Plant Cell Reports

, Volume 36, Issue 12, pp 1929–1942 | Cite as

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

  • Rui He
  • Guohong Yu
  • Xiaori Han
  • Jiao Han
  • Wei Li
  • Bing Wang
  • Shengcai Huang
  • Xianguo Cheng
Original Article

Abstract

Key message

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.

Keywords

Alkali stress Gene expression Inorganic pyrophosphatase ThPP1 gene Rice Transcriptome sequencing 

Notes

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.

Compliance with ethical standards

Conflict of interest

All authors have agreed on the content of the manuscript and declare no conflicts of interests.

Supplementary material

299_2017_2208_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 17 kb)

References

  1. 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 313:797–811CrossRefPubMedGoogle Scholar
  2. 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):1–5Google Scholar
  3. Baltscheffsky M, Schultz A, Baltscheffsky H (1999) H+-PPases: a tightly membrane-bound family. FEBS Lett 457:527–533CrossRefPubMedGoogle Scholar
  4. Carman GM, Han GS (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem Sci 31:694–699CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 160:1293–1302CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cui Y, Wang Q (2006) Physiological responses of maize to elemental sulphur and cadmium stress. Plant Soil Environ 52:523–529Google Scholar
  7. 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 52:493–500CrossRefGoogle Scholar
  8. 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 205:428–437CrossRefPubMedGoogle Scholar
  9. 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 154:55–66CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 44:826–839CrossRefPubMedGoogle Scholar
  11. 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 253:229–242CrossRefPubMedGoogle Scholar
  12. 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 69:323–333CrossRefGoogle Scholar
  13. Harold FM (1966) Inorganic polyphosphates in biology: structure, metabolism, and function. Bacteriol Rev 30:772–794PubMedPubMedCentralGoogle Scholar
  14. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:258–261CrossRefGoogle Scholar
  15. Heikinheimo P, Lehtonen J, Baykov A, Lahti R, Cooperman BS, Goldman A (1996) The structural basis for pyrophosphatase catalysis. Structure 4:1491–1508CrossRefPubMedGoogle Scholar
  16. 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 187:39–48CrossRefPubMedGoogle Scholar
  17. 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 122:1129–1136CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 53:2127–2141CrossRefPubMedGoogle Scholar
  19. 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 346:105–112CrossRefPubMedGoogle Scholar
  20. Kajander T, Kellosalo J, Goldman A (2013) Inorganic pyrophosphatases: one substrate, three mechanisms. FEBS Lett 587:1863–1869CrossRefPubMedGoogle Scholar
  21. 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 581:5445–5453CrossRefPubMedGoogle Scholar
  22. 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 300:68–74CrossRefPubMedGoogle Scholar
  23. 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 36:134–141CrossRefPubMedGoogle Scholar
  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  25. 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 186:5418–5426CrossRefPubMedPubMedCentralGoogle Scholar
  26. Maeshima M (2000) Vacuolar H+-pyrophosphatase. Biochem Biophys Acta 1465:37–51CrossRefPubMedGoogle Scholar
  27. 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 50:216–229CrossRefPubMedGoogle Scholar
  28. 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 9:289–297CrossRefPubMedGoogle Scholar
  29. 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 38:355–360CrossRefGoogle Scholar
  30. 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 42:725–730CrossRefPubMedGoogle Scholar
  31. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Plant Biol 59:651–681CrossRefGoogle Scholar
  32. 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 46:1228–1239CrossRefPubMedGoogle Scholar
  33. Öztürk ZN, Greiner S, Rausch T (2014) Subcellular localization and developmental regulation of cytosolic, soluble pyrophosphatase isoforms in Arabidopsis thaliana. Turk J Bot 38:1036–1049CrossRefGoogle Scholar
  34. Öztürk ZN, Greiner S, Rausch T (2015) Differential expression of soluble pyrophosphatase isoforms in Arabidopsis upon external stimuli. Turk J Bot 39:571–579CrossRefGoogle Scholar
  35. 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 428:201–212CrossRefPubMedGoogle Scholar
  36. 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 39:449–461CrossRefPubMedGoogle Scholar
  37. Schulze S, Mant A, Kossmann J, Lloyd J (2004) Identification of an Arabidopsis inorganic pyrophosphatase capable of being imported into the chloroplast. FEBS Lett 565:101–105CrossRefPubMedGoogle Scholar
  38. 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 35:144–149Google Scholar
  39. 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 116:1539–1549CrossRefPubMedPubMedCentralGoogle Scholar
  40. Vernon DM, Bohnert HJ (1992) A novel methyl transferase induced by osmotic stress in the facultative Mesembryanthemum crystallinum. EMBO J 11:2077–2085PubMedPubMedCentralGoogle Scholar
  41. Vianello A, Macrí F (1999) Proton pumping pyrophosphatase from higher plant mitochondria. Physiol Plant 105:763–768CrossRefGoogle Scholar
  42. 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 48:342–353CrossRefPubMedGoogle Scholar
  43. 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 26:136–138CrossRefPubMedGoogle Scholar
  44. 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 168:51149–51159Google Scholar
  45. 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 52:157–160CrossRefGoogle Scholar
  46. 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 127:695–708CrossRefPubMedGoogle Scholar
  47. 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 34:293–297CrossRefGoogle Scholar
  48. 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 144:2563–2571CrossRefPubMedGoogle Scholar
  49. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Plant Biol 6:441–445Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Rui He
    • 1
    • 2
  • Guohong Yu
    • 2
  • Xiaori Han
    • 1
  • Jiao Han
    • 2
    • 3
  • Wei Li
    • 2
  • Bing Wang
    • 2
  • Shengcai Huang
    • 2
  • Xianguo Cheng
    • 2
  1. 1.College of Land and EnvironmentShenyang Agricultural UniversityShenyangPeople’s Republic of China
  2. 2.Key Lab of Plant Nutrition and Fertilizers, Ministry of Agriculture, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingPeople’s Republic of China
  3. 3.College of Life ScienceShanxi Normal UniversityLinfenPeople’s Republic of China

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