Download PDF
Plant Biol (Stuttg) 2004; 6(6): 702-707
DOI: 10.1055/s-2004-821293
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Importance of N Source on Heat Stress Tolerance Due to the Accumulation of Proline and Quaternary Ammonium Compounds in Tomato Plants

R. M. Rivero1 , J. M. Ruiz2 , L. M. Romero2
  • 1University of Davis-California, Department of Pomology, Wickson Hall 1048, One Shields Avenue, Davis 95616, CA, USA
  • 2Department of Plant Physiology, Faculty of Sciences, University of Granada, 18071 Granada, Spain
Further Information

Publication History

Received: November 17, 2003

Accepted: July 30, 2004

Publication Date:
20 October 2004 (online)

   Permissions and Reprints

Abstract

Proline and quaternary ammonium compounds (QAC), in addition to being N-rich, are known to accumulate in plants under different environmental stress conditions. The accumulation of N-rich compounds in plants has been shown to confer stress resistance. The aim of our work is two-fold: first, to study the influence of temperature on proline, QAC, and choline metabolism in tomato leaves; and second, to investigate the relationship between N source applied (NO3 - or NH4 +) and thermal stress resistance in these plants. To do this, experiments were conducted at three different temperatures (10 °C, 25 °C, 35 °C); at each temperature half of the plants received NO3 -, and the other half received NH4 +. At 35 °C the plants had the lowest biomass production with respect to 25 °C (optimal temperature) and 10 °C (cold stress), suggesting that tomato plants were most affected by heat stress. At 35 °C, there were also high levels of choline and proline due to the activation of Δ1-pyrroline-5-carboxylate synthetase (P5CS) and ornithine aminotransferase (OAT), and simultaneous inhibition of proline dehydrogenase (PDH) and proline oxidase (PO). However, plants with NH4 + as the N source exhibited reduced growth with respect to the plants fed with NO3 -. This is interesting because, under heat stress (35 °C), biomass production, as well as proline and choline accumulation, in NH4 + fed plants was higher than in NO3 - fed plants. From this, we concluded that tomato plants fed with NH4 + as the N source show higher tolerance to heat stress (35 °C) than plants fed with NO3 -.

Key words

Choline - heat stress - Lycopersicon esculentum L. - N source - proline - quaternary ammonium compounds

References

  • 1 Becker T. W., Fock H. P.. The activity of nitrate reductase and the pool size of some amino acids and some sugars in water-stressed maize leaves.  Photosynthesis Research. (1986);  8 267-274
    CrossrefPubMedGoogle Scholar
  • 2 Bohnert H. J., Nelson D. E., Jensen R. G.. Adaptations to environmental stresses.  The Plant Cell. (1995);  7 1099-1111
    PubMedGoogle Scholar
  • 3 Bradford M. M.. A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein-dye binding.  Analytical Biochemistry. (1976);  72 248-254
    PubMedGoogle Scholar
  • 4 Brinen G. H.. Plant and row apacing, mulch and fertilizer rate effects on watermelon production.  Journal of the American Society of Horticultural Science. (1979);  104 724-726
    PubMedGoogle Scholar
  • 5 Bryan J. K.. The biochemistry of plants: A comprehensive treatise. Miflin, B. J. and Lea, P. J., eds. Intermediary Nitrogen Metabolism, Vol. 16. San Diego; Academic Press Inc. (1990): 161-195
    Google Scholar
  • 6 Chang Y. C., Lee T. M.. High temperature-induced free proline accumulation in Gracilaria tenuistipitata (Rhodophyta).  Botanical Bulletin of the Academy Sinensis. (1999);  40 289-294
    PubMedGoogle Scholar
  • 7 Charest C., Phan C. T.. Cold acclimation of wheat: Properties of enzymes involved in proline metabolism.  Physiologia Plantarum. (1990);  80 159-168
    CrossrefPubMedGoogle Scholar
  • 8 Chen T. H. H., Murata N.. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes.  Current Opinion in Plant Biology. (2002);  5 250-257
    CrossrefPubMedGoogle Scholar
  • 9 Che T. M., Aspinall D., Paleg L. G.. Stress metabolism. VI. Temperature stress and the accumulation of proline in barley and radish.  Australian Journal of Plant Physiology. (1974);  1 87-97
    PubMedGoogle Scholar
  • 10 Davies W. J., van Volkenburg E.. The influence of water deficit on the factors controlling the daily pattern of growth of Phaseolus trifoliates. .  Journal of Experimental Botany. (1983);  34 987-999
    PubMedGoogle Scholar
  • 11 Delauney A. J., Verma D. P. S.. Proline biosynthesis and osmoregulation in plants.  The Plant Journal. (1993);  4 215-223
    CrossrefPubMedGoogle Scholar
  • 12 Dhindsa R. S., Cleland R. B.. Water stress and protein synthesis.  Plant Physiology. (1975);  55 781-788
    PubMedGoogle Scholar
  • 13 Geladopoulus T. P., Sotiroudis T. G., Evangelopoulus A. E.. A malachite green colorimetric assay for protein phosphatase activity.  Analytical Biochemistry. (1991);  192 112-116
    CrossrefPubMedGoogle Scholar
  • 14 Grive C. M., Gratton R.. Rapid assay for determination of water soluble quaternary ammonium compounds.  Plant and Soil. (1983);  70 303-307
    PubMedGoogle Scholar
  • 15 Huang A. H., Cavaliery A. J.. Proline oxidase and water stress-induced proline accumulation in spinach leaves.  Plant Physiology. (1979);  63 531-535
    PubMedGoogle Scholar
  • 16 Irigoyen J. J., Emerich D. W., Sánchez-Díaz M.. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants.  Physiologia Plantarum. (1992);  84 55-60
    CrossrefPubMedGoogle Scholar
  • 17 Kavi Kishor P. B. K., Hong Z., Miao G. H., Hu C. A. A., Verma D. P. S.. Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants.  Plant Physiology. (1995);  108 1387-1394
    PubMedGoogle Scholar
  • 18 Kuo C. G., Chen H. M., Ma L. H.. Effect of high temperature on proline content in tomato floral buds and leaves.  Journal of the American Society of Horticultural Science. (1986);  111 746-750
    PubMedGoogle Scholar
  • 19 Kuznestov V. V., Shevyakova N. I.. Stress responses of tobacco cells to high temperature and salinity.  Proline Accumulation and Phosphorylation of Polypeptides. (1997);  100 320-326
    PubMedGoogle Scholar
  • 20 Le-Rundulier D., Strom A. R., Dandekar A. M., Smith L. T., Valentine R. C.. Molecular biology of osmoregulation.  Science. (1984);  224 1064-1068
    PubMedGoogle Scholar
  • 21 Lin C. C., Kao C. H.. Regulation of ammonium-induced proline accumulation in detached rice leaves.  Plant Growth Regulation. (2001);  35 69-74
    CrossrefPubMedGoogle Scholar
  • 22 Madan S., Nainawatee H. S., Jain R. K., Chowdhury J. B.. Proline and proline metabolising enzymes in in-vitro selected NaCl-tolerant Brassica Juncea L. under salt stress.  Annals of Botany. (1995);  76 51-57
    CrossrefPubMedGoogle Scholar
  • 23 Maroto J. V.. Hortalizas aprovechables por sus frutos: tomate. Maroto J. V., ed. Horticultura Herbácea Especial, 4th ed. Madrid, España; Mundiprensa (1995): 714 -775
    Google Scholar
  • 24 McCue R. F., Hanson A. D.. Drought and salt tolerance: toward understanding and application.  TIBTECH. (1990);  8 358-362
    PubMedGoogle Scholar
  • 25 Naidu B. P., Paleg L. G., Aspinall D., Jennings A. C., Jones G. P.. Amino acids and glycine betaine accumulation in cold-stressed wheat seedlings.  Phytochemistry. (1991);  30 407-409
    CrossrefPubMedGoogle Scholar
  • 26 Paleg L. G., Douglas T. J., Van Daal A., Keech D. B.. Proline, betaine and other organic solutes protect enzymes against heat inactivation.  Australian Journal of Plant Physiology. (1981);  8 107-114
    PubMedGoogle Scholar
  • 27 Paquin R., Lechasseur P.. Observations sur une méthode de dosage de la proline libre dans les extraits de plantes.  Canadian Journal of Botany. (1979);  57 1851-1854
    PubMedGoogle Scholar
  • 28 Polesskaya O. G., Kashirina E. I., Andreeva S. E., Goryaeva O. V., Glazunova M. A., Alekhina N. D.. Morphophysiological indices of the source leaf in wheat plants acclimated to conditions of nitrogen nutrition.  Russian Journal of Plant Physiology. (2001);  48 716-722
    CrossrefPubMedGoogle Scholar
  • 29 Rathinasabapathi B., Gage D., Mackill D., Hanson A.. Cultivated and wild rices do not accumulate glycine-betaine due to deficiencies in two biosynthetic steps.  Crop Science. (1993);  33 534-538
    PubMedGoogle Scholar
  • 30 Rathinasabapathi B., Sigua C., Ho J., Gage D. A.. Osmoprotectant α-alanine betaine synthesis in the Plumbaginaceae: S-adenosyl-L-methionine dependent N-methylation of α-alanine to its betaine is via N-methyl and N,N-diemethyl α-alanines.  Physiologia Plantarum. (2000);  109 225-231
    CrossrefPubMedGoogle Scholar
  • 31 Schobert B., Tschesche H.. Unusual solution properties of proline and its interaction with proteins.  Biochemica and Biophysica Acta. (1978);  541 270-277
    PubMedGoogle Scholar
  • 32 Sese M. L., Shono M., Tobita S.. Effects of proline and betaine on heat inactivation of ribulose-1,5-biphosphate carboxilase/oxygenase in crude extracts of rice seedlings.  Photosynthesis. (1999);  36 557-563
    PubMedGoogle Scholar
  • 33 Stewart G. R., Lee J. A.. The role of proline accumulation in halophytes.  Planta. (1974);  120 279-289
    CrossrefPubMedGoogle Scholar
  • 34 Storey R., Ahmad N., Wyn Jones R. G.. Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants.  Oecologica. (1977);  27 319-322
    PubMedGoogle Scholar
  • 35 Tully R. E., Hanson A. D., Nelson C. E.. Proline accumulation in water stressed barley leaves in relation to translocation and the nitrogen budget.  Plant Physiology. (1979);  63 518-523
    PubMedGoogle Scholar
  • 36 Van Zinderen E. M.. Development of hydroponic system and look into the future. In Annual Conference on Hydroponics, Hydroponics Society of America, Concord, CA. (1986): 371-372
    Google Scholar
  • 37 Weretilnyk E. A., Hanson A. D.. Betaine aldehyde dehydrogenase from spinach leaves: purification, in vitro translation the mRNA, and regulation by salinity.  Archives of Biochemistry and Biophysics. (1989);  271 56-63
    CrossrefPubMedGoogle Scholar
  • 38 Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N.. Living with water stress: evolution of osmolyte systems.  Science. (1982);  217 1214-1222
    CrossrefPubMedGoogle Scholar
  • 39 Zhang C. S., Lu Q., Verma D. P. S.. Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalizing the first two steps of proline biosynthesis in plants.  Journal of Biological Chemistry. (1995);  270 20491-20496
    CrossrefPubMedGoogle Scholar

R. M. Rivero

University of Davis-California
Department of Pomology
Wickson Hall 1048

One Shields Avenue

Davis, CA 95616

USA

Email: rmrivero@ucdavis.edu

Editor: J. T. M. Elzenga

      >