Biologia Plantarum 63: 122-133, 2019 | DOI: 10.32615/bp.2019.015

Overexpression of a gene AhFBA from Arachis hypogaea confers salinity stress tolerance in Escherichia coli and tobacco

Z.K. Du1,2, Y.F. Hu3, J.M. Li1,2,*
1 Zhejiang Provincial Key Laboratory of Plant Evolution and Conservation, Taizhou University, Taizhou, Zhejiang 318000, P.R. China
2 Institute of Ecology, Taizhou University, Taizhou, Zhejiang 318000, P.R. China
3 College of Agronomy, Sichuan Agricultural University, Chengdu, Sichuan 611130, P.R. China

Fructose-1,6-bisphosphate aldolase (FBA), an essential enzyme involved in the glycolytic pathway, gluconeogenesis, and the Calvin cycle, plays significant roles in the regulation of plant growth, development, and stress responses. In this study, a novel gene, AhFBA (GenBank accession number KF470788), containing a 1077-bp open reading frame and encoding a protein of 358 amino acids, was isolated from Arachis hypogaea L. Bioinformatic analysis revealed that AhFBA belonged to class-I aldolases and preferentially localized in the cytoplasm. Real-time quantitative PCR analysis indicated that AhFBA had a higher expression in young fruits than in leaves and stems, and NaCl could trigger the highest expression of AhFBA in roots and leaves after 3-h and 6-h treatments. The salinity tolerance and survival of Escherichia coli transformed with AhFBA were notably enhanced compared with the control. Transgenic tobacco (Nicotiana tabacum L.) overexpressing the AhFBA gene exhibited a lower hydrogen peroxide content, electrolyte leakage, and malondialdehyde content and a higher photosynthetic efficiency, net photosynthetic rate, relative water content, and sucrose and proline content compared with control plants. Taken together, the results demonstrate that AhFBA functioned as a positive factor enhancing the tolerance of E. coli and N. tabacum to salinity stress, possibly by maintaining the osmotic balance and scavenging hydrogen peroxide.

Keywords: fructose-1,6-bisphosphate aldolase, H2O2, net photosynthetic rate, Nicotiana tabaccum, peanut, proline, RWC

Accepted: November 15, 2018; Prepublished online: November 15, 2018; Published online: January 19, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Du, Z.K., Hu, Y.F., & Li, J.M. (2019). Overexpression of a gene AhFBA from Arachis hypogaea confers salinity stress tolerance in Escherichia coli and tobacco. Biologia plantarum, 63, 122-133. doi: 10.32615/bp.2019.015.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    Supplementary files

    Download fileDU5687.pdf

    File size: 3.34 MB

    References

    1. Abd Elgawad, H., Zinta, G., Hegab, M.M., Pandey, R., Asard, H., Abuelsoud, W.: High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. - Front. Plant Sci. 7: 1-11, 2016. Go to original source...
    2. Cai, B., Li, Q., Xu, Y., Yang, L., Bi, H., Ai, X.: Genome-wide analysis of the fructose 1, 6-bisphosphate aldolase (FBA) gene family and functional characterization of FBA7 in tomato. - Plant Physiol. Biochem. 108: 251-265, 2016. Go to original source...
    3. Chen, H., Jiang, J.-G.: Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. - Environ. Rev. 18: 309-319, 2010. Go to original source...
    4. Chen, Y., Cui, J., Li, G., Yuan, M., Zhang, Z., Yuan, S., Zhang, H.: Effect of salicylic acid on the antioxidant system and photosystem II in wheat seedlings. - Biol. Plant. 60: 139-147, 2016. Go to original source...
    5. Cheng, L., Wang, Y., He, Q., Li, H., Zhang, X., Zhang, F.: Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration. - BMC Plant Biol. 16: 188-210, 2016. Go to original source...
    6. Cieśla, M., Mierzejewska, J., Adamczyk, M., Farrants, A.-K.Ö., Boguta, M.: Fructose bisphosphate aldolase is involved in the control of RNA polymerase III-directed transcription. - BBA 1843: 1103-1110, 2014.
    7. Dennis, E., Gerlach, W., Walker, J., Lavin, M., Peacock, W.: Anaerobically regulated aldolase gene of maize:a chimaeric origin? - J. mol. Biol. 202: 759-767, 1988. Go to original source...
    8. Fan, W., Zhang, Z., Zhang, Y.: Cloning and molecular characterization of fructose-1,6-bisphosphate aldolase gene regulated by high-salinity and drought in Sesuvium portulacastrum. - Plant Cell Rep. 28: 975-984, 2009. Go to original source...
    9. Flechner, A., Gross, W., Martin, W.F., Schnarrenberger, C.: Chloroplast class I and class II aldolases are bifunctional for fructose-1, 6-biphosphate and sedoheptulose-1,7-biphosphate cleavage in the Calvin cycle. - FEBS Lett. 447: 200-202, 1999. Go to original source...
    10. Gross, W., Lenze, D., Nowitzki, U., Weiske, J., Schnarrenberger, C.: Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. - Gene 230: 7-14, 1999. Go to original source...
    11. Haake, V., Zrenner, R., Sonnewald, U., Stitt, M.: A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. - Plant J. 14: 147-157, 1998. Go to original source...
    12. Hanin, M., Ebel, C., Ngom, M., Laplaze, L., Masmoudi, K.: New insights on plant salt tolerance mechanisms and their potential use for breeding. - Front. Plant Sci. 7: 1-17, 2016. Go to original source...
    13. Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J., Ahmad, A.: Role of proline under changing environments: a review. - Plant Signal. Behav. 7: 1456-1466, 2012. Go to original source...
    14. Kagaya, Y., Nakamura, H., Ejiri, S.-i., Tsutsumi, K.-i., Hidaka, S.: The promoter from the rice nuclear gene encoding chloroplast aldolase confers mesophyll-specific and light-regulated expression in transgenic tobacco. - Mol. gen. Genet. 248: 668-674, 1995. Go to original source...
    15. Kavas, M., Akça, O.E., Akçay, U.C., Peksel, B., Eroğlu, S., Öktem, H.A., Yücel, M.: Antioxidant responses of peanut (Arachis hypogaea L.) seedlings to prolonged salt-induced stress. - Arch. Biol. Sci. 67: 1303-1312, 2015. Go to original source...
    16. Konishi, H., Yamane, H., Maeshima, M., Komatsu, S.: Characterization of fructose-bisphosphate aldolase regulated by gibberellin in roots of rice seedling. - Plant mol. Biol. 56: 839-848, 2004. Go to original source...
    17. Lao, X., Azuma, J.-i., Sakamoto, M.: Two cytosolic aldolases show different expression patterns during shoot elongation in moso bamboo, Phyllostachys pubescens Mazel. - Physiol. Plant. 149: 422-431, 2013. Go to original source...
    18. Lebherz, H., Leadbetter, M., Bradshaw, R.: Isolation and characterization of the cytosolic and chloroplast forms of spinach leaf fructose diphosphate aldolase. - J. biol. Chem. 259: 1011-1017, 1984.
    19. Lee, B.-R., Muneer, S., Park, S.-H., Zhang, Q., Kim, T.-H.: Ammonium-induced proline and sucrose accumulation, and their significance in antioxidative activity and osmotic adjustment. - Acta Physiol. Plant. 35: 2655-2664, 2013. Go to original source...
    20. Lv, G.Y., Guo, X.G., Xie, L.P., Xie, C.G., Zhang, X.H., Yang, Y., Xiao, L., Tang, Y.Y., Pan, X.L., Guo, A.G.: Molecular characterization, gene evolution, and expression analysis of the fructose-1,6-bisphosphate aldolase (FBA) gene family in wheat (Triticum aestivum L.). - Front. Plant Sci. 8: 1-18, 2017. Go to original source...
    21. Mohapatra, S., Mittra, B.: Protein glutathionylation protects wheat (Triticum aestivum var. Sonalika) against Fusarium induced oxidative stress. - Plant Physiol. Biochem. 109: 319-325, 2016. Go to original source...
    22. Okuma, E., Murakami, Y., Shimoishi, Y., Tada, M., Murata, Y.: Effects of exogenous application of proline and betaine on the growth of tobacco cultured cells under saline conditions. - Soil Sci. Plant Nutr. 50: 1301-1305, 2004. Go to original source...
    23. Páez-Valencia, J., Valencia-Mayoral, P., Sánchez-Gómez, C., Contreras-Ramos, A., Hernández-Lucas, I., Martínez-Barajas, E., Gamboa-deBuen, A.: Identification of fructose-1,6-bisphosphate aldolase cytosolic class I as an NMH7 MADS domain associated protein. - Biochem. biophys. Res. Commun. 376: 700-705, 2008. Go to original source...
    24. Park, J., Tran, L. H., Jung, S.: A protoporphyrinogen oxidase gene expression influences responses of transgenic rice to oxyfluorfen. - Biol. Plant. 61: 659-666, 2017. Go to original source...
    25. Patel, M. K., Joshi, M., Mishra, A., Jha, B.: Ectopic expression of SbNHX1 gene in transgenic castor (Ricinus communis L.) enhances salt stress by modulating physiological process. - Plant Cell Tissue Organ Cult. 122: 477-490, 2015. Go to original source...
    26. Purev, M., Kim, M.K., Samdan, N., Yang, D.-C.: Isolation of a novel fructose-1,6-bisphosphate aldolase gene from Codonopsis lanceolata and analysis of the response of this gene to abiotic stresses. - Mol. Biol. 42: 179-186, 2008. Go to original source...
    27. Schmittgen, T.D., Livak, K.J.: Analyzing real-time PCR data by the comparative CT method. - Nat. Protoc. 3: 1101-1108, 2008. Go to original source...
    28. Shams, F., Oldfield, N.J., Wooldridge, K.G., Turner, D.P.: Fructose-1,6-bisphosphate aldolase (FBA)  a conserved glycolytic enzyme with virulence functions in bacteria: 'ill met by moonlight'. - Biochem. Soc. Trans. 42: 1792-1795, 2014. Go to original source...
    29. Shi, H., Wang, Y., Cheng, Z., Ye, T., Chan, Z.: Analysis of natural variation in bermudagrass (Cynodon dactylon) reveals physiological responses underlying drought tolerance. - PLoS ONE 7: e53422, 2012. Go to original source...
    30. Shrivastava, P., Kumar, R.: Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. - Saudi J. biol. Sci. 22: 123-131, 2015. Go to original source...
    31. Singh, P.K., Shrivastava, A.K., Chatterjee, A., Pandey, S., Rai, S., Singh, S., Rai, L.: Cadmium toxicity in diazotrophic Anabaena spp. adjudged by hasty up-accumulation of transporter and signaling and severe down-accumulation of nitrogen metabolism proteins. - J. Proteomics 127: 134-146, 2015. Go to original source...
    32. Strand, Å., Zrenner, R., Trevanion, S., Stitt, M., Gustafsson, P., Gardeström, P.: Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. - Plant J. 23: 759-770, 2000. Go to original source...
    33. Sui, J., Jiang, D., Zhang, D., Song, X., Wang, J., Zhao, M., Qiao, L.: The salinity responsive mechanism of a hydroxyproline-tolerant mutant of peanut based on digital gene expression profiling analysis. - PLoS ONE 11: e0162556, 2016. Go to original source...
    34. Toscano, S., Farieri, E., Ferrante, A., Romano, D.: Physiological and biochemical responses in two ornamental shrubs to drought stress. - Front. Plant Sci. 7: ??-??, 2016.
    35. Uematsu, K., Suzuki, N., Iwamae, T., Inui, M., Yukawa, H.: Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. - J. exp. Bot. 63: 3001-3009, 2012. Go to original source...
    36. Wu, G., Wang, G., Ji, J., Gao, H., Guan, W., Wu, J., Guan, C., Wang, Y.: Cloning of a cytosolic ascorbate peroxidase gene from Lycium chinense Mill. and enhanced salt tolerance by overexpressing in tobacco. - Gene 543: 85-92, 2014. Go to original source...
    37. Zeng, Y., Tan, X., Zhang, L., Jiang, N., Cao, H.: Identification and expression of fructose-1,6-bisphosphate aldolase genes and their relations to oil content in developing seeds of tea oil tree (Camellia oleifera). - PLoS ONE 9: e107422, 2014. Go to original source...
    38. Zeng, Y., Tan, X., Zhang, L., Long, H., Wang, B., Li, Z., Yuan, Z.: A fructose-1, 6-biphosphate aldolase gene from Camellia oleifera: molecular characterization and impact on salt stress tolerance. - Mol. Breed. 35: 17, 2015. Go to original source...
    39. Zhang, F., Li, S., Yang, S., Wang, L., Guo, W.: Overexpression of a cotton annexin gene, GhAnn1, enhances drought and salt stress tolerance in transgenic cotton. - Plant mol. Biol. 87: 47-67, 2015. Go to original source...
    40. Zhang, F., Zhang, P., Zhang, Y., Wang, S., Qu, L., Liu, X., Luo, J.: Identification of a peroxisomal-targeted aldolase involved in chlorophyll biosynthesis and sugar metabolism in rice. - Plant Sci. 250: 205-215, 2016. Go to original source...

    Return to the content