Abstract
Throughout evolution, plants have developed various strategies to tolerate water stress. Among them, the accumulation of proline has been reported in a wide range of species. The metabolic pathway of this compatible solute is relatively well characterized in Arabidopsis thaliana. However, the signaling cascades involved in its regulation remain largely unknown. Thellungiella halophila, which is a close relative of Arabidopsis, tolerates extreme salinity up to 500 mM NaCl. In this work, the involvement of lipid signaling pathways in the regulation of proline accumulation was investigated in these two species upon water stress. A pharmacological approach has been performed using specific inhibitors of key signaling elements. The effects of these inhibitors have been investigated on proline accumulation. The present data show that phospholipases D (PLDs) are negative regulators of proline anabolism under normal conditions inA. thaliana. When such PLD-mediated regulation is abolished by 1-butanol, plants show a higher proline responsiveness to osmotic stress. In contrast to Arabidopsis, 1-butanol does not have any effect on proline accumulation in T. halophila under non-stress conditions. However, upon water constraints, 1-butanol reduces rather than increase proline accumulation. Our data suggest the involvement of a PLD-mediated signaling pathway in the tight regulation of proline metabolism that acts in a opposite way in A. thaliana and T. halophila. On the other hand, phospholipases C exert a positive control on proline accumulation in A. thaliana upon salt stress and a negative control in T. halophila upon water stress and non-stress conditions. In conclusion, we provide experimental evidence that positive and negative regulators are involved in the fine regulation of proline metabolism upon moderate water stress. Our study has defined a critical role of lipid signaling pathways in proline accumulation in A. thaliana and in T. halophila. Thus, in Arabidopsis, our data indicate that PLC-based signaling is a committed step in proline biosynthesis upon salinity but not upon hyperosmotic stress.
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References
Boyer JS (1982) Plant productivity and environment. Science 218: 443–448
Hare P, Cress W, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21: 535–553
Nakashima K, Satoh R, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1998) A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. Plant Physiol 118: 1233–1241
Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schütze K, Alonso R, Harter K, Vicente-Carbajosa J, Dröge-Laser W (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25: 3133–3143
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4: 215–223
Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants.Annu Rev Plant Biol 54: 265–306
DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and ino-sitol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis Plant Physiol 126: 759–769
Pical C, Westergren T, Dove SK, Larsson C, Sommarin M (1999) Salinity and hyperos-motic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J Biol Chem 274: 38232–38240
Drobak BK, Watkins PA (2000) Inositol(1,4,5)trisphosphate production in plant cells: An early response to salinity and hyperosmotic stress. FEBS Lett 481: 240–244
Takahashi S, Katagiri T, Hirayama T, Yamaguchi-Shinozaki K, Shinozaki K (2001) Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture. Plant Cell Physiol 42: 214–222
Testerink C, Munnik T (2005) Phosphatidic acid: A multifunctional stress signaling lipid in plants. Trends Plant Sci 10: 368–375
Frank W, Ratnadewi D, Reski R (2005) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220: 384–394
Munnik T, Meijer HJ,Ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22:147–154
Thiery L, Leprince AS, Lefebvre D, Ghars MA, Debarbieux E, Savouré A (2004) Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis thaliana. J Biol Chem 279:14812–14818
Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH et al (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280: 3697–3706
Parre E, Ghars MA, Leprince AS, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savoure A (2007) Calcium signaling via phospholipase C is essential for pro-line accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiol 144: 503–512
Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J et al (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737
Ghars MA, Parre E, Debez A, Bordenave M, Richard L, Leport L, Bouchereau A, Savouré A, Abdelly C (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol (in press)
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue culture. Physiol Plant 15: 473–497
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39: 205–207
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Ghars, M.A. et al. (2008). Opposite lipid signaling pathways tightly control proline accumulation in Arabidopsis thaliana and Thellungiella halophila . In: Abdelly, C., Öztürk, M., Ashraf, M., Grignon, C. (eds) Biosaline Agriculture and High Salinity Tolerance. Birkhäuser Basel. https://doi.org/10.1007/978-3-7643-8554-5_29
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DOI: https://doi.org/10.1007/978-3-7643-8554-5_29
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