and resistance to hyaloperonospora arabidopsidis. Plant J, 2013, 76(3): 466-480.

[28]

Martín M, Rius SP, Podestá FE. Two phosphoenolpyruvate carboxykinases coexist in the crassulacean acid metabolism plant Ananas comosus. Isolation and characterization of the smaller 65 kDa form. Plant Physiol Biochem, 2011, 49(6): 646-653.

[29]

Mattoo AK, Fatima T, Upadhyay RK, Handa AK. D’Mello JPF. Polyamines in plants: biosynthesis from arginine, and metabolic, physiological and stress-response roles. Amino acids in higher plants, 2015, Wallingford: CAB International 177 194

[30]

Meijer AJ, Lamers WH, Chamuleau RA. Nitrogen metabolism and ornithine cycle function. Physiol Rev, 1990, 70(3): 701-748.

[31]

Movahedi A, Zhang J, Amirian R, Zhuge Q. An efficient agrobacterium-mediated transformation system for poplar. Int J Mol Sci, 2014, 15(6): 10780-10793.

[32]

Murooka Y, Mori Y, Hayashi M. Variation of the amino acid content of Arabidopsis seeds by expressing soybean aspartate aminotransferase gene. J Biosci Bioeng, 2002, 94(3): 225-230.

[33]

Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng, 2007, 104(1): 34-41.

[34]

Osorio S, Vallarino JG, Szecowka M, Ufaz S, Tzin V, Angelovici R, Gad G, Fernie RA. Alteration of the interconversion of pyruvate and malate in the plastid or cytosol of ripening tomato fruit invokes diverse consequences on sugar but similar effects on cellular organic acid, metabolism, and transitory starch accumulation. Plant Physiol, 2013, 161(2): 628-643.

[35]

Owen OE, Kalhan SC, Hanson RW. The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem, 2002, 277(34): 30409-30412.

[36]

Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VP, Frommer WB. Overexpression of glutamine dumper1 leads to hypersecretion of glutamine from hydathodes of arabidopsis leaves. Plant Cell, 2004, 16(7): 1827-1840.

[37]

Pinto H, Sharwood RE, Tissue DT, Ghannoum O. Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2. J Exp Bot, 2014, 65(13): 3669-3681.

[38]

Price MB, Kong D, Okumoto S. Inter-subunit interactions between glutamate-like receptors in Arabidopsis. Plant Signal Behav, 2013 8 12 e27034

[39]

Roosens NH, Bitar FA, Loenders K, Angenon G, Jacobs M. Overexpression of ornithine-δ-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breeding, 2002, 9(2): 73-80.

[40]

Shi JH, Yi KK, Yu L, Li X, Zhou ZJ, Chen Y, Hu ZH, Tao Z, Liu RH, Chen YL, Chen JQ. Phosphoenolpyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol, 2015, 167(3): 671-681.

[41]

Sun Su. Functional analysis of photosynthesis by transgenic maize ZmPCK1 gene. Jilin Agric Univ, 2018, 1(1): 11-13.

[42]

Urbina JA, Osorno CE, Rojas A. Inhibition of phosphoenolpyruvate carboxykinase from Trypanosoma (Schizotrypanum) cruzi epimastigotes by 3-mercaptopicolinic acid: in vitro and in vivo studies. Arch Biochem Biophys, 1990, 282(1): 91-99.

[43]

Walker RP, Chen ZH. Phosphoenolpyruvate carboxykinase: structure, function and regulation. Adv Bot Res, 2002, 38(02): 93-189.

[44]

Walker RP, Leegood R. Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds. Biochem J, 1996, 317(3): 653-658.

[45]

Walker R, Tecsi L, Famiani FP, Leegood R, Chen Z. Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development. Planta, 1999, 210(1): 9-18.

[46]

Walker RP, Benincasa P, Battistelli A, Moscatello S, Técsi L, Leegood RC, Famiani F. Gluconeogenesis and nitrogen metabolism in maize. Plant Physiol Biochem, 2018, 130: 324-333.

[47]

Wang JY. Amino acid metabolism. Biochemistry, 2011, 31: 340-341.

[48]

Wang LN, Wang YC, Yang CP. The comparative study of callus and direct differentiation regeneration system of 84K poplar. Bull Bot Res, 2017, 37(4): 542-548.

[49]

Wingler A. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol, 1999, 120(2): 539-546.

[50]

Yu ZH (2012) Research and application of HPCE-TOF/MS technology in the analysis of common toxic alkaloids. Doctoral dissertation, Fudan University, pp 8–11

[51]

Zeng J, Kuang H, Hu C, Shi X, Yan M, Xu L, Xu GW. Effect of bisphenol a on rat metabolic profiling studied by using capillary electrophoresis time-of-flight mass spectrometry. Environ Sci Technol, 2013, 47(13): 7457-7465.

[52]

Zhao JX (2016) A new method based on CE-MS for metabolomics analysis and its application in tobacco research. Doctoral dissertation, Dalian University of Technology, pp 43–45

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