Stomatal Abundance and Distribution in Prosopis strombulifera Plants Growing under Different Iso-Osmotic Salt Treatments

Abstract

Changes in several environmental parameters are thought to affect stomatal development. Under salt stress, plants can regulate their transpiration flux through a better control of the stomatal opening (as a short-term response) and through modifications of leaf anatomy (as a long-term response). We investigate how leaf micromorphology (stomatal abundance and distribution) of the halophyte Prosopis strombulifera (a spiny shrub particularly abundant in high-salinity areas of central Argentina) responds to different water status when plants are subjected to different salt treatments (NaCl, Na2SO4 and their iso-osmotic mixture). Different salt treatments on P. strombulifera plants influenced leaf micromorphological traits differently. In this study, Na2SO4-treated plants showed an increase in stomatal density (SD) and epidermal cell density (ECD) (with smaller stomata) at moderate and high salinity (-1.9 and -2.6 MPa), whereas in NaCl and NaCl + Na2SO4 treated plants, a decrease in these variables was observed. In Na2SO4-treated plants, transpiration was the highest at moderate and high salinity, with the highest content of ABA registered. A possible explanation is that, despite of these high ABA levels, there is no inhibition in stomatal opening, resulting in increased water loss, growth inhibition, and acceleration of senescence processes. We demonstrate that P. strombulifera responds to progressive salt stress by different salts changing the leaf development, particularly in Na2SO4-treated plants, leading to structural modifications in leaf size and micro-morphology of leaf cells.

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M. Reginato, H. Reinoso, A. Llanes and M. Luna, "Stomatal Abundance and Distribution in Prosopis strombulifera Plants Growing under Different Iso-Osmotic Salt Treatments," American Journal of Plant Sciences, Vol. 4 No. 12C, 2013, pp. 80-90. doi: 10.4236/ajps.2013.412A3010.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] “FAO Land and Plant Nutrition Management Service,” 2008. http://www.fao.org/ag/agl/agll/spush/
[2] A. Burkart, “A Monograph of the Genus Prosopis (Leguminosae subfam Mimosoideae), Catalogue of the Recognized Species of Prosopis,” Journal of the Arnold Arboretum, Vol. 57, No. 4, 1876, pp. 450-525.
[3] N. M. Pasiecznik, P. Felker, P. J. Harris, L. Harsh, G. Cruz, J. C. Tewari, K. Cadoret and L. J. Maldonado, “The Prosopis juliflora-Prosopis pallida Complex: A Monograph,” HDRA, Coventry, 2001, p. 172.
[4] D. Rhodes and P. Felker, “Mass Screening Prosopis (Mesquite) Seedlings for Growth at Seawater Salinity,” Forest Ecological Management, Vol. 24, 1987, pp. 169-176.
http://dx.doi.org/10.1016/0378-1127(88)90041-2
[5] L. Sosa, A. Llanes, H. Reinoso, M. Reginato and V. Luna, “Osmotic and Specific Ion Effects on the Germination of Prosopis strombulifera,” Annals of Botany, Vol. 96, No. 2, 2004, pp. 261-267. http://dx.doi.org/10.1093/aob/mci173
[6] H. R. Manchanda and S. K. Sharma, “Tolerance of Chloride and Sulphate Salinity in Chickpea (Cicer arietinum),” The Journal of Agricultural Science, Vol. 113, No. 3, 1989, pp. 407-410.
http://dx.doi.org/10.1017/S0021859600070131
[7] R. M. Iqbal, “Leaf Area and Ion Contents of Wheat Grown under NaCl and Na2SO4 Salinity,” Pakistan Journal of Biological Sciences, Vol. 6, 2003, pp. 1512-1514.
http://dx.doi.org/10.3923/pjbs.2003.1512.1514
[8] D. Shi and Y. Sheng, “Effect of Various Salt-Alkaline Mixed Stress Conditions on Sunflower Seedlings and Analysis of Their Stress Factors,” Environmental and Experimental Botany, Vol. 54, No. 1, 2005, pp. 8-21.
http://dx.doi.org/10.1016/j.envexpbot.2004.05.003
[9] P. Manivannan, C. Abdul Jaleel, B. Sankar, A. Kishore Kumar, P. V. Murali, R. Somasundaram and R. Panneerselvam, “Mineral Uptake and Biochemical Changes in Helianthus annuus under Treatment with Different Sodium Salts,” Colloids and Surfaces Biointerfaces, Vol. 62, No. 1, 2008, pp. 58-63.
http://dx.doi.org/10.1016/j.colsurfb.2007.09.019
[10] H. Reinoso, L. Sosa, L. Ramirez and V. Luna, “Salt-Induced Changes in the Vegetative Anatomy of Prosopis strombulifera (Leguminosae),” Canadian Journal of Botany, Vol. 82, No. 5, 2004, pp. 618-628.
http://dx.doi.org/10.1139/b04-040
[11] M. Reginato, L. Sosa, A. Llanes, E. Hampp, N. Vettorazzi, H. Reinoso and V. Luna, “Na2SO4 and NaCl Determine Different Growth Responses and Ion Accumulation in the Halophytic Legume Prosopis strombulifera,” Plant Biology, 2013. http://dx.doi.org/10.1111/plb.12001
[12] H. Reinoso, L. Sosa, M. Reginato and V. Luna, “Histological Alterations Induced by Sodium Sulfate in the Vegetative Anatomy of Prosopis strombulifera (Lam.) Benth,” World Journal of Agricultural Sciences, Vol. 1, No. 2, 2005, pp. 109-119.
[13] A. Maggio, G. Raimondi, A. Martino and S. De Pascale, “Salt Stress Response in Tomato beyond the Salinity Tolerance Threshold,” Environmental and Experimental Botany, Vol. 59, 2007, pp. 276-282.
http://dx.doi.org/10.1016/j.envexpbot.2006.02.002
[14] C. Y. Yoo, H. E. Pence, P. M. Hasegawa and M. V. Mickelbart, “Regulation of Transpiration to Improve Crop Water Use,” Critical Reviews in Plant Science, Vol. 28, No. 6, 2009, pp. 410-431.
http://dx.doi.org/10.1080/07352680903173175
[15] T. N. Buckley, “The Control of Stomata by Water Balance,” New Phytologist, Vol. 168, No. 2, 2005, pp. 275-292.
http://dx.doi.org/10.1111/j.1469-8137.2005.01543.x
[16] K. J. McCree and S. D. Davis, “Effect of Water Stress and Temperature on Leaf Size and Number of Epidermal Cells in Grain Sorghum,” Crop Science, Vol. 14, 1974, pp. 751-755.
http://dx.doi.org/10.2135/cropsci1974.0011183X001400050041x
[17] J. M. Cutler, D. W. Rains and R. S. Loomis, “The Importance of Cell Size in the Water Relations of Plants,” Physiologia Plantarum, Vol. 40, No. 4, 1977, pp. 225-260.
http://dx.doi.org/10.1111/j.1399-3054.1977.tb04068.x
[18] H. M. Yang and G. X. Wang, “Leaf Stomatal Densities and Distribution in Triticum aestivum under Drought and CO2 Enrichment,” Acta Phytoecologica Sinica, Vol. 25, 2001, pp. 312-316.
[19] Y. P. Zhang, Z. M. Wang, Y. C. Wu and X. Zhang, “Stomatal Characteristics of Different Green Organs in Wheat under Different Irrigation Regimes,” Acta Agronomica Sinica, Vol. 32, No. 1, 2006, pp. 70-75.
[20] S. A. Quarrie and H. G. Jones, “Effects of Abscistic Acid and Water Stress on Development and Morphology of Wheat,” Journal of Experimental Botany, Vol. 28, 1977, pp. 192-203. http://dx.doi.org/10.1093/jxb/28.1.192
[21] R. D. Spence, H. Wu, P. J. Sharpe and K. Clark, “Water Stress Effects on Guard Cell Anatomy and the Mechanical Advantage of the Epidermal Cells,” Plant, Cell and Environment, Vol. 9, 1986, pp. 197-202.
[22] J. P. Martinez, H. Silva, J. F. Ledent and M. Pinto, “Effect of Drought Stress on the Osmotic Adjustment, Cell Wall Elasticity and Cell Volume of Six Cultivars of Common Beans (Phaseolus vulgaris L.),” European Journal of Agronomy, Vol. 26, 2007, pp. 30-38.
http://dx.doi.org/10.1016/j.eja.2006.08.003
[23] D. Delgado, C. Alonso-Blanco, C. Fenoll and M. Mena, “Natural Variation in Stomatal Abundance of Arabidopsis Thaliana Includes Cryptic Diversity for Different Developmental Processes,” Annals of Botany, 2011.
http://dx.doi.org/10.1093/aob/mcr060
[24] M. Geisler, M. Yang and F. D. Sack, “Divergent Regulation of Stomatal Initiation and Patterning in Organ and Suborgan Regions of the Arabidopsis Mutants Too Many Mouths and Four Lips,” Planta, Vol. 205, 1998, pp. 522-530. http://dx.doi.org/10.1007/s004250050351
[25] M. Geisler and F. D. Sack, “Variable Timing of Developmental Progression in the Stomatal Pathway in Arabidopsis Cotyledons,” New Phytologist, Vol. 153, 2002, pp. 469-476.
http://dx.doi.org/10.1046/j.0028-646X.2001.00332.x
[26] M. Carosio, M. Junqueras, A. Endersen, M. Fernandez Belmonte, E. Martinez Carretero and A. Dalmasso, “Flora de las Salinas del Bebedero,” Sociedad de Biología de Cuyo, Argentina, 2009.
[27] L. Sosa, “Adaptaciones Fisiológicas de Prosopis strombulifera a Condiciones de Salinidad por Cloruros y Sulfatos,” Ph.D. Thesis, Universidad Nacional de Río Cuarto, Córdoba, 2005.
[28] C. Peña Zubiate, D. Anderson, M. Demmi, J. Saenz and A. D’Hiriart, “Carta de Suelos y Vegetación de la Provincia de San Luis,” Secretaria de Agricultura, Ganadería, Pesca y Alimentación, INTA, Estación Experimental Agropecuaria, San Luis, 1998.
[29] D. Ambrogio and A. Argüeso, “A. Manual de Técnicas en Histología Vegetal,” Hemisferio Sur, Buenos Aires, 1986.
[30] F. I. Woodward, “Stomatal Numbers Are Sensitive to Increases in CO2 from Preindustrial Levels,” Nature, Vol. 327, 1987, pp. 617-618.
http://dx.doi.org/10.1038/327617a0
[31] J. Burguess, “An Improved Photometer,” School Science Review, Vol. 64, 1983, pp. 699-701.
[32] D. García Vargas, “Efectos Fisiológicos y Compartimentación Radicular en Plantas de Zea mays L. Expuestas a la Toxicidad por Plomo,” Ph.D. Thesis, Universidad Autónoma de Barcelona, España, 2006.
[33] “Infostat Student, Version 2011,” Universidad Nacional de Córdoba, Córdoba, 2011.
[34] S. Q. Ouyang, Y. F. Liu, P. Liu, G. Lei, S. J. He and B. Ma, “Receptor-Like Kinase OsSIK1 Improves Drought and Salt Stress Tolerance in Rice (Oryza sativa) Plants,” The Plant Journal, Vol. 62, 2010, pp. 316–329.
http://dx.doi.org/10.1111/j.1365-313X.2010.04146.x
[35] D. C. Bergmann and F. D. Sack, “Stomatal Development,” Annual Review of Plant Biology, Vol. 58, 2007, pp. 163-181.
http://dx.doi.org/10.1146/annurev.arplant.58.032806.104023
[36] S. A. Casson and A. M. Hetherington, “Environmental Regulation of Stomatal Development,” Current Opinion in Plant Biology, Vol. 13, No. 1, 2010, pp. 90-95.
http://dx.doi.org/10.1016/j.pbi.2009.08.005
[37] E. Flores-Vindas, “La Planta: Estructura y Función,” Libro Universitario Regional (LUR), Vol. 1, 1999, Costa Rica.
[38] S. Driscoll, A. Prins, E. Olmos, K. Kunert and C. Foyer, “Specification of Adaxial and Abaxial Stomata, Structure and Photosynthesis to CO2 Enrichment Maize Leaves,” Journal of Experimental Botany, Vol. 57, No. 2, 2006, pp. 381-390. http://dx.doi.org/10.1093/jxb/erj030
[39] K. Aasamaa, A. Sober and M. Rahi, “Leaf Anatomical Characteristics Associated with Shoot Hydraulic Conductance, Stomatal Conductance and Stomatal Sensitivity to Changes of Leaf Water Status in Temperate Deciduous Trees,” Australian Journal of Plant Physiology, Vol. 28, No. 8, 2001, pp. 765-774.
[40] D. W. Pearce, S. Millard, D. F. Bray and S. B. Rood, “Stomatal Characteristics of Riparian Poplar Species in a Semi-Arid Environment,” Tree Physiology, Vol. 26, No. 2, 2006, pp. 211-218.
http://dx.doi.org/10.1093/treephys/26.2.211
[41] W. Beyschlag and J. Eckstein, “Towards a Causal Analysis of Stomatal Patchiness. The Role of Stomatal Size Variability and Hydrological Heterogeneity,” Acta Oecologica, Vol. 22, No. 3, 2001, pp. 161-173.
http://dx.doi.org/10.1016/S1146-609X(01)01110-9
[42] G. Inan, Q. Zhang, P. Li, Z. Wang, Z. Cao, H. Zhang, C. Zhang, T. Quist, S. Goodwin, J. Zhu, H. Shi, B. Damsz, T. Charbaji, Q. Gong, S. Ma, M. Fredricksen, D. Galbraith, M. Jenks, D. Rhodes, P. Hasegawa, H. Bohnert, R. Joly, R. Bressan and J. K. Zhu, “Salt Cress. A Halophyte and Cryophyte Arabidopsis Relative Model System and Its Applicability to Molecular Genetic Analyses of Growth and Development of Extremophiles,” Plant Physiology, Vol. 135, No. 3, 2004, pp. 1718-1737.
http://dx.doi.org/10.1104/pp.104.041723
[43] A. Llanes, G. Bertazza, G. Palacio and V. Luna, “Different Sodium Salts Cause Different Solute Accumulation in the Halophyte Prosopis stombulifera,” Plant Biology, Vol. 15, Suppl. s1, 2012, pp. 118-125.
http://dx.doi.org/10.1111/j.1438-8677.2012.00626.x
[44] R. Munns, “Comparative Physiology of Salt and Water Stress,” Plant, Cell and Environment, Vol. 25, No. 2, 2002, pp. 239-250.
http://dx.doi.org/10.1046/j.0016-8025.2001.00808.x
[45] C. Lovelock and M. Ball, “Influence of Salinity on Photosynthesis of Halophytes,” In: A. Läuchli and U. Lüttge, Eds., Salinity: Environment-Plants-Molecules, Kluwer Academic Publishers, Dordrecht, 2002, pp. 315-339.
[46] A. Llanes, O. Masciarelli, R. Ordoñez, M. I. and V. Luna, “Differential Growth Responses to Sodium Salts Involve Different ABA Catabolism and Transport in the Halophyte Prosopis strombulifera,” Biologia Plantarum, 2013.
http://dx.doi.org/10.1007/s10535-013-0365-6
[47] L. Earns, J. Goodger, S. Alvarez, E. Marsh, B. Berla, E. Lockhart, J. Jung, P. Li, H. Bohnert and D. Schachtman, “Sulphate as a Xylem-Borne Chemical Signal Precedes the Expression of ABA Biosynthetic Genes in Maize Roots,” Journal of Experimental Botany, Vol. 61, No. 12, 2012, pp. 3395-3405.
[48] G. Karimi, M. Ghorbanli, H. Heidari, R. A. Nejad and M. H. Assareh, “The Effects of NaCl on Growth, Water Relations, Osmolytes and Ion Content in Kochia prostrate,” Biologia Plantarum, Vol. 49, No. 2, 2005, pp. 301-304.
http://dx.doi.org/10.1007/s10535-005-1304-y
[49] T. J. Flowers, “Physiology of Halophytes,” Plant and Soil Vol. 89, No. 1-3, 1985, pp. 41-56.
http://dx.doi.org/10.1007/BF02182232
[50] P. R. Kemp and G. L. Cunningham, “Light, Temperature and Salinity Effects on Growth, Leaf Anatomy and Photosynthesis of Distichlis spicata (L) Greene,” American Journal of Botany, Vol. 68, No. 4, 1981, pp. 507-516.
http://dx.doi.org/10.2307/2443026
[51] F. Boughalleb, M. Denden and B. Ben Tiba, “Photosystem II Photochemistry and Physiological Parameters of Three Fodder Shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea under Salt Stress,” Acta Physiologiae Plantarum, Vol. 31, No. 3, 2009, pp. 463-476.
http://dx.doi.org/10.1007/s11738-008-0254-3
[52] N. Naz, M. Hameed, M. Ashraf, F. Al-Qurainy and M. Arshad, “Relationships between Gas-Exchange Characteristics and Stomatal Structural Modifications in Some Desert Grasses under High Salinity,” Photosynthetica, Vol. 48, No. 3, 2010, pp. 446-456.
http://dx.doi.org/10.1007/s11099-010-0059-7
[53] C. Botti, D. Palzkill, D. Munoz and L. Prat, “Morphological and Anatomical Characterization of Six Jojoba Clones at Saline and Non-Saline Sites,” Industrial Crops and Products, Vol. 9, No. 1, 1998, pp. 53-62.
http://dx.doi.org/10.1016/S0926-6690(98)00014-4
[54] Y. Hwang and S. Chen, “Anatomical Responses in Kandelia candel (L.) Druce Seedlings Growing in the Presence of Different Concentrations of NaCl,” Botanical Bulletin of Academia Sinica, Vol. 36, No. 3, 1995, pp. 181-188.
[55] S. Shabala, “Learning from Halophytes: Physiological Basis and Strategies to Improve Abiotic Stress Tolerance in Crops,” Annals of Botany, Vol. 112, No. 7, 2013, pp. 1209-1221. http://dx.doi.org/10.1093/aob/mct205
[56] L. Shabala, A. Mackay, Y. Tian, S. E. Jacobsen, D. W. Zhou and S. Shabala, “Oxidative Stress Protection and Stomatal Patterning as Components of Salinity Tolerance Mechanism in Quinoa (Chenopodium quinoa),” Physiologia Plantarum, Vol. 146, No. 1, 2012, pp. 26-38.
http://dx.doi.org/10.1111/j.1399-3054.2012.01599.x
[57] V. I. Adolf, S. Shabala, M. N. Andersen, F. Razzaghi and S. E. Jacobsen, “Varietal Differences of Quinoa’s Tolerance to Saline Conditions,” Plant and Soil, Vol. 357, No. 1-2, 2012, pp. 117-129.
http://dx.doi.org/10.1007/s11104-012-1133-7
[58] G. Barbieri, S. Vallone, F. Orsini, R. Paradiso, S. De Pascale, F. Negre-Zakharov and A. Maggio, “Stomatal Density and Metabolic Determinants Mediate Salt Stress Adaptation and Water Use Efficiency in Basil (Ocimum basilicum L.),” Journal of Plant Physiology, Vol. 169, No. 17, 2012, pp. 1737-1746.
http://dx.doi.org/10.1016/j.jplph.2012.07.001
[59] L. J. De Kok, A. Castro, M. Durenkamp, A. Koralewska, F. S. Posthumus, C. E. Stuiver, L. Yang and I. Stulen, “Pathways of Plant Sulfur Uptake and Metabolism—An Overview,” Landbauforschung Völkenrode, Special Issue, Vol. 283, 2005, pp. 5-13.
[60] A. Schmidt, “Metabolic Background of H2S Release from Plants,” Landbauforschung Völkenrode, Special Issue, Vol. 283, 2005, pp. 121-129.

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