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ThPP1 gene, encodes an inorganic pyrophosphatase in Thellungiella halophila, enhanced the tolerance of the transgenic rice to alkali stress

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An inorganic pyrophosphorylase gene, ThPP1 , modulated the accumulations of phosphate and osmolytes by up-regulating the differentially expression genes, thus enhancing the tolerance of the transgenic rice to alkali stress (AS).

Abstract

Inorganic pyrophosphorylase is essential in catalyzing the hydrolysis of pyrophosphate to inorganic phosphate during plant growth. Here, we report the changes of physiological osmolytes and differentially expression genes in the transgenic rice overexpressing a soluble inorganic pyrophosphatase gene ThPP1 of Thellungiella halophila in response to AS. Analyses showed that the ThPP1 gene was a PPase family I member which is located to the cytoplasm. Data showed that the transgenic lines revealed an enhanced tolerance to AS compared to the wild type, and effectively increased the accumulations of inorganic phosphate and organic small molecules starch, sucrose, proline and chlorophyll, and maintained the balance of osmotic potential by modulating the ratio of Na+/K+ in plant cells. Under AS, total 379 of differentially expression genes were up-regulated in the leaves of the transgenic line compared with control, and the enhanced tolerance of the transgenic rice to the AS seemed to be associated with the up-regulations of the osmotic stress-related genes such as the L-type lectin-domain containing receptor kinase (L-type LecRK), the cation/H+ antiporter gene and the vacuolar cation/proton exchanger 1 gene (CAX1), which conferred the involvements in the biosynthesis and metabolic pathways. Protein interaction showed that the ThPP1 protein specifically interacted with a 16# target partner of the photosystem II light-harvesting-Chl-binding protein. This study suggested that the ThPP1 gene plays an important regulatory role in conferring the tolerance of the transgenic rice to AS, and is an effective candidate in molecular breeding for crop cultivation of the alkali tolerance.

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References

  • Ahn S, Milner AJ, Fütterer K, Konopka M, Ilias M, Young TW (2001) The “open” and “closed” structures of the type-c inorganic pyrophosphatases from Bacillus subtilis and Streptococcus gordonii. J Mol Biol 313:797–811

    Article  CAS  PubMed  Google Scholar 

  • Baliardini C, Corso M, Verbruggen N (2016) Transcriptomic analysis supports the role of cation exchanger 1 in cellular homeostasis and oxidative stress limitation during cadmium stress. Plant Signal Behav 11(e1183861):1–5

    Google Scholar 

  • Baltscheffsky M, Schultz A, Baltscheffsky H (1999) H+-PPases: a tightly membrane-bound family. FEBS Lett 457:527–533

    Article  CAS  PubMed  Google Scholar 

  • Carman GM, Han GS (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem Sci 31:694–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho D, Villiers F, Kroniewicz L, Lee S, Seo YJ, Hirschi KD, Leonhardt N, Kwak JM (2012) Vacuolar cax1 and cax3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol 160:1293–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Wang Q (2006) Physiological responses of maize to elemental sulphur and cadmium stress. Plant Soil Environ 52:523–529

    CAS  Google Scholar 

  • Deng K, Wang Q, Zeng J, Guo X, Zhao X, Tang D, Liu X (2009) A lectin receptor kinase positively regulates ABA response during seed germination and is involved in salt and osmotic stress response. J Plant Biol 52:493–500

    Article  CAS  Google Scholar 

  • Geigenberger P, Hajirezaei M, Geiger M, Deiting U, Sonnewald U, Stitt M (1998) Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversions, and increased levels of nucleotides in growing potato tubers. Planta 205:428–437

    Article  CAS  PubMed  Google Scholar 

  • George GM, Van MJ, Nunesnesi A, Bauer R, Fernie AR, Kossmann J (2010) Virus-induced gene silencing of plastidial soluble inorganic pyrophosphatase impairs essential leaf anabolic pathways and reduces drought stress tolerance in Nicotiana benthamiana. Plant Physiol 154:55–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Luna FM, Sancha ENDL, Vázquez-Santana S, Rodríguez-Sotres R (2016) Evidence for a non-overlapping subcellular localization of the family I isoforms of soluble inorganic pyrophosphatase in Arabidopsis thaliana. Plant Sci 253:229–242

    Article  PubMed  Google Scholar 

  • Haffani S, Mezni M, Slama I, Ksontini M, Chaïbi W (2014) Plant growth, water relations and proline content of three vetch species under water-limited conditions. Grass Forage Sci 69:323–333

    Article  CAS  Google Scholar 

  • Harold FM (1966) Inorganic polyphosphates in biology: structure, metabolism, and function. Bacteriol Rev 30:772–794

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:258–261

    Article  Google Scholar 

  • Heikinheimo P, Lehtonen J, Baykov A, Lahti R, Cooperman BS, Goldman A (1996) The structural basis for pyrophosphatase catalysis. Structure 4:1491–1508

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Domíguez EE, Valencia-Turcotte LG, Rodríguez-Sotres R (2012) Changes in expression of soluble inorganic pyrophosphatases of Phaseolus vulgaris under phosphate starvation. Plant Sci 187:39–48

    Article  PubMed  Google Scholar 

  • Hong Z (2000) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Yuan Q, Wang Y, Cai R, Deng X, Wang J, Zhou S, Chen M, Chen L, Huang C, Ma Z, Yang G, He G (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53:2127–2141

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Fan LL, Yang SJ, Kuo SY, Pan RL (1997) Purification and characterization of thylakoid membrane-bound inorganic pyrophosphatase from Spinacia oleracea L. Arch Biochem Biophys 346:105–112

    Article  CAS  PubMed  Google Scholar 

  • Kajander T, Kellosalo J, Goldman A (2013) Inorganic pyrophosphatases: one substrate, three mechanisms. FEBS Lett 587:1863–1869

    Article  CAS  PubMed  Google Scholar 

  • Ko KM, Lee W, Yu JR, Ahnn J (2007) PYP-1, inorganic pyrophosphatase, is required for larval development and intestinal function in C. elegans. FEBS Lett 581:5445–5453

    Article  CAS  PubMed  Google Scholar 

  • Lee HS, Cho Y, Kim YJ, Lho TO, Cha SS, Lee JH, Kang SG (2009) A novel inorganic pyrophosphatase in Thermococcus onnurineus NA1. FEMS Microbiol Lett 300:68–74

    Article  CAS  PubMed  Google Scholar 

  • Leyva A, Quintana A, Sanchez M, Rodriguez EN, Cremata J, Sanchez JC (2008) Rapid and sensitive anthrone-sulfuric acid assay in microplate format to quantify carbohydrate in biopharmaceutical products: method development and validation. Biologicals 36:134–141

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López-Marqués RL, Pérez-Castiñeira JR, Losada M, Serrano A (2004) Differential regulation of soluble and membrane-bound inorganic pyrophosphatases in the photosynthetic bacterium Rhodospirillum rubrum provides insights into pyrophosphate-based stress bioenergetics. J Bacteriol 186:5418–5426

    Article  PubMed  PubMed Central  Google Scholar 

  • Maeshima M (2000) Vacuolar H+-pyrophosphatase. Biochem Biophys Acta 1465:37–51

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto T, Lian HL, Su WA, Tanaka D, Liu CW, Iwasaki I, Kitagawa Y (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50:216–229

    Article  CAS  PubMed  Google Scholar 

  • Merckel MC, Fabrichniy IP, Salminen A, Kalkkinen N, Baykov AA, Lahti R, Goldman A (2001) Crystal structure of Streptococcus mutans pyrophosphatase: a new fold for an old mechanism. Structure 9:289–297

    Article  CAS  PubMed  Google Scholar 

  • Minoru K, Susumu G, Miho F, Mao T, Mika H (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38:355–360

    Article  Google Scholar 

  • Möckli N, Deplazes A, Hassa PO, Zhang ZL, Peter M, Hottiger MO, Stagljar I, Auerbach D (2007) Yeast split-ubiquitin-based cytosolic screening system to detect interactions between transcriptionally active proteins. Biotechniques 42:725–730

    Article  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Oksanen E, Ahonen AK, Tuominen H, Tuominen V, Lahti R, Goldman A, Heikinheimo P (2007) A complete structural description of the catalytic cycle of yeast pyrophosphatase. Biochemistry 46:1228–1239

    Article  CAS  PubMed  Google Scholar 

  • Öztürk ZN, Greiner S, Rausch T (2014) Subcellular localization and developmental regulation of cytosolic, soluble pyrophosphatase isoforms in Arabidopsis thaliana. Turk J Bot 38:1036–1049

    Article  Google Scholar 

  • Öztürk ZN, Greiner S, Rausch T (2015) Differential expression of soluble pyrophosphatase isoforms in Arabidopsis upon external stimuli. Turk J Bot 39:571–579

    Article  Google Scholar 

  • Petreikov M, Eisenstein M, Yeselason Y, Preiss J, Schaffer A (2010) Characterization of the AGPase large subunit isoforms from tomato indicates that the recombinant L3 subunit is active as a monomer. Biochem J 428:201–212

    Article  CAS  PubMed  Google Scholar 

  • Rojas-Beltrán JA, Dubois F, Mortiaux F, Portetelle D, Gebhardt C, Sangwan RS, Du Jardin P (1999) Identification of cytosolic Mg2+-dependent soluble inorganic pyrophosphatases in potato and phylogenetic analysis. Plant Mol Biol 39:449–461

    Article  PubMed  Google Scholar 

  • Schulze S, Mant A, Kossmann J, Lloyd J (2004) Identification of an Arabidopsis inorganic pyrophosphatase capable of being imported into the chloroplast. FEBS Lett 565:101–105

    Article  CAS  PubMed  Google Scholar 

  • Shi D, Yin L (1993) Difference between salt (NaCl) and alkaline (Na2CO3) stresses on Puccinellia tenuiflora (Griseb.) Scribn. et Merr. plants. J Integr Plant Biol 35:144–149

    CAS  Google Scholar 

  • Smart LB, Vojdani F, Maeshima M, Wilkins TA (1998) Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiol 116:1539–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernon DM, Bohnert HJ (1992) A novel methyl transferase induced by osmotic stress in the facultative Mesembryanthemum crystallinum. EMBO J 11:2077–2085

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vianello A, Macrí F (1999) Proton pumping pyrophosphatase from higher plant mitochondria. Physiol Plant 105:763–768

    Article  CAS  Google Scholar 

  • Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. Plant J 48:342–353

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  PubMed  Google Scholar 

  • Wu GQ, Xi JJ, Wang SM (2011) The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. J Plant Physiol 168:51149–51159

    Google Scholar 

  • Wu ZH, Yang CW, Yang MY (2014) Photosynthesis, photosystem II efficiency, amino acid metabolism and ion distribution in rice (Oryza sativa, L.) in response to alkaline stress. Photosynthetica 52:157–160

    Article  CAS  Google Scholar 

  • Xin SC, Yu GH, Sun LL, Qiang XJ, Xu N, Cheng XG (2014) Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in the transgenic Arabidopsis and interacts with target proteins. J Plant Res 127:695–708

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:293–297

    Article  Google Scholar 

  • Young TW, Kuhn NJ, Wadeson A, Ward S, Burges D, Cooke GD (1998) Bacillus subtilis ORF yybQ encodes a manganese-dependent inorganic pyrophosphatase with distinctive properties: the first of a new class of soluble pyrophosphatase? Microbiology 144:2563–2571

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Plant Biol 6:441–445

    CAS  Google Scholar 

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Acknowledgements

We are grateful to Prof. Youzhi Ma and Prof. Ming Chen for providing the S. cerevisiae NMY51 and technical support. This work was supported by the National Key Project for Cultivation of New Varieties of Genetically Modifying Organisms (2016ZX08002-005) and the National Key Project for 973 Fundamental Research (2015CB150800). Special thanks to Prof. Wan Jianmin’s team for rice transformation.

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Correspondence to Xianguo Cheng.

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Communicated by Leena Tripathi.

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He, R., Yu, G., Han, X. et al. ThPP1 gene, encodes an inorganic pyrophosphatase in Thellungiella halophila, enhanced the tolerance of the transgenic rice to alkali stress. Plant Cell Rep 36, 1929–1942 (2017). https://doi.org/10.1007/s00299-017-2208-y

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