Advertisement

Acta Biologica Hungarica

, Volume 63, Issue 1, pp 97–112 | Cite as

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

  • Imène Ben SalahEmail author
  • Nahida Jelali
  • T. Slatni
  • Margaret Gruber
  • A. Albacete
  • Cristina Martínez Andújar
  • V. Martinez
  • F. Pérez-Alfocea
  • C. Abdelly
Open Access
Article
First Online:
  • 1 Downloads

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.

Keywords

Nitrogen fixation phytohormones salt stress source-sink activity sucrose enzyme activities 
Download to read the full article text

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.PubMedPubMedCentralGoogle 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.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.PubMedGoogle 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.PubMedGoogle Scholar
  5. 5.
    Brault, M., Maldiney, R., Miginiac, E. (1997) Cytokinin-binding proteins. Physiol. Plant. 100, 520–527.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.PubMedPubMedCentralGoogle 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.PubMedPubMedCentralGoogle 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.PubMedPubMedCentralGoogle 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.PubMedPubMedCentralGoogle 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.PubMedPubMedCentralGoogle 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.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.PubMedGoogle 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.PubMedPubMedCentralGoogle 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.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.PubMedGoogle 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.PubMedPubMedCentralGoogle 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.PubMedGoogle 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.PubMedGoogle 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.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.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.Google Scholar
  28. 28.
    Munns, R., Tester, M. (2008) Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59, 651–681.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.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.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.Google Scholar
  32. 32.
    Roitsch, T. (1999) Source-sink regulation by sugar and stress. Curr. Opin. Plant Biol. 2, 198–206.PubMedGoogle 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.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.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.Google Scholar
  36. 36.
    Stearns, J. C., Glick, B. R. (2003) Transgenic plants with altered ethylene biosynthesis or perception. Biotech. Advances 21, 193–210.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.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.PubMedGoogle 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.PubMedPubMedCentralGoogle 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.Google Scholar
  41. 41.
    Vreugdenhil, D. (1983) Abscisic acid inhibits phloem loading of sucrose. Plant Physiol. 57, 463–467.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.PubMedPubMedCentralGoogle 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.PubMedPubMedCentralGoogle 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

Copyright information

© Akadémiai Kiadó, Budapest 2012

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Imène Ben Salah
    • 1
    Email author
  • Nahida Jelali
    • 1
  • T. Slatni
    • 1
  • Margaret Gruber
    • 3
  • A. Albacete
    • 2
  • Cristina Martínez Andújar
    • 2
  • V. Martinez
    • 2
  • F. Pérez-Alfocea
    • 2
  • C. Abdelly
    • 1
  1. 1.Laboratoire de Plantes ExtrêmophilesCBBCTunisia
  2. 2.Department of Plant NutritionCEBAS-CSICMurciaSpain
  3. 3.Saskatoon Research CentreAgriculture and Agri-Food Canada. 107 Science CrescSaskatoonCanada

Personalised recommendations