Russian Journal of Plant Physiology

, Volume 62, Issue 3, pp 360–366 | Cite as

Transgenic tomato overexpressing ath-miR399d improves growth under abiotic stress conditions

  • N. Gao
  • X. M. Qiang
  • B. N. Zhai
  • J. Min
  • W. M. ShiEmail author
Research Papers


Phosphorus (P) is an essential element required for plant growth and development. Abiotic stresses, such as cold and P deficiency cause adverse effects on growth of plants, inhibit accumulation or translocation of mineral nutrients such as P, and often constrain the productivity and quality of crops. miR399 as a long-distance signal controls systemic phosphate homeostasis by modulating phosphate uptake and transport. However, overexpression of miR399 causes P toxicity and results in retarded growth. Thus, we constructed a transgenic tomato (Solanum lycopersicum L., C1), which contains foreign gene ath-miR399d under the control of rd29A promoter. In the transgenic C1 expression of the miR399d gene showed a stress-inducible pattern. Results showed that miR399d was moderately up-regulated in response to salinity and cold stresses. In soil, dry weight was enhanced in transgenic tomato under low temperature and P deficiency conditions. The transgenic tomato has potential to improve growth when it is exposed to other abiotic stresses such as salinity and drought.


Solanum lycopersicum transgenic tomato microRNA399 abiotic stress 



plants grown in chamber at 24°C for day-time and at 16°C for night-time


plants grown in chamber at constant 24°C


150 mg P2O5/kg soil as KH2PO4 added into soil


300 mg P2O5/kg soil as KH2PO4 added into soil


inorganic phosphorus


real-time quantitative reverse transcription PCR


wild type


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Martinez, V. and Lauchli, A., Salt-induced inhibition of phosphate-uptake in plants of cotton (Gossypium hirsutum L.), New Phytol., 1994, vol. 126, pp. 609–614.CrossRefGoogle Scholar
  2. 2.
    Starck, Z., Niemyska, B., Bogdan, J., and Tawalbeh, R.N.A., Response of tomato plants to chilling stress in association with nutrient or phosphorus starvation, Plant Soil, 2000, vol. 226, pp. 99–106.CrossRefGoogle Scholar
  3. 3.
    Min, J., Zhao, X., Shi, W.M., Xing, G.X., and Zhu, Z.L., Nitrogen balance and loss in a greenhouse vegetable system in Southeastern China, Pedosphere, 2011, vol. 21, pp. 464–472.CrossRefGoogle Scholar
  4. 4.
    Tang, C.X., Jin, J., Wang, G.H., Liu, X.B., Pan, X.W., and Herbert, S.J., Interaction between phosphorus nutrition and drought on grain yield, and assimilation of phosphorus and nitrogen in two soybean cultivars differing in protein concentration in grains, J. Plant Nutr., 2006, vol. 29, pp. 1433–1449.CrossRefGoogle Scholar
  5. 5.
    Waraich, E.A., Ahmad, R., Saifullah, Ashraf, M.Y., and Ehsanullah, Role of mineral nutrition in alleviation of drought stress in plants, Aust. J. Crop Sci., 2011, vol. 5, pp. 764–777.Google Scholar
  6. 6.
    Zia, M.S., Salim, M., Aslam, M., and Gill, M.A., Rahmatullah, Effect of low-temperature of irrigation water on rice growth and nutrient-uptake, J. Agron. Crop Sci., 1994, vol. 173, pp. 22–31.Google Scholar
  7. 7.
    Fujii, H., Chiou, T.J., Lin, S.I., Aung, K., and Zhu, J.K., A miRNA involved in phosphate-starvation response in Arabidopsis, Curr. Biol., 2005, vol. 15, pp. 2038–2043.CrossRefPubMedGoogle Scholar
  8. 8.
    Pant, B.D., Buhtz, A., Kehr, J., and Scheible, W., MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis, Plant J., 2008, vol. 53, pp. 731–738.CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Luan, F.L., Han, Y.S., Zhu, H.L., Shao, Y., Chen, A.J., Tian, H.Q., Luo, Y.B., and Zhu, B.Z., Computational predicting novel microRNAs in tomato and validating with RT-PCR, Russ. J. Plant Physiol., 2010, vol. 57, pp. 469–479.CrossRefGoogle Scholar
  10. 10.
    Pashkovsky, P.P. and Ryazansky, S.S., Biogenesis, evolution, and functions of plant microRNAs, Biochemistry (Moscow), 2013, vol. 78, pp. 627–637.Google Scholar
  11. 11.
    Gao, N., Su, Y.H., Min, J., Shen, W.S., and Shi, W.M., Transgenic tomato overexpressing ath-miR399d has enhanced phosphorus accumulation through increased acid phosphatase and proton secretion as well as phosphate transporters, Plant Soil, 2010, vol. 334, pp. 123–136.CrossRefGoogle Scholar
  12. 12.
    Yamaguchi-Shinozaki, K. and Shinozaki, K., Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants, Mol. Gen. Genet., 1993, vol. 236, pp. 331–340.CrossRefPubMedGoogle Scholar
  13. 13.
    Lee, H., Xiong, L., Ishitani, M., Stevenson, B., and Zhu, J.K., Cold-regulated gene expression and freezing tolerance in an Arabidopsis thaliana mutant, Plant J., 1999, vol. 17, pp. 301–308.CrossRefPubMedGoogle Scholar
  14. 14.
    Islam, M.S., Hur, J.H., and Wan, M.H., The influence of abiotic stresses on expression of zinc finger protein gene in rice, Russ. J. Plant Physiol., 2009, vol. 56, pp. 695–701.CrossRefGoogle Scholar
  15. 15.
    Gao, N., Shen, W.S., Cao, Y., Su, Y.H., and Shi, W.M., Influence of bacterial density during preculture on Agrobacterium-mediated transformation of tomato, Plant Cell Tissue Organ Cult., 2009, vol. 98, pp. 321–330.CrossRefGoogle Scholar
  16. 16.
    Xu, W.F. and Shi, W.M., Expression profiling of the 14-3-3 gene family in response to salt stress and potassium and iron deficiencies in young tomato (Solanum lycopersicum) roots: analysis by real-time RT-PCR, Ann. Bot., 2006, vol. 98, pp. 965–974.CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Yao, J., Shi, W.M., and Xu, W.F., Effects of salt stress on expression of nitrate transporter and assimilationrelated genes in tomato roots, Russ. J. Plant Physiol., 2008, vol. 55, pp. 232–240.CrossRefGoogle Scholar
  18. 18.
    Huan, H.F., Zhou, J.M., Duan, Z.Q., Wang, H.Y., and Gao, Y.F., Contributions of greenhouse soil nutrients accumulation to the formation of the secondary salinization: a case study of Yixing ñity, China, Agrochimica, 2007, vol. 51, nos. 4–5, pp. 207–221.Google Scholar
  19. 19.
    Olsen, S.R., Cole, C.V., Watanabe, F.S., and Dean, L.A., Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate, United States Department of Agriculture (USDA), circular no. 939, Washington: USDF, 1954.Google Scholar
  20. 20.
    Kalifa, Y., Gilad, A., Konrad, Z., Zaccai, M., Scolnik, P.A., and Bar-Zvi, D., The water-and saltstress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein, Biochem. J., 2004, vol. 381, pp. 373–378.CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Fujita, K., Okada, M., Lei, K., Ito, J., Ohkura, K., Adu-Gyamfi, J.J., and Mohapatra, P.K., Effect of P-deficiency on photoassimilate partitioning and rhythmic changes in fruit and stem diameter of tomato (Lycopersicon esculentum) during fruit growth, J. Exp. Bot., 2003, vol. 54, pp. 2519–2528.CrossRefPubMedGoogle Scholar
  22. 22.
    Xu, G.H., Chague, V., Melamed-Bessudo, C., Kapulnik, Y., Jain, A., Raghothama, K.G., Levy, A.A., and Silber, A., Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression, J. Exp. Bot., 2007, vol. 58, pp. 2491–2501.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • N. Gao
    • 1
  • X. M. Qiang
    • 1
    • 2
  • B. N. Zhai
    • 2
  • J. Min
    • 1
  • W. M. Shi
    • 1
    Email author
  1. 1.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  2. 2.College of Resource and EnvironmentNorthwest Agriculture and Forestry UniversityBeijingChina

Personalised recommendations