Research Advances of NDPKs in Plants

doi:10.13560/j.cnki.biotech.bull.1985.2017-0261

Abstract

Abstract: Nucleoside diphosphate kinases（NDPKs）are a class of highly conserved proteins with a size between 70 to 100 kD. They exist as hexamers in most organisms while as tetramers only in few prokaryotes. NDPKs are mainly responsible for keeping the in vivo cellular balance between nucleoside diphosphates and nucleoside triphosphates. Four types of NDPKs,i.e.,NDPKⅠ,NDPKⅡ,NDPKⅢ and NDPKⅣ,are found in plants,however,till now researches have been mainly focused on the first three. NDPKIs are found to be involved in plant growth and development,and response to abiotic stress,pathogens and hormones. NDPKⅡs take part in photosynthesis and removal of reactive oxygen species. NDPKIIIs are involved in energy metabolism and programmed cell death. NDPKIVs are only found in Arabidopsis and rice genomes and predicted to be located in endoplasmic reticulum with unknown function. Besides,NDPKs also display special functions in certain plants,such as DNA replication,starch and cellulose synthesis,auxin signaling and ribozyme activities;however,whether these functions are species-specific needs further study. This article summarizes the phylogenetic analysis and the most recent research progress on biological functions of NDPKs. Finally,the article discusses the prospect of NDPKs research,thus it will facilitate the in-depth and comprehensive study of their function in plants in the future.

Key words: nucleoside diphosphate kinase, NDPK, phylogeny analysis, function

ZHU Xin-ni, WANG Shan-shan, ZHOU Jia-qin, ZHU Shi-hua. Research Advances of NDPKs in Plants[J]. Biotechnology Bulletin, 2017, 33(11): 19-28.

References

[1] Krebs HA, Hems R. Some reactions of adenosine and inosine phosphates in animal tissues[J]. Biochim Biophys Acta, 1953, 12（1/2）：172-180.
[2] Edlund B. Purification of a nucleoside diphosphate kinase from pea seed and phosphorylation of the enzyme with adenosine（32 P）triphosphate[J]. Acta Chem Scand, 1971, 25（4）：1370-1376.
[3] Morera S, Chiadmi MG, Lascu I, et al. Mechanism of phosphate transfer by nucleoside diphosphate kinase：X-ray structures of the phosphohistidine intermediate of the enzymes from Drosophila and dictyostelium[J]. Biochemistry, 1995, 34（35）：11062-11070.
[4] Dorion S, Dumas F, Rivoal J. Autophosphorylation of Solanum chacoense cytosolic nucleoside diphosphate kinase on Ser117[J]. J Exp Bot, 2006, 57（15）：4079-4088.
[5] Johansson M, Mackenziehose A, Andersson I, et al. Structure and mutational analysis of a plant mitochondrial nucleoside diphosphate kinase. Identification of residues involved in serine phosphorylation and oligomerization[J]. Plant Physiol, 2004, 136（2）：3034-3042.
[6] Shen Y, Kim J, Song PS. Autophosphorylation of Arabidopsis nucleoside diphosphate kinase 2 occurs only on its active histidine residue[J]. Biochemistry, 2006, 45（6）：1946-1949.
[7] Dorion S, Rivoal J. Characterization of a cytosolic nucleoside diphosphate kinase associated with cell division and growth in potato[J]. Planta, 2006, 224（1）：108-124.
[8] Dorion S, Clendenning A, Rivoal J. Engineering the expression level of cytosolic nucleoside diphosphate kinase in transgenic Solanum tuberosum rootsb alters growth, respiration and carbon metabolism[J]. Plant J, 2017, 89（5）：914-926.
[9] Martínez-Esteso MJ, Sellés-Marchart S, Lijavetzky D, et al. A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism[J]. J Exp Bot, 2011, 62（8）：2521-2569.
[10] Kav NV, Srivastava S, Goonewardene L, et al. Proteome-level changes in the roots of Pisum sativum in response to salinity[J]. Ann Appl Biol, 2004, 145（2）：217-230.
[11] Zhou QY, Xie ZM, Zhang AG, et al. Cloning, expression and characterization of a nucleoside diphosphate kinase（NDPK）gene from tobacco[J]. Prog Nat Sci-Mater, 2007, 17（8）：906-912.
[12] Guo G, Lv D, Yan X, et al. Proteome characterization of developing grains in bread wheat cultivars（Triticum aestivum L.）[J]. BMC Plant Biol, 2012, 12（1）：147-171.
[13] Fatehi F, Hosseinzadeh A, Alizadeh H, et al. The Proteome response of Hordeum spontaneum to salinity stress[J]. Cereal Res Commun, 2013, 41（1）：78-87.
[14] 梁潘霞, 李杨瑞, 杨丽涛. 甘蔗核苷二磷酸激酶（NDPK1）基因克隆及表达分析[J]. 热带作物学报, 2012, 33（12）：2199-2205.
[15] Harris N, Taylor JE, Roberts JA. Isolation of a mRNA encoding a nucleoside diphosphate kinase from tomato that is up-regulated by wounding[J]. Plant Mol Biol, 1994, 25（4）：739-742.
[16] Kopylov M, Bass HW, Stroupe ME. The maize（Zea mays L.）nucleoside diphosphate kinase1（ZmNDPK1）gene encodes a human NM23-H2 homologue that binds and stabilizes G-quadruplexDNA[J]. Biochemistry, 2015, 54（9）：1743-1757.
[17] Zhang J, Fukui T, Ichikawa A. A third type of nucleoside diphosphate kinase from spinach leaves：purification, characterization and amino-acid sequence[J]. Biochim Biophys Acta, 1995, 1248（1）：19-26.
[18] Shin DH, In JG, Lim YP, et al. Molecular cloning and characterization of nucleoside diphosphate（NDP）kinases from Chinese cabbage（Brassica campestris）[J]. Mol Cells, 2004, 17（1）：86-94.
[19] Hammargren J, Sundström J, Johansson M, et al. On the phylogeny, expression and targeting of plant nucleoside diphosphate kinases[J]. Physiol Plantarum, 2007, 129（1）：79-89.
[20] Ovečka M, Takáč T, Komis G, et al. Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis[J]. J Exp Bot, 2014, 65（9）：2335-2350.
[21] 王凤茹, 董金皋, 司贺龙, 等. 水稻OsNDPK1基因在提高植物抗病性方面的应用：中国, CN201210143843. 8[P]. 2013-11-13.
[22] Pan L, Kawai M, Yano A, et al. Nucleoside diphosphate kinase required for coleoptile elongation in rice[J]. Plant Physiol, 2000, 122（2）：447. 452.
[23] Yano A, Umeda M, Uchimiya H. Expression of functional proteins of cDNA encoding rice nucleoside diphosphate kinase（NDK）in Escherichia coli, and organ-related alteration of NDK activities during rice seed germination（Oryza sativa, L.）[J]. Plant Mol Biol, 1995, 27（5）：1053-1058.
[24] Lee DG, Ahsan N, Lee SH, et al. An approach to identify cold-induced low-abundant proteins in rice leaf[J]. CR Biol, 2007, 330（3）：215-225.
[25] Chen JH, Tian L, Xu HF, et al. Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis[J]. Plant Omics J Plant, 2012, 5（2）：194-199.
[26] Lin SK, Chang MC, Tsai YG, et al. Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression[J]. Proteomics, 2005, 5（8）：2140-2156.
[27] Kawasaki S, Borchert C, Deyholos M, et al. Gene expression profiles during the initial phase of salt stress in rice[J]. Plant Cell, 2001, 13（4）：889-905.
[28] Cho SM, Shin SH, Kim KS, et al. Enhanced expression of a gene encoding a nucleoside diphosphate kinase 1（OsNDPK1）in rice plants upon infection with bacterial pathogens[J]. Mol Cells, 2004, 18（3）：390-395.
[29] 凌丹燕, 路梅. 细菌性条斑病菌JH01诱导水稻抗病均一化差减文库的构建[J]. 安徽农业科学, 2016（2）：188-191.
[30] Ahsan N, Lee DG, Lee KW, et al. Glyphosate-induced oxidative stress in rice leaves revealed by proteomic approach[J]. Plant Physiol Bioch, 2008, 46（12）：1062-1070.
[31] Salekdeh GH, Siopongco J, Wade LJ, et al. Proteomic analysis of rice leaves during drought stress and recovery[J]. Proteomics, 2002, 2（9）：1131-45.
[32] Ishikawa T, Morimoto Y, Madhusudhan R, et al. Acclimation to diverse environmental stresses caused by a suppression of cytosolic ascorbate peroxidase in tobacco BY-2 cells[J]. Plant Cell Physiol, 2005, 46（8）：1264-1271.
[33] Choi G, Yi H, Lee J, et al. Phytochrome signalling is mediated through nucleoside diphosphate kinase 2[J]. Nature, 1999, 401（6753）：610-613.
[34] Choi G, Kim JI, Hong SW, et al. A possible role for NDPK2 in the regulation of auxin-mediated responses for plant growth and development[J]. Plant Cell Physiol, 2005, 46（8）：1246-1254.
[35] Seong ES, Guo J, Kim YH, et al. Regulations of marker genes involved in biotic and abiotic stress by overexpression of the AtNDPK2 gene in rice[J]. Biochem Bioph Res Co, 2007, 363（1）：126-132.
[36] Shen Y, Han Y, Kim J, et al. Arabidopsis nucleoside diphosphate kinase-2 as a plant GTPase activating protein[J]. Bmb Rep, 2008, 41（9）：645-650.
[37] Fukamatsu Y, Yabe N, Hasunuma K. Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases[J]. Plant Cell Physiol, 2003, 44（10）：982-989.
[38] Moon H, Lee B, Choi G, et al. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants[J]. P Natl Acad Sci USA, 2003, 100（1）：358-363.
[39] Hamada T, Tanaka N, Noguchi T, et al. Phytochrome regulates phosphorylation of a protein with characteristics of a nucleoside diphosphate kinase in the crude membrane fraction from stem sections of etiolated pea seedlings[J]. J Photoch Photobio B Bio, 1996, 33（2）：143-151.
[40] Tanaka N, Ogura T, Noguchi T, et al. Phytochrome-mediated light signals are transduced to nucleoside diphosphate kinase in Pisumsativum L. cv. Alaska[J]. J Photoch Photobio B, 1998, 45（2-3）：113-121.
[41] Haque ME, Yoshida Y, Hasunuma K. ROS resistance in Pisum sativum cv. Alaska：the involvement of nucleoside diphosphate kinase in oxidative stress responses via the regulation of antioxidants[J]. Planta, 2010, 232（2）：367-382.
[42] 白晓娟, 刘丽娟, 张春华, 等. H 2 O 2 预处理对不同水稻品种Cd耐性的影响[J]. 中国水稻科学, 2010, 24（4）：391-397.
[43] 丁艳, 韩卓, 王泽港, 等. 不同基因型玉米幼苗对低磷条件的响应[J]. 中国农学通报, 2011, 27（30）：32-34.
[44] Zhang J, Fukui T, Ichikawa A. A third type of nucleoside diphosphate kinase from spinach leaves：purification, characterization and amino-acid sequence[J]. Biochim Biophys Acta, 1995, 1248（1）：19-26.
[45] Valenti D, Vacca RA, Pinto MCD, et al. In the early phase of programmed cell death in Tobacco Bright Yellow 2 cells the mitochondrial adenine nucleotide translocator, adenylate kinase and nucleoside diphosphate kinase are impaired in a reactive oxygen species-dependent manner[J]. Biochim Biophys Acta, 2007, 1767（1）：66-78.
[46] EscobarGalvis ML, Håkansson G, Alexciev K, et al. Cloning and characterisation of a pea mitochondrial NDPK[J]. Biochimie, 1999, 81（12）：1089-1096.
[47] Galvis MLE, Marttila S, HaKansson G, et al. Heat stress response in pea involves interaction of mitochondrial nucleoside diphosphate kinase with a novel 86-kilodalton protein[J]. Plant Physiol, 2001, 126（1）：69-77.
[48] Knorpp C, Johansson M, Baird AM. Plant mitochondrial nucleoside diphosphate kinase is attached to the membrane through interaction with the adenine nucleotide translocator[J]. Febs Letters, 2003, 555（2）：363-366.
[49] Galvis MLE, Marttila S, HaKansson G, et al. Heat stress response in pea involves interaction of mitochondrial nucleoside diphosphate kinase with a novel 86-kilodalton protein[J]. Plant Physiol, 2001, 126（1）：69-77.
[50] Johansson M. The role of nucleoside diphosphate kinase in plant mitochondria[D]. Acta U Agr Sueciae, 2006.
[51] Monika J, Jenni H, Eva U, et al. The activities of nucleoside diphosphate kinase and adenylate kinase are influenced by their interaction[J]. Plant Sci, 2008, 174（2）：192-199.
[52] Hammargren J, Sundström J, Johansson M, et al. On the phylogeny, expression and targeting of plant nucleoside diphosphatekinases[J]. Physiol Plantarum, 2007, 129（1）：79-89.
[53] Hammargren J, Salinas T, Maréchal-Drouard L, et al. The pea mitochondrial nucleoside diphosphate kinase cleaves DNA and RNA[J]. Febs Letters, 2007, 581（18）：3507-3511.
[54] Hammargren J, Rosenquist S, Jansson C, et al. A novel connection between nucleotide and carbohydrate metabolism in mitochondria：sugar regulation of the Arabidopsis, nucleoside diphosphate kinase 3a gene[J]. Plant Cell Rep, 2008, 27（3）：529-534.
[55] Kihara A, Saburi W, Wakuta S, et al. Physiological and biochemical characterization of three nucleoside diphosphate kinase isozymes from rice（Oryza sativa L.）[J]. Biosci Biotech Bioch, 2011, 75（9）：1740-1745.
[56] Manigbas NL, Park DS, Park SK, et al. Enhanced tolerance of transgenic rice overexpressing Arabidopsis thaliana nucleoside diphosphate kinase（AtNDPK2）against various environmental stresses[J]. Philipp Agric Sci, 2011, 94（1）：29-37.
[57] Hetmann A, Kowalczyk S. Nucleoside diphosphate kinase isoforms regulated by phytochrome A isolated from oat coleoptiles[J]. Acta Biochimica Poloni, 2009, 56（1）：143-153.
[58] Zrenner R, Stitt M, Sonnewald U, et al. Pyrimidine and purine biosynthesis and degradation in plants[J]. Annu Rev Plant Biol, 2006, 57（1）：805-836.
[59] Anderca MI, Furuichi T, Muto S. Mitochondrial NDP kinase from Dunaliella tertiolecta（Chlorophyceae, Chlorophyta）[J]. Phycol Res, 2003, 51（3）：147-153.
[60] Dharmasiri S, Harrington HM, Dharmasiri N. Heat shock modulates phosphorylation status and activity of nucleoside diphosphate kinase in cultured sugarcane cells[J]. Plant Cell Rep, 2010, 29（11）：1305-1314.
[61] Cao TS, Srivastava S, Rahman MH, et al. Proteome-level changes in the roots of Brassica napus as a result of Plasmodiophora brassicae infection[J]. Plant Sci, 2008, 174（1）：97-115.
[62] Sharma N, Rahman MH, Strelkov S, et al. Proteome-level changes in two Brassica napus lines exhibiting differential responses to the fungal pathogen Alternaria brassicae[J]. Plant Sci, 2007, 172（1）：95-110.
[63] Postel EH. Multiple biochemical activities of NM23/NDP kinase in gene regulation[J]. J Bioenerg Biomer, 2003, 35（1）：31-40.
[64] Lübeck J, Soll J. Nucleoside diphosphate kinase from pea chloroplasts：purification, cDNA cloning and import into chloroplasts[J]. Planta, 1995, 196（4）：668-673.
[65] Bovet L, Meylan-Bettex M, Eggman T, et al. CDP phosphotransferase activity in spinach intact chloroplasts：Possible involvement of nucleoside diphosphate kinase II[J]. Plant Physiol Bioch, 1999, 37（37）：645-652.
[66] Hamada T, Hasunuma K, Komatsu S. Phosphorylation of proteins in the stem section of etiolated rice seedling irradiated with red light[J]. Biol Pharm Bull, 1999, 22（2）：122-126.
[67] Ito K, Hamada T, Hasunuma K. Blue light signal transmission to 15 kDa proteins in the crude membrane fraction from the stem section of etiolated pea seedlings[J]. J Photoch Photobio B, 1995, 28（3）：223-227.
[68] Im YJ, Kim JI, Shen Y, et al. Structural analysis of Arabidopsis thaliana nucleoside diphosphate kinase-2 for phytochrome-mediated light signaling[J]. J Mol Biol, 2004, 343（3）：659-670.
[69] Kim JI, Song PS. Phytochrome phosphorylation modulates light signaling by influencing the protein-protein interaction[J]. Plant Cell, 2004, 16（10）：2629-2640.
[70] Hetmann A, Wujak M, Kowalczyk S. Protein transphosphorylation during the mutual interaction between phytochrome a and a nuclear isoform of nucleoside diphosphate kinase is regulated by red light[J]. Biochemistry, 2016, 81（10）：1153-1162.
[71] 王丽娜, 王丽艳, 刘景文, 等. AtNDPK2基因转化敖汉苜蓿及其耐盐性分析[J]. 激光生物学报, 2014, 23（1）：65-70.
[72] 侯夫云, 赵兵, 王庆美, 等. 转AtNDPK2基因甘薯的耐盐性鉴定[J]. 山东农业科学, 2014（2）：29-31.
[73] Kim YH, Kim MD, Choi YI, et al. Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance[J]. Plant Biotechnol J, 2011, 9（3）：334-347.
[74] Manigbas NL, Park DS, Park SK, et al. Enhanced tolerance of transgenic rice overexpressing Arabidopsis thaliana nucleoside diphosphate kinase（AtNDPK2）against various environmental stresses[J]. Philipp Agric Sci, 2011, 94（1）：29-37.
[75] Kim YH, Lim S, Yang KS, et al. Expression of Arabidopsis NDPK2 increases antioxidant enzyme activities and enhances tolerance to multiple environmental stresses in transgenic sweet potato plants[J]. Mol Breeding, 2009, 24（3）：233-244.
[76] Tang L, Kim MD, Yang KS, et al. Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase2 against multiple environmental stresses[J]. Transgenic Res, 2008, 17（4）：705-715.
[77] Verslues PE, Batelli G, Grillo S, et al. Interaction of SOS2 with nucleoside diphosphate kinase 2 and catalases reveals a point of connection between salt stress and H 2 O 2 signaling in Arabidopsis thaliana[J]. Mol Cell Biol, 2007, 27（22）：7771-7780.
[78] Yang KA, Moon H, Kim G, et al. NDP kinase 2 regulates expression of antioxidant genes in Arabidopsis[J]. P Jpn Acad B-Phys, 2003, 79（3）：86-91.
[79] Spetea C, Hundal T, Lundin B, et al. Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen[J]. P Natl Acad Sci USA, 2004, 101（5）：1409-1414.
[80] Monika J, Jenni H, Eva U, et al. The activities of nucleoside diphosphate kinase and adenylate kinase are influenced by their interaction[J]. Plant Sci, 2008, 174（2）：192-199.
[81] Matsushita Y, Suzuki T, Kubota R, et al. Isolation of a cDNA for a nucleoside diphosphate kinase capable of phosphorylating the kinase domain of the self-incompatibility factor SRK of Brassica campestris[J]. J Exp Bot, 2002, 53（369）：765-767.