AJPS  Vol.2 No.6 , December 2011
Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations
Abstract: Hydrologic alterations of river systems in western North America over the past century have increased soil salinity, contributing to the establishment and spread of an introduced halophytic species, Tamarix ramosissima (Ledeb.). The physiological responses of Tamarix ramosissima to salinity stress are incompletely known. To assess the salinity tolerance of this species, we measured several whole plant and leaf-level physiological responses of Tamarix ramosissima cuttings grown in a controlled environment over three NaCl concentrations (0, 15 and 40 g l-1). Tamarix ramosissima photosynthesis (A2000), stomatal conductance to water (gs), water potential (Ψw), and the maximum quantum yield of photosystem II (Fv/Fm) decreased at 15 and 40 g l-1 NaCl compared to control treatments. However, after approximately 35 days, Tamarix ramosissima had increased photosynthetic rates, maximum quantum yield of photosystem II, and stomatal conductance to water. These data suggests that physiological functioning of Tamarix ramosissima acclimated to extremely high NaCl concentrations over a relatively short period of time. Additionally, we present preliminary evidence that suggests proline synthesis may be the mechanism by which this species adjusts osmotically to increasing salinity.
Cite this paper: nullJ. Carter and J. Nippert, "Physiological Responses of Tamarix ramosissima to Extreme NaCl Concentrations," American Journal of Plant Sciences, Vol. 2 No. 6, 2011, pp. 808-815. doi: 10.4236/ajps.2011.26095.

[1]   P. Friederici, “The Alien Saltcedar,” American Forests, Vol. 101, No. 1-2, 1995, pp. 45-47.

[2]   J. Cleverly, S. Smith, A. Sala and D. Devitt, “Invasive Capacity of Tamarix ramosissima in a Mojave Desert Floodplain: The Role of Drought,” Oecologia, Vol. 108, 1997, pp. 583-595.

[3]   D. Busch and S. Smith, “Effects of Fire on Water and Salinity Relations of Riparian Woody Taxa,” Oecologia, Vol. 94, No. 2, 1993, pp. 186-194. doi:10.1007/BF00341316

[4]   J. B. Nippert, J. J. Butler, G. J. Kluitenberg, D. O. Whittemore, D. Arnold, S. E. Spal and J. K. Ward, “Patterns of Tamarix Water Use during a Record Drought,” Oecologia, Vol. 162, No. 2, 2010, pp. 283-292. doi:10.1007/s00442-009-1455-1

[5]   V. B. Beauchamp, C. Walz and P. B. Shafroth, “Salinity Tolerance and Mycorrhizal Responsiveness of Native Xeroriparian Plants in Semi-Arid western USA,” Applied Soil Ecology, Vol. 43, 2009, pp. 175-184. doi:10.1016/j.apsoil.2009.07.004

[6]   D. M. Merritt and N. L Poff, “Shifting Dominance of Riparian Populus and Tamarix along Gradients of Flow Alteration in Western North American Rivers,” Ecological Applications, Vol. 20, No. 1, 2010, pp. 135-152. doi:10.1890/08-2251.1

[7]   J. C. Stromberg, S. J. Lite, R. Marler, C. Paradzick, P. B. Shafroth, D. Shorrock, et al., “Altered Stream-Flow Regimes and Invasive Plant Species: The Tamarix Case,” Global Ecology and Biogeography, Vol. 16, No. 3, 2007, pp. 381-393. doi:10.1111/j.1466-8238.2007.00297.x

[8]   E. Glenn, R. Tanner, S. Mendez, T. Kehret, D. Moore, J. Garcia and C. Valdes, “Growth Rates, Salt Tolerance and Water Use Characteristics of Native and Invasive Riparian Plants from the Delta of the Colorado River Delta, Mexico,” Journal of Arid Environments, Vol. 40, No. 3, 1998, pp. 281-294. doi:10.1006/jare.1998.0443

[9]   E. Glenn and P. Nagler, “Comparative Ecophysiology of Tamarix ramosissima and Native Trees in Western U.S. Riparian Zones,” Journal of Arid Environments, Vol. 61, No. 3, 2005, pp. 419-446. doi:10.1016/j.jaridenv.2004.09.025

[10]   W. E. Hayes, L. R. Walker and E. A. Powell, “Competitive Abilities of Tamarix aphylla in Southern Nevada,” Plant Ecology, Vol. 202, No. 1, 2009, pp. 159-167. doi:10.1007/s11258-008-9569-9

[11]   G. E. Kleinkopf and A. Wallace, “Physiological Basis for Salt Tolerance in Tamarix ramosissima,” Plant Science Letters, Vol. 3, No. 3, 1974, pp. 157-163. doi:10.1016/0304-4211(74)90071-6

[12]   A. Amtmann and D. Sanders, “Mechanisms of Na? Uptake by Plant Cells,” Advances in Botanical Research, Vol. 29, 1999, pp. 75-112. doi:10.1016/S0065-2296(08)60310-9

[13]   T.A. Cuin, A. Miller, S. Laurie and R. Leigh, “Potassium Activities in Cell Compartments of Salt-Grown Barley Leaves,” Journal of Experimental Botany, Vol. 54, No. 383, 2003, pp. 657-661. doi:10.1093/jxb/erg072

[14]   R. Munns, “Comparative Physiology of Salt and Water Stress,” Plant, Cell and Environment, Vol. 25, 2002, pp. 239-250. doi:10.1046/j.0016-8025.2001.00808.x

[15]   S. Agarie , T. Shimoda, Y. Shimizu, K. Baumann, H. Sunagawa, A. Kondo, et al., “Salt Tolerance, Salt Accumulation, and Ionic Homeostasis in an Epidermal BladderCell-Less Mutant of the Common Ice Plant Mesembryanthemum crystallinum,” Journal of Experimental Botany, Vol. 58, No. 8, 2007, pp. 1957-1967. doi:10.1093/jxb/erm057

[16]   J. Park, T. Okita and G. Edwards, “Salt Tolerant Mechanisms in Single-Cell C-4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae),” Plant Science, Vol. 176, No. 5, 2009, pp. 616-626. doi:10.1016/j.plantsci.2009.01.014

[17]   S. Mahajan and N. Tuteja, “Cold, Salinity and Drought Stresses: An Overview,” Archives of Biochemistry and Biophysics, Vol. 444, No. 2, 2005, pp. 139-158. doi:10.1016/

[18]   A. K. Parida and A. Das, “Salt Tolerance and Salinity Effects on Plants: A Review,” Ecotoxicology and Environmental Safety, Vol. 60, No. 3, 2005, pp. 324-349. doi:10.1016/j.ecoenv.2004.06.010

[19]   M. Tester and R. Davenport, “Na? Tolerance and Na? Transport in Higher Plants,” Annals of Botany, Vol. 91, 2003, pp. 503-527. doi:10.1093/aob/mcg058

[20]   G. Zhifang and W. H. Loescher, “Expression of a Celery Mannose-6-phosphate Reductase in Arabidopsis thaliana Enhances Salt Tolerance and Induces Biosynthesis of Both Mannitol and a Glucosyl-Mannitol Dimer,” Plant Cell and Environment, Vol. 26, No. 2, 2003, pp. 275-283. doi:10.1046/j.1365-3040.2003.00958.x

[21]   J. A. Raven, “Regulation of pH and Generation of Osmolarity in Vascular Plants: A Cost-Benefit Analysis in Relation to Efficiency of Use of Energy, Nitrogen and Water,” New Phytologist, Vol. 101, No. 1, 1985, pp. 25-77. doi:10.1111/j.1469-8137.1985.tb02816.x

[22]   R. Wilkinson, “Seasonal Development of Anatomical Structures of Saltcedar Foliage,” Botanical Gazette, Vol. 127, No. 4, 1966, pp. 231-234. doi:10.1086/336369

[23]   W. Berry, “Characterisitics of Salts Secreted by Tamarix aphylla,” American Journal of Botany, Vol. 57, No. 10, 1970, pp. 1226-1230. doi:10.2307/2441362

[24]   X. Ruan, Q. Wang, Y. Chen and W. Li, “Physiological Response of Riparian Plants to Watering in Hyper-Arid Areas of Tarim River, China,” Frontiers of Biology in China, Vol. 2, No. 1, 2007, pp. 54-61. doi:10.1007/s11515-007-0010-x

[25]   X. Ruan, Q. Wang, C. Pan, Y. Chen and H. Jian, “Physiological Acclimation Strategies of Riparian Plants to Environment Change in the Delta of the Tarim River, China,” Environmental Geology, Vol. 57, No. 8, 2009, pp. 1761-1773. doi:10.1007/s00254-008-1461-3

[26]   B. Cui, Q. Yang, K. Zhang, X. Zhao and Z. You, “Responses of Saltcedar (Tamarix chinensis) to Water Table Depth and Soil Salinity in the Yellow River Delta, China,” Plant Ecology, Vol. 209, No. 2, 2010, pp. 279-290. doi:10.1007/s11258-010-9723-z

[27]   A. Solomon, S. Beer, Y. Waisel, G. P. Jones and L. G. Paleg, “Effects of NaCl on the Carboxylating Activity of Rubisco from Tamarix jordanis in the Presence and Absence of Proline-Related Compatible Solutes,” Physiologia Plantarum, Vol. 90, No. 1, 1994, pp. 198-204. doi:10.1111/j.1399-3054.1994.tb02211.x

[28]   L. S. Bates, R. P. Waldren and I. D. Teare, “Rapid Determination of Free Proline for Water-Stress Studies,” Plant and Soil, Vol. 39, No. 1, 1972, pp. 205-207. doi:10.1007/BF00018060

[29]   S. K. Arndt, C. Arampatsis, A. Foetzki, X. Li, F. Zeng and X. Zhang, “Contrasting Patterns of Leaf Solute Accumulation and Salt Adaptation in Four Phreatophytic Desert Plants in a Hyperarid Desert with Saline Groundwater,” Journal of Arid Environments, Vol. 59, No. 2, 2004, pp. 259-270. doi:10.1016/j.jaridenv.2004.01.017

[30]   C. G. Ladenburger, A. L. Hild, D. J. Kazmer and L. C. Munn, “Soil Salinity in Tamarix Invasions in the Bighorn Basin, Wyoming, USA,” Journal of Arid Environments, Vol. 65, No. 1, 2006, pp. 111-128. doi:10.1016/j.jaridenv.2005.07.004

[31]   P. B. Shafroth, J. M. Friedman and L. S. Ischinger, “Effects of Salinity on Establishment of Populus fremontii (cottonwood) and Tamarix ramosissima (Saltcedar) in Southwestern United States,” Great Basin Naturalist, Vol. 55, No. 1, 1995, pp. 58-65.

[32]   M. W. Vandersande, E. P. Glenn and J. L. Walworth, “Tolerance of Five Riparian Plants from the Lower Colorado River to Salinity Drought and Inundation,” Journal of Arid Environments, Vol. 49, No. 1, 2001, pp. 147-159. doi:10.1006/jare.2001.0839

[33]   M. A. Khan, I. A. Ungar and A. M. Showalter, “Effects of Sodium Chloride Treatments on Growth and Ion Accumulation of the Halophyte Haloxylon recurvum,” Communications in Soil Science and Plant Analysis, Vol. 31, No. 17-18, 2000, pp. 2763-2774. doi:10.1080/00103620009370625

[34]   L. Leport, J. Baudry, A. Radureau and A. Bouchereau, “Sodium, Potassium and Nitrogenous Osmolyte Accumulation in Relation to the Adaptation to Salinity of Elytrigia pycnantha, an Invasive Plant of the Mont SaintMichel Bay,” Les Cashiers de Biologie Marine, Vol. 47, No. 1, 2006, pp. 31-37.

[35]   Y. Huang, Z. Bie, Z. Liu, A. Zhen and W. Wang, “Protective Role of Proline against Salt Stress is Partially Related to the Improvement of Water Status and Peroxidase Enzyme Activity in Cucumber,” Soil Science and Plant Nutrition, Vol. 55, No. 5, 2009, pp. 698-704. doi:10.1111/j.1747-0765.2009.00412.x

[36]   A. R. Yeo, S. M. Capron and T. J. Flowers, “The Effect of Salinity upon Photosynthesis in Rice (Oryza sativa L.): Gas Exchange by Individual Leaves Relation to Their Salt Content,” Journal of Experimental Botany, Vol. 36, No. 8, 1985, pp. 1240-1248. doi:10.1093/jxb/36.8.1240

[37]   B. W. Touchette, K. L. Rhodes, G. A. Smith and M. Poole, “Salt Spray Induces Osmotic Adjustment and Tissue Rigidity in Smooth Cordgrass, Spartina alterniflora (Loisel.),” Estuaries and Coasts, Vol. 32, No. 5, 2009, pp. 917-925. doi:10.1007/s12237-009-9178-4

[38]   B. W. Touchette, G. A. Smith, K. L. Rhodes and M. Poole, “Tolerance and Avoidance: Two Contrasting Physiological Responses to Salt Stress in Mature Marsh Halophyte Juncus roemerianus Scheele and Spartina alterniflora Loisel.,” Journal of Experimental Marine Biology and Ecology, Vol. 380, No. 1-2, 2009, pp. 106-112. doi:10.1016/j.jembe.2009.08.015

[39]   I. Slama, T. Ghnaya, K. Hessini, D. Messedi, A. Savouré and C. Abdelly, “Comparative Study of the Effects of Mannitol and PEG Osmotic Stress on Growth and Solute Accumulation in Sesuvium portulacastrum,” Environmental and Experimental Botany, Vol. 61, No. 1, 2007, pp. 10-17. doi:10.1016/j.envexpbot.2007.02.004

[40]   S. Bhaskaran, R. H. Smith and R. J. Newton, “Physiological Changes in Cultured Sorghum Cells in Response to Induced Water Stress. I. Free Proline,” Plant Physiology, Vol. 79, No. 1, 1985, pp. 266-269. doi:10.1104/pp.79.1.266

[41]   T. N. Singh, D. Aspinall and L. G. Paleg, “Proline Accumulation and Varietal Adaptability to Drought in Barley: A Potential Metabolic Measure of Drought Resistance,” Nature-New Biology, Vol. 236, No. 67, 1972, pp. 188-190.

[42]   E. Glenn, R. Lee, C. Felger and S. Zengel, “Effects of Water Management on the Wetlands of the Colorado River Delta, Mexico,” Journal of Arid Environments, Vol. 10, No. 4, 1996, pp. 281-294.

[43]   J. S. Boyer, “Effects of Osmotic Water Stress on Metabolic Rates of Cotton Plants with Open Stomata,” Plant Physiology, Vol. 40, No. 2, 1965, pp. 229-234. doi:10.1104/pp.40.2.229

[44]   M. R. Kaufmann, “Evaluations of Season, Temperature, and Water Stress Effects on Stomata Using a Leaf Conductance Model,” Plant Physiology, Vol. 69, No. 5, 1982, pp. 1023-1026. doi:10.1104/pp.69.5.1023

[45]   T. E. Dawson, S. Mambelli, A. H. Plamboeck, P. H. Templer and K. P. Tu, “Stable Isotopes in Plant Ecology,” Annual Review of Ecology, Evolution, and Systematics, Vol. 33, No. 1, 2002, pp. 507-559. doi:10.1146/annurev.ecolsys.33.020602.095451

[46]   D. Busch and S. Smith, “Mechanisms Associated with The Decline of Woody Species in Riparian Ecosystems of the Southwestern U.S.,” Ecological Monographs, Vol. 65, 1995, pp. 347-370. doi:10.2307/2937064

[47]   J. M. Carter and J. B. Nippert, “Leaf-Level Physiological Response of Tamarix ramosissima to Increasing Salinity,” Journal of Arid Environments, in press.

[48]   P. Nagler, E. Glenn and T. L. Thompson, “Comparison of Transpiration of Cottonwood, Willow and Saltcedar Trees Measured by Sap Flow and Canopy Temperature Methods,” Agricultural and Forest Metereology, Vol. 116, No. 1-2, 2003, pp. 73-89. doi:10.1016/S0168-1923(02)00251-4