Involvement of Source-Sink Relationship and Hormonal Control in the Response of Medicago Ciliaris — Sinorhizobium Medicae Symbiosis to Salt Stress

Abstract

In order to explore the relationship between leaf hormonal status and source-sink relations in the response of symbiotic nitrogen fixation (SNF) to salt stress, three major phytohormones (cytokinins, abscisic acid and the ethylene precursor 1-aminocyclopropane-l-carboxylic acid), sucrose phosphate synthase activity in source leaves and sucrolytic activities in sink organs were analysed in two lines of Medicago ciliaris (salt-tolerant TNC 1.8 and salt-sensitive TNC 11.9). SNF (measured as nitrogenase activity and amount of N-fixed) was more affected by salt treatment in the TNC 11.9 than in TNC 1.8, and this could be explained by a decrease in nodule sucrolytic activities. SNF capacity was reflected in leaf biomass production and in the sink activity under salinity, as suggested by the higher salt-induced decrease in the young leaf sucrolytic activities in the sensitive line TNC 11.9, while they were not affected in the tolerant line TNC 1.8. As a consequence of maintaining sink activities in the actively growing organs, the key enzymatic activity for synthesis of sucrose (sucrose phosphate synthase) was also less affected in the mature leaves of the more tolerant genotype. Ours results showed also that the major hormone factor associated with the relative tolerance of TNC 1.8 was the stimulation of abscisic acid concentration in young leaves under salt treatment. This stimulation may control photosynthetic organ growth and also may contribute to a certain degree in the maintenance of coordinated sink-source relationships. Therefore, ABA may be an important component which conserves sucrose synthesis in source leaves.

References

  1. 1.

    Albacete, A., Ghanem, M. E., Martinez-Andújar, C., Acosta, M., Sánchez-Bravo, J., Martínez, V., Lutts, S., Dodd, I. C., Pérez-Alfocea, F. (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinised tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 59, 4119–4131.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Balibrea, M. E., Dell’Amico, J., Bolarin, M. C., Pérez-Alfocea, F. (2000) Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiol. Plant. 110, 503–511.

    CAS  Google Scholar 

  3. 3.

    Balibrea, M. E., Cuartero, J., Bolarin, M. C., Pérez-Alfocea, F. (2003) Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity. Physiol. Plant. 118, 38–46.

    CAS  PubMed  Google Scholar 

  4. 4.

    Ben Salah, I., Albacete, A., Martínez Andújar, C., Haouala, R., Labidi, N., Zribi, F., Martinez, V., Pérez-Alfocea, F., Abdelly, C. (2009) Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress. J. Plant Physiol. 166, 477–488.

    CAS  PubMed  Google Scholar 

  5. 5.

    Brault, M., Maldiney, R., Miginiac, E. (1997) Cytokinin-binding proteins. Physiol. Plant. 100, 520–527.

    CAS  Google Scholar 

  6. 6.

    Cheikh, N., Brenner, M. L. (1992) Regulation of key enzymes of sucrose biosynthesis in soybean leaves. Plant Physiol. 100, 1230–1237.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Doehlert, D. C., Huber, S. C. (1983) Regulation of spinach leaf sucrose phosphate synthase by glucose-6-phosphate, inorganic phosphate, and pH. Plant Physiol. 73, 989–994.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Galtier, N., Foyer, C. H., Huber, J. L., Voelker, T. A., Huber, S. C. (1993) Effects of elevated sucrosephosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycopersicon esculentum var UC82B). Plant Physiol. 101, 535–5439.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Ghanem, M. E., Albacete, A., Martinez-Andújar, C., Acosta, M., Romero-Aranda, R., Dodd, I. C., Lutts, S., Pérez-Alfocea, F. (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J. Exp. Bot. 59, 3039–3050.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Hardy, W. F R., Holsten, R., Jackson, E., Burns, E. (1968) The acetylene ethylene assay for nitrogen fixation: lab and field assay for nitrogen evaluation. Plant Physiol. 43, 1185–1207.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Hare, P. D., Cress, W. A., Van Staden, J. (1997) The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul. 23, 79–103.

    CAS  Google Scholar 

  12. 12.

    Hartig, K., Beck, E. (2006) Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol. 8, 389–396.

    CAS  PubMed  Google Scholar 

  13. 13.

    Hewitt, E. J. (1966) Sand and Water Culture Methods Used in the Study of Plant Nutrition, 2nd ed. Commonwealth Bureau of Horticulture Technical Communications, p. 22.

    Google Scholar 

  14. 14.

    Huber, S. C. (1983) Role of sucrose phosphate synthase in partitioning of carbon in leaves. Plant Physiol. 71, 818–821.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Huber, S. C., Huber, J. L. (1996) Role and regulation of sucrose phosphate synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 432–444.

    Google Scholar 

  16. 16.

    Isopp, H., Frehner, M., Long, S. P., Nösberger, J. (2000) Sucrose-phosphate synthase responds differently to source-sink relations and to photosynthetic rates: Lolium perenne L. growing at elevated pCO2 in the field. Plant Cell Environ. 23, 597–607.

    CAS  Google Scholar 

  17. 17.

    Jebara, S., Drevon, J. J., Jebara, M. (2010) Modulation of symbiotic efficiency and nodular antioxidant enzyme activities in two Phaseolus vulgaris genotypes under salinity. Acta Physiol. Plant. 32, 925–932.

    Google Scholar 

  18. 18.

    Kieseleva, I. S., Kaminskaya, O. A. (2002) Hormonal regulation of assimilate utilization in barley leaves in relation to the development of their source function. Russ. J. Plant Physiol. 49, 534–540.

    Google Scholar 

  19. 19.

    Kjeldahl, J. Z. (1983) Neue Methode zur Bestimmung des Stickstoffs in organischen Körpern. Anal. Chem. 22, 366–382.

    Google Scholar 

  20. 20.

    Klein, R. R., Crafts-Brandner, S. J., Salvucci, M. E. (1993) Cloning and developmental expression of the sucrose-phosphate synthase gene from spinach. Planta 190, 498–510.

    CAS  PubMed  Google Scholar 

  21. 21.

    Ladrera, R., Marino, D., Larrainzar, E., González, E. M., Arrese-Igor, C. (2007) Reduced carbon availability to bacteroids and elevated ureids in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol. 145, 539–546.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    López, M., Herrera-Cervera, J. A., Iribarne, C., Tejera, N. A., Lluch, C. (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: Nodule carbon metabolism. J. Plant Physiol. 165, 641–650.

    PubMed  Google Scholar 

  23. 23.

    M’rah, S., Ouerghi, Z., Berthomieu, C., Havaux, M., Jungas, C., Hajji, M., Grignon, C., Lachaâl, M. (2006) Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila. J. Plant Physiol. 163, 1022–1031.

    PubMed  Google Scholar 

  24. 24.

    Meloni, D. A., Oliva, M. A., Martinez, C. A., Cambraia, J. (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 49, 69–76.

    CAS  Google Scholar 

  25. 25.

    Munné-Bosch, S., Alegre, L. (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Fund. Plant Biol. 31, 203–216.

    Google Scholar 

  26. 26.

    Munns, R. (2002) Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239–250.

    CAS  Google Scholar 

  27. 27.

    Munns, R., Husain, S., Rivelli, A. R., James, R. A., Condon, A. G., Lindsay, M. R., Lagudah, E. S., Schachtman, D. P., Hare, R. A. (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247, 93–105.

    CAS  Google Scholar 

  28. 28.

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

    CAS  Google Scholar 

  29. 29.

    Pelleschi, S., Rocher, J. P., Prioul, J. L. (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ. 20, 493–503.

    CAS  Google Scholar 

  30. 30.

    Ramos, M. L. G., Gordon, A. J., Minchin, F. R., Sprint, J. I., Parsons, R. (1999) Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean (Phaseolus vulgaris L.). Ann. Bot. 83, 57–63.

    CAS  Google Scholar 

  31. 31.

    Rivero, R. M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., Blumwald, E. (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proceedings of the National Academy of Sciences USA 104, 19631–19636.

    CAS  Google Scholar 

  32. 32.

    Roitsch, T. (1999) Source-sink regulation by sugar and stress. Curr. Opin. Plant Biol. 2, 198–206.

    CAS  PubMed  Google Scholar 

  33. 33.

    Serraj, R., Fleurat-Lessard, P., Jaillard, B., Drevon, J. J. (1995) Structural changes in the inner-cortex cells of soybean root nodules are induced by short-term exposure to high salt or oxygen concentrations. Plant Cell Environ. 18, 455–462.

    CAS  Google Scholar 

  34. 34.

    Sharp, R. E. (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ. 25, 211–222.

    CAS  Google Scholar 

  35. 35.

    Soussi, M., Lluch, C., Ocaña, A. (1999) Comparative study of nitrogen fixation and carbon metabolism in two chick-pea (Cicer arietinum L.) cultivars under salt stress. J. Exp. Bot. 50, 1701–1708.

    CAS  Google Scholar 

  36. 36.

    Stearns, J. C., Glick, B. R. (2003) Transgenic plants with altered ethylene biosynthesis or perception. Biotech. Advances 21, 193–210.

    CAS  Google Scholar 

  37. 37.

    Stitt, M., Gerhardt, R., Wilke, I., Heldt, H. W. (1987) The contribution of fructose-2,6-bisphosphate to the regulation of sucrose synthesis during photosynthesis. Physiol. Plant. 69, 377–386.

    CAS  Google Scholar 

  38. 38.

    Sturm, A., Tang, G. Q. (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 4, 401–407.

    CAS  PubMed  Google Scholar 

  39. 39.

    Vassey, T. L., Sharkey, T. D. (1989) Mild water stress of Phaseolus vulgaris plants leads to reduce starch synthesis and extractable sucrose phosphate synthase activity. Plant Physiol. 89, 1066–1070.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Vessey, J. K., Waterer, J. (1992) In search of the mechanism of nitrate inhibition of nitrogenase activity in legume nodules: recent developments. Physiol. Plant. 84, 171–176.

    CAS  Google Scholar 

  41. 41.

    Vreugdenhil, D. (1983) Abscisic acid inhibits phloem loading of sucrose. Plant Physiol. 57, 463–467.

    CAS  Google Scholar 

  42. 42.

    Wulfetange, K., Saenger, W., Schmülling, T., Heyl, A. (2010) E. coli-based cell-free expression, purification and characterization of the membrane-bound ligand-binding CHASE-TM domain of the cytokinin receptor CRE1/AHK4 of Arabidopsis thaliana. Mol. Biotechnol. PMID: 20886313 epublc. ahead of print.

    Google Scholar 

  43. 43.

    Xiong, L. (2007) Abscisic acid in plant response and adaptation to drought and salt stress. In: Jenks, M. A., Hasegawa, P. M., Mohan Jain, S. (eds) Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. Springer, Dordrecht, pp. 193–221.

    Google Scholar 

  44. 44.

    Zahran, H. H. (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 63, 968–989.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Zimmerman, R. C., Kohrs, D. G., Steiler, D. L., Alberte, R. S. (1995) Carbon partitioning in eelgrass. Plant Physiol. 108, 1665–1671.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Zribi, K., Badri, Y., Saidi, S., van Berkum, R., Aouani, M. E. (2007) Medicago ciliaris growing in Tunisian soils is preferentially nodulated by Sinorhizobium medicae. Austral. J. Soil Res. 45, 473–477.

    Google Scholar 

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Correspondence to Imène Ben Salah.

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Salah, I.B., Jelali, N., Slatni, T. et al. Involvement of Source-Sink Relationship and Hormonal Control in the Response of Medicago Ciliaris — Sinorhizobium Medicae Symbiosis to Salt Stress. BIOLOGIA FUTURA 63, 97–112 (2012). https://doi.org/10.1556/ABiol.63.2012.1.8

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Keywords

  • Nitrogen fixation
  • phytohormones
  • salt stress
  • source-sink activity
  • sucrose enzyme activities