Towards the Production of Salt-Tolerant Crops

  • B. J. Barkla
  • R. Vera-Estrella
  • O. Pantoja
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 464)


Crop production is affected by numerous environmental factors, with soil salinity and drought having the most detrimental effects. Attempts to improve yield under stress conditions by plant breeding have been unsuccessful, primarily due to the multigenic origin of the adaptive responses. The transfer of genes through genetic engineering of crop plants appears more feasible. Important adaptive mechanisms targeted for potential gene transfer would be the tonoplast Na+H+ antiport, compatible solute synthesis and, regulation of water channel activity and expression, mechanisms involved in cellular osmoregulation. In this review we discuss recent advances in our understanding of these adaptive mechanisms.


Salt Stress Compatible Solute CRASSULACEAN Acid Metabolism Proline Accumulation Glycine Betaine 
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  1. Adams, P.; Nelson, D.E.; Yamada, S.; Chmara, W.; Jensen, R.G.; Bohnert, HJ.; Griffiths, H. Growth and development of Mesembryanthemum crystallinum (Aizoacae). New Phytol. 1998, 138, 171–190.CrossRefGoogle Scholar
  2. Adams, P.; Thomas, J.C.; Vernon, D.M.; Bohnert, HJ.; Jensen, R.G. Distinct cellular and organismic responses to salt stress. Plant Cell Physiol 1992, 33, 1215–1223.Google Scholar
  3. Azaizeh, H.; Gunse, B.; Steudle, E. Effects of NaCl and CaCl2 on water transport across root cells of Maize (Zea mays L.) seedlings. Plant Physiol. 1992, 99, 886–894.PubMedCrossRefGoogle Scholar
  4. Barkla, B.J.; Blumwald, E. Identification of a 170-kDa protein associated with the vacuolar Na+H+ antiport of Beta vulgaris. Proc. Natl. Acad. Sci. USA 1991, 88, 11177–11181.PubMedCrossRefGoogle Scholar
  5. Barkla, B.J.; Apse, M.P.; Manolson, M.F.; Blumwald, E. The plant vacuoiar Na+/H+ antiport. In Membrane transport in Plants and Fungi: Molecular mechanisms and control, Blatt, M.R., Leigh, R.A., Sanders, D.A., Eds.; Company of Biologists: Cambridge, 1994. Google Scholar
  6. Barkla, B.J.; Zingarelli, L.; Blumwald, E.; Smith, J.A.C. Tonoplast Na+/H+ antiport activity and its energization by the vacuoiar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum. Plant Physiol 1995, 105, 549–556.Google Scholar
  7. Binzel, M.L.; Dunlap, J.R. Abscisic acid does not mediate NaCl-induced accumulation of 70-kDa subunit tonoplast H+-ATPase message in tomato. Planta 1995, 197, 563–568.CrossRefGoogle Scholar
  8. Blumwald, E.; Poole, R.J.; Salt tolerance in suspension cultures of sugar beet: induction of Na+/H+ antiport activity at the tonoplast by growth in salt. Plant Physiol 1987, 83, 884–887.PubMedCrossRefGoogle Scholar
  9. Bohnert, HJ.; Nelson, D.E.; Jensen, R.G. Adaptations to environmental Stresses. Plant Cell. 1995, 7, 1099–1111.PubMedGoogle Scholar
  10. Chu, C.,; Dai, Z.; Ku, M.S.B.; Edwards, G.E. Induction of crassulacean acid metabolism in the facultative halo-phyte Mesembryanthemum crystallinum by abscisic acid. Plant Physiol 1990,93,1253–1260.PubMedCrossRefGoogle Scholar
  11. Cushman, J.C. Characterization and expression of NADP-malic enzyme cDNA induced by salt stress from the facultative CAM plant, Mesembryanthemum crystallinum. Eur. J. Biochem. 1992, 208, 259–266.PubMedCrossRefGoogle Scholar
  12. Cushman, J.C. Molecular cloning and expression of chloroplast NADP-malate dehydrogenase during crassulacean acid metabolism induction by salt stress. Photosynth. Res. 1993, 35, 15–27.CrossRefGoogle Scholar
  13. Cushman, J.C.; Bohnert, H.J. Molecular genetics of Crassulacean acid metabolism. Plant Physiol 1997, 113, 667–676.PubMedGoogle Scholar
  14. Cushman, J.C.; Bohnert, H.J. Transcriptional activation of CAM genes during development and environmental stress. In Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution; Winter, K., Smith, J.A.C. Eds. Springer-Verlag: Berlin, 1996.Google Scholar
  15. Cushman, J.C.; Meyer, G.; Michalowski, C.B.; Schmitt, J.M.; Bohnert, HJ. Salt stress leads to differential expression of phosphoenolpyruvate carboxylase during crassulacean acid metabolism induction in the common ice plant. Plant Cell. 1989, 1, 715–725.PubMedGoogle Scholar
  16. Cushman, J.C.; Vernon, D.M.; Bohnert, HJ. ABA and the transcriptional control of CAM induction during salt stress in the common ice plant. In Control of plant gene expression; Verma, D.P.S. Ed. CRC Press; Boca Raton, 1993. Google Scholar
  17. Daniels, M.J.; Chaumont, F.; Mirkov, T.E.; Chrispeels, M.J. Characterization of a new vacuoiar membrane aquaporin sensitive to mercury at a unique site. Plant Cell. 1996, 8, 587–599.PubMedGoogle Scholar
  18. Daniels, M.J.; Mirkov, T.E.; Chrispeels, M.J. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 1994, 106, 1325–1333.PubMedCrossRefGoogle Scholar
  19. Delauney, A.J.; Verma, D.P.S. Proline biosynthesis and osmoregulation in plants. Plant J. 1993, 4, 215–223.CrossRefGoogle Scholar
  20. Demming, B.; Winter, K. Sodium, potassium, chloride and proline concentrations of chloroplasts isolated from the halophyte, Mesembryanthemum crystallinum. Planta. 1986, 168, 421–426.CrossRefGoogle Scholar
  21. Dietz, K.J.; Arbinger, B. cDNA sequence and expression of subunit E of the vacuoiar H+-ATPase in the inducible Crassulacean acid metabolism plant Mesembryanthemum crystallinum. Biochem. Biophys. Acta 1996, 1281,134–138.PubMedCrossRefGoogle Scholar
  22. Edwards, u.E.; Dai, Z.; Cheng, S.H.; Ku, M.S.B. Factors affecting the induction of crassulacean acid metabolism in Mesembryanthemum crystallinum. In Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution; Winter, K., Smith, J.A.C. Eds. Springer-Verlag: Berlin, 1996. Google Scholar
  23. El-Ghareeb, R. Vegetation and soil changes induced by Mesembryanthemum crystallinum L. in a Mediterranean desert ecosystem. J. Arid Environments. 1991, 20, 321–330.Google Scholar
  24. Flowers, J.T.; Yeo, R.A. Breeding for salinity resistance in crop plants: where next? Aust. J. Plant. Physiol. 1995, 22,875–884.CrossRefGoogle Scholar
  25. Garbarino, J.; DuPont, F.M. NaCl induced a Na+/H+ antiport in tonoplast vesicles from barley roots. Plant Physiol. 1988,86,231–236.PubMedCrossRefGoogle Scholar
  26. Guerrero, F.D.; Jones, J.T.; Mullet, J.E. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol. 1990, 15, 11–26.PubMedCrossRefGoogle Scholar
  27. Hanson, A.D.; Rathinasabapathi, B.; Rivoal, J.; Burnet, M.; Dillon, M.O.; Gage, D.A. Osmoprotective compounds in the Plumbaginaceae: A natural experiment in metabolic engineering of stress tolerance. Proc. Natl. Acad. Sci. USA 1994, 91, 306–310.PubMedCrossRefGoogle Scholar
  28. Hare, P.D.; Cress, W.A. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 1997,21,79–102.CrossRefGoogle Scholar
  29. Hetherington, A.M.; Quatrano, R.S. Mechanisms of action of abscisic acid at the cellular level. New Phytol. 1991, 119,9–32.CrossRefGoogle Scholar
  30. Johnson, K.D.; Herman, E.M.; Chrispeels, M.J. An abundant, highly conserved tonoplast protein in seeds. Plant Physiol. 1989, 91, 1006–1013.PubMedCrossRefGoogle Scholar
  31. Kaldenhoff, R.; Kölling, A.; Meyers, J.; Karmann, U.; Ruppel, G.; Richter, G. The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J. 1995, 7, 87–95.PubMedCrossRefGoogle Scholar
  32. Kammerloher, W.; Fisher, U.; Piechottka, G.P.; Schaffner, A.R. Water channels in the plant plasma membrane cloned by immurioselection from a mammalian expression system. Plant J. 1994, 6, 187–199.PubMedCrossRefGoogle Scholar
  33. Kishor, P.; Hong, Z.L.; Miao, G.H.; Hu, C; Verma, D. Overexpression of delta-pyrroline-5-carboxylate synthase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 1995, 108, 1387–1394.PubMedGoogle Scholar
  34. Letham, D.S.; Palni, L.M.S. The biosynthesis and metabolism of cytokinins. Ann. Rev. Plant Phyiol. 1983, 34, 163–197.CrossRefGoogle Scholar
  35. Liu, J.; Zhu, J-K. Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol. 1991, 114, 591–596.CrossRefGoogle Scholar
  36. Löw, R.; Rockel, B.; Kirsch, M.; Ratajczak, R.; Hörtensteiner, S.; Martinoia, E., Lüttge, U.; Rausch, T. Early stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol. 1996, 110, 259–265.PubMedCrossRefGoogle Scholar
  37. Matsumoto, H.; Chung, G.C. Increase in proton-transport activity of tonoplast vesicles as an adaptive response of barley roots to NaCl stress. Plant Cell Physiol. 1988, 29, 1133–1140.Google Scholar
  38. Maurel, C. Aquaporins and water permeability of plant membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997,48,399–429.PubMedCrossRefGoogle Scholar
  39. Maurel, C.; Tacnet, F.; Güelü, J.; Guern, J.; Ripoche, P. Purified vesicles of tobacco cells vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc. Nati. Acad. Sci. USA. 1997, 94, 7103–7108.CrossRefGoogle Scholar
  40. Maurel, C.; Reizer, J.; Schroeder, J.I.; Chrispeels, M.J. The vacuolar membrane protein Y-TIP creates water specific channels in Xenopus oocytes. EMBO J. 1993. 12, 2241–2247.Google Scholar
  41. McCue, K.F.; Hanson, A.D. Drought and salt tolerance: towards thé understanding and application. Trends Biotechnol. 1990, 8, 358–362.CrossRefGoogle Scholar
  42. McElwain, E.F,; Bohnert, HJ.; Thomas, J.C. Light moderates the induction of phosphoenolpyruvate carboxylase by NaCl and abscisic acid in Mesembryanthemum crystallinum. Plant Physiol. 1992, 99, 1261–1264.PubMedCrossRefGoogle Scholar
  43. Nakamura, Y.; Kasamo, K.; Shimosato, N.; Sakata, M.; Ohta, E. Stimulation of the extrusion of protons and H+-ATPase activities with the decline in pyrophosphatase activity of the tonoplast in intact mung bean roots under high-NaCl stress and its relation to external levels of Ca2+ ions. Plant Cell Physiol. 1992, 33, 139–149.Google Scholar
  44. Narasimhan, M.L.; Binzel, M.L.; Perez-Prat, E.; Chen, Z.; Nelson, D.E.; Singh, N.K.; Bressan, R.A.; Hasegawa, P.M. NaCl regulation of tonoplast ATPase 70-kilodalton subunit mRNA in tobacco cells. Plant Physiol. 1991,97,562–568.PubMedCrossRefGoogle Scholar
  45. Nelson, D.E.; Rammesmayer, G.; Bohnert, H.J. The regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell 1998, 10,1–14.Google Scholar
  46. Niemietz, C.M.; Tyerman, S.D. Characterization of water channels in wheat root membrane vesicles. Plant Physiol. 1997, 115, 561–567.PubMedGoogle Scholar
  47. Osmond, C.B.; Greenway, H.; Salt response of carboxylation enzymes from species differing in salt tolerance. Plant Physiol. 1972, 49, 260–263.PubMedCrossRefGoogle Scholar
  48. Ostrem, J.A.; Vernon, D.M.; Bohnert, HJ. Increased expression of a gene coding for NAD:glyceraldehyde-3-phos-phate dehydrogenase during the transition from C3 photosynthesis to crassulacean acid metabolism in Mesembryanthemum crystallinum. J. Biol Chem. 1990,265, 3497–3502.PubMedGoogle Scholar
  49. Paul, M.J.; Cockburn, W. Pinitol, a compatible solute in Mesembryanthemum crystallinum. L. J. Exp. Bot. 1989, 40, 1093–1098.CrossRefGoogle Scholar
  50. Perera, I.Y.; Li, X.; Sze, H. Several distinct genes encode nearly identical 16 kDa proteolipids of the vacuolar H+-ATPase from Arabidopsis thaliana. Plant Mol Biol. 1995, 29, 227–244.PubMedCrossRefGoogle Scholar
  51. Raskin, I.; Nanda-Kumar, P.B.; Dushenkov, S.; Salt, D.E. Bioconcentration of heavy metals by plants. Current Biology 1994, 5, 285–290.Google Scholar
  52. Rockel, B.; Ratajczak, R.; Becker, A.; Lüttge, U. Changed densities and diameters of intra-membrane tonoplast particles of Mesembryanthemum crystallinum in correlation with NaCl-induced CAM. J. Plant Physiol. 1994,143,318–324.CrossRefGoogle Scholar
  53. Sarda, X.; Tousch, D.; Ferrare, K.; Legrand, E.; Dupuis, J.M.; Casse-Delbart, F.; Lamaze, T. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J. 1997, 12, 1103–1111.PubMedCrossRefGoogle Scholar
  54. Schäffner, A.R. Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 1998, 204, 131–139.PubMedCrossRefGoogle Scholar
  55. Sheveleva, E.; Chmara, W.; Bohnert, HJ.; Jensen, R.G. Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol. 1997, 115, 1211–1219.PubMedGoogle Scholar
  56. Smirnoff N.; Cumbes Q.J. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 1989, 28, 1057–1060.CrossRefGoogle Scholar
  57. Szaboles, I. The global problems of salt-affected soils. Acta Agronomica Hungarica 1987, 36, 159–172.Google Scholar
  58. Tarczynski, M.C.; Jensen, R.G.; Bohnert, H.J. Stress protection of transgenic tobacco by production of the os-molyte mannitol. Science. 1993, 259, 508–510.PubMedCrossRefGoogle Scholar
  59. Thomas, J.C.; Bohnert, HJ. Salt stress perception and plant growth regulators in the halophyte Mesembryanthemum crystallinum. Plant Physiol. 1993, 103, 1299–1304.PubMedGoogle Scholar
  60. Thomas, J.C.; De Armond, R.L.; Bohnert, HJ. Influence of NaCl on growth, proline, and phosphoenolpyruvate carboxylase levels in Mesembryanthemum crystallinum suspension cultures. Plant Physiol. 1992a, 98, 626–631.PubMedCrossRefGoogle Scholar
  61. Thomas, J.C.; McElwain, E.F.; Bohnert, HJ. Convergent induction of osmotic stress-responses. Abscisic acid, cy-tokinin, and the effects of NaCl. Plant Physiol. 1992b, 100, 416–423.PubMedCrossRefGoogle Scholar
  62. Thomas, J.C.; Sepahi, M,; Arendall, B.; Bohnert, HJ. Enhancement of seed germination in high salinity by engineering mannitol-expression in Arabidopsis thaliana. Plant Cell Environ. 1995, 18, 801–806.CrossRefGoogle Scholar
  63. Tsiantis, M.S.; Bartholomew, D.M.; Smith, J.A.C. Salt-regulation of transcript levels for the c subunit of a leaf vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum. Plant J. 1996, 9, 729–736.PubMedCrossRefGoogle Scholar
  64. van Schilfgaarde, J. Irrigated agriculture, is it sustainable? In Agricultural salinity assessment and management. Tanji, K. Ed. American Society of Civil Engineers; New York, 1990.Google Scholar
  65. Vera-Estrella R.; Barkla B.J.; Bohnert HJ.; Pantoja, O. Salt-stress in Mesembryanthemum crystallinum cell suspensions activates mechanisms similar to those observed in the whole plant. Plants 1999, 207, 426–435.CrossRefGoogle Scholar
  66. Vernon, D.M.; Bohnert, H.J. Increased expression of a myo-inositol methyl transferase in Mesembryanthemum crystallinum is part of a stress response distinct from crassulacean acid metabolism induction. Plant Physiol 1992, 99, 1695–1698.PubMedCrossRefGoogle Scholar
  67. Vernon, D.M.; Tarczynski, M.C.; Jensen, R.G.; Bohnert, H.J. Cyclitol production in transgenic tobacco. Plant J. 1993, 4, 199–205.CrossRefGoogle Scholar
  68. Yamada, S.; Katsuhara, M.; Kelly, W.B.; Michalowski, C.B.; Bohnert, H.J. A family of transcripts encoding water channel proteins: Tissue-specific expression in the common ice plant. Plant Cell 1995, 7, 1129–1142.PubMedGoogle Scholar
  69. Yamaguchi-Shinozaki, K.; Koizumi, M.; Urao, S.; Shinozaki, K. Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: Sequence analysis of one cDNA that encodes a putative transmembrane channel protein. Plant Cell Physiol. 1992, 3,217–224.Google Scholar
  70. Zingarelli, L.; Anzani, P.; Lado, P. Enhanced K+-stimulated pyrophosphatase activity in NaCl-adapted cells of Acer pseudoplatanus. Physiol. Plant. 1994, 91, 510–516.Google Scholar

Copyright information

© Springer Science+Business Media New York 1999

Authors and Affiliations

  • B. J. Barkla
    • 1
  • R. Vera-Estrella
    • 1
  • O. Pantoja
    • 1
  1. 1.Departamento de Biología Molecular de PlantasInstituto de Biotecnología, UNAMCol. Miraval CuernavacaMexico

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