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Ectopic expression of sorbitol-6-phosphate 2-dehydrogenase gene from Haloarcula marismortui enhances salt tolerance in transgenic Arabidopsis thaliana

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Abstract

d-Sorbitol-6-phosphate 2-dehydrogenase (S6PDH, E.C. 1.1.1.140) catalyzes the NADH-dependent conversion of d-fructose 6-phosphate (F6P) to d-sorbitol 6-phosphate (S6P). In this work, recombination and characterization of Haloarcula marismortui d-sorbitol-6-phosphate 2-dehydrogenase are reported. Haloarcula marismortui d-sorbitol-6-phosphate 2-dehydrogenase was expressed in P. pastoris and Arabidopsis thaliana. Enzyme assay indicated that HmS6PDH catalyzes the reduction of d-fructose 6-phosphate to d-sorbitol 6-phosphate and HmS6PDH activity was enhanced by NaCl. Furthermore, transgenic A. thaliana ectopic expressing HmS6PDH accumulate more sorbitol under salt stress. These results suggest that the ectopic expression of HmS6PDH in plants can facilitate future studies regarding the engineering and breeding of salt-tolerant crops.

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Abbreviations

S6PDH:

Sorbitol-6-phosphate 2-dehydrogenase

HmS6PDH:

Haloarcula marismortui sorbitol-6-phosphate 2-dehydrogenase

SDH:

Sorbitol dehydrogenase

F6P:

d-Fructose 6-phosphate

S6P:

d-Sorbitol 6-phosphate

MDA:

Malondialdehyde

References

  • Bianco RL, Rieger M, Sung SS (2000) Effect of drought on sorbitol and sucrose metabolism in sinks and sources of peach. Physiol Plant 108(1):71–78

    Article  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099–1111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen GC, Ren L, Zhang J, Reed BM, Zhang D, Shen XH (2015) Cryopreservation affects ROS-induced oxidative stress and antioxidant response in Arabidopsis seedlings. Cryobiology 70(1):38–47

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Tian Q, Zhang WH (2016) Glutamate receptors are involved in mitigating effects of amino acids on seed germination of Arabidopsis thaliana under salt stress. Environ Exp Bot 130:68–78

    Article  CAS  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90(5):856–867

    Article  PubMed  CAS  Google Scholar 

  • Christian JH, Waltho JA (1962) Solute concentrations within cells of halophilic and non-halophilic bacteria. Biochem Biophys Acta 65:506–508

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Tao R, Miura K, Dandekar AM, Sugiura A (2001) Transformation of Japanese persimmon (Diospyros kaki Thunb.) with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Sci 160(5):837–845

    Article  PubMed  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Kanamaru N, Ito Y, Komori S, Saito M, Kato H, Takahashi S, Omura M, Soejima J, Shiratake K, Yamada K, Yamaki S (2004) Transgenic apple transformed by sorbitol-6-phosphate dehydrogenase cDNA Switch between sorbitol and sucrose supply due to its gene expression. Plant Sci 167:55–61

    Article  CAS  Google Scholar 

  • Kanayama Y, Mori H, Imaseki H, Yamaki S (1992) Nucleotide sequence of a cDNA encoding NADP-sorbitol-6-phosphate dehydrogenase from apple. Plant Physiol 100(3):1607–1608

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim HY, Ahn JC, Choi JH, Hwang B, Choi DW (2007) Expression and cloning of the full-length cDNA for sorbitol-6-phosphate dehydrogenase and NAD-dependent sorbitol dehydrogenase from pear (Pyrus pyrifolia N.). Sci Hortic 112:406–412

    Article  CAS  Google Scholar 

  • Kobashi K, Gemma H, Iwahori S (2000) Abscisic acid content and sugar metabolism of peaches grown under water stress. J Am Soc Hortic Sci 125(4):425–428

    CAS  Google Scholar 

  • Kurth E, Cramer GR, Läuchli A, Epstein E (1986) Effects of NaCl and CaCl2 on cell enlargement and cell production in cotton roots. Plant Physiol 82(4):1102–1106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lengeler J, Lin EC (1972) Reversal of the mannitol-sorbitol diauxie in Escherichia coli. J Bacteriol 112:840–848

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liss M, Horwitz SB, Kaplan NO (1962) d-Mannitol-l-phosphate dehydrogenase and d-sorbitol-6-phosphate dehydrogenase in Aerobacter aerogenes. J Biol Chem 237:1342–1350

    PubMed  CAS  Google Scholar 

  • Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168(1):343–356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164

    Article  PubMed  CAS  Google Scholar 

  • Mundree SG, Farrant JM (2000) Some physiological and molecular insights into the mechanisms of desiccation tolerance in the resurrection plant Xerophyta viscosa Baker. Plant Toler Abiotic Stresses Agric Role Genet Eng 83:201–222

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nosarzewski M, Downie AB, Wu B, Archbold DD (2012) The role of sorbitol dehydrogenase in Arabidopsis thaliana. Funct Plant Biol 39:462–470

    Article  CAS  PubMed  Google Scholar 

  • Oura Y, Yamada K, Shiratake K, Yamaki S (2000) Purification and characterization of a NAD+-dependent sorbitol dehydrogenase from Japanese pear fruit. Phytochemistry 54(6):567–572

    Article  PubMed  CAS  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22(6):4056–4075

    Article  CAS  Google Scholar 

  • Pharr DM, Stoop JMH, Williamson JD, Feusi MES, Massel MO, Conkling MA (1995) The dual role of mannitol as osmoprotectant and photoassimilate in celery. Am Soc Hortic Sci 30(6):1151–1192

    Google Scholar 

  • Qiu ZB, Wang YF, Zhu AJ, Peng FL, Wang LS (2014) Exogenous sucrose can enhance tolerance of Arabidopsis thaliana seedlings to salt stress. Biol Plant 58(4):611–617

    Article  CAS  Google Scholar 

  • Saleki R, Young P, Lefebvre DD (1993) Mutants of Arabidopsis thaliana capable of germination under saline conditions. Plant Physiol 101:839–845

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sheveleva E, Marquez S, Chmara W, Wegeer A, Jensen RG, Bohnert HJ (1998) Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. Plant Physiol 117:831–839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shimada TL, Shimada T, Takahashi H, Fukao Y, Hara-Nishimura I (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. Plant J 55(5):798–809

    Article  PubMed  CAS  Google Scholar 

  • Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio/Technol 14(3):407–426

    Article  CAS  Google Scholar 

  • Umezawa T, Mizuno K, Fujimura T (2002) Discrimination of genes expressed in response to the ionic or osmotic effect of salt stress in soybean with cDNA-AFLP. Plant Cell Environ 25(12):1617–1625

    Article  CAS  Google Scholar 

  • West G, Inze D, Beemster GTS (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu S, Letchworth GJ (2004) High efficiency transformation by electroporation of Pichia pastoris pretreated with lithium acetate and dithiothreitol. Biotechniques 36:152–154

    Article  PubMed  CAS  Google Scholar 

  • Xiong AS, Yao QH, Peng RH, Li X, Fan HQ, Cheng ZM, Li Y (2004) A simple, rapid, high-fidelity and cost-effective PCR-based two-step DNA synthesis method for long gene sequence. Nucleic Acids Res 32:e98

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiong AS, Yao QH, Peng RH, Duan H, Li X, Fan HQ, Cheng ZM, Li Y (2006) PCR-based accurate synthesis of long DNA sequences. Nat Protoc 1:791–797

    Article  PubMed  CAS  Google Scholar 

  • Xu ZS, Xue W, Xiong AS, Lin YQ, Xu J, Zhu B, Zhao W, Peng RH, Yao QH (2013) Characterization of a bifunctional O- and N-Glucosyltransferase from Vitis vinifera in glucosylating phenolic compounds and 3,4-dichloroaniline in Pichia pastoris and Arabidopsis thaliana. PLoS One 8(11):e80449

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaki S, Ishikawa K (1986) Roles of four sorbitol related enzymes and invertase in the seasonal alteration of sugar metabolism in apple tissue. J Am Soc Hortic Sci 111:134–137

    CAS  Google Scholar 

  • Zhou R, Cheng LL, Wayne R (2003) Purification and characterization of sorbitol-6-phosphate phosphatase from apple leaves. Plant Sci 165:227–232

    Article  CAS  Google Scholar 

  • Zhou S, Tang QJ, Zhang Z, Li CH, Cao H, Yang Y, Zhang JS (2015) Nutritional composition of three domesticated culinary-medicinal mushrooms: Oudemansiella sudmusida, Lentinus squarrosulus, and Tremella aurantialba. Int J Med Mushrooms 17(1):43–49

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research was sponsored by Shanghai Sailing Program(15YF1410400), the Young Growing Project Fund of the Shanghai Municipal Committee of Agriculture (2015, 1-27), the run-up project of the Shanghai Academy of Agricultural Sciences (ZP18), the Key Project Fund of the Shanghai Municipal Committee of Agriculture (zhongzi2014-2, zhongzi2014 7-1-3, zhongzi2016 1-2), the Agriculture Science Technology Achievement Transformation Fund (143919N0300), the National Natural Science Foundation (31200212, 31200075, 31200076, and 31672439), and the Basic Research in the Field of Science and Technology Project of Science and Technology Commission of the Shanghai Municipality (14JC1403602).

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    Authors and Affiliations

    1. Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences, 2901 Beidi Road, Shanghai, 201106, China

      Jian-jie Gao, Yu-ru Sun, Bo Zhu, Ri-He Peng, Bo Wang, Li-Juan Wang, Zhen-Jun Li & Quan-Hong Yao

    2. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

      Yu-ru Sun

    3. College of Food Science and Technology, Shanghai Ocean University, Shanghai, 201306, China

      Lei Chen

    4. Shanghai Key Laboratory of Agricultural Genetics and Breeding, Shanghai Academy of Agricultural Sciences, Shanghai, 201106, China

      Jian-jie Gao, Bo Zhu, Ri-He Peng, Bo Wang, Li-Juan Wang, Zhen-Jun Li & Quan-Hong Yao

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    1. Jian-jie Gao
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    Communicated by Q. Wang.

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    Nucleotides acid sequence alignment of HmSorD and HmSorDI. (TIFF 1696 KB)

    11738_2018_2668_MOESM2_ESM.jpg

    Analysis of transgenic HmS6PDH lines. (A) Schematic of the vector used in this study. The vector contains a double CaMV 35S (DCaMV35S) promoter and the tobacco mosaic virus (TMV) sequence fused to the HmSorDI gene. For steady transcription of the HmSorDI gene, two scaffold attachment regions (SAR) were fused upstream of the DCaMV35S promoter and downstream of the Nos-terminator (Nos-T). (B) Analysis by PCR of HmSorDI expression in Arabidopsis transgenic lines. Wild-type (lane 5) and transgenic lines (line 3, line 4, and lines 6–8) of A. thaliana were used as PCR templates. Line 3 represents HT-1, and lines 6 and 7 represent HT-8 and HT-9, respectively. Line 2 represents a water-only control. Specific primer pairs for PCR amplification of HmSorDI were used. (JPEG 60 KB)

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    Gao, Jj., Sun, Yr., Zhu, B. et al. Ectopic expression of sorbitol-6-phosphate 2-dehydrogenase gene from Haloarcula marismortui enhances salt tolerance in transgenic Arabidopsis thaliana. Acta Physiol Plant 40, 108 (2018). https://doi.org/10.1007/s11738-018-2668-x

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