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Anatomical changes induced by increasing NaCl salinity in three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea

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Abstract

Nitraria retusa and Atriplex halimus (xero-halophytes) plants were grown in the range 0–800 mM NaCl while Medicago arborea (glycophyte) in 0–300 mM NaCl. Plants were harvested after 120 days of salt-treatment. The present study was designed to study the effect of salinity on root, stem and leaf anatomy, water relationship, and plant growth in greenhouse conditions. Salinity induced anatomical changes in the roots, stems and leaves. The cuticle and epidermis of N. retusa and A. halimus stems were unaffected by salinity. However, root anatomical parameters (root cross section area, cortex thickness and stele to root area ratio), and stem anatomical parameters (stem cross section area and cortex area) were promoted at 100–200 mM NaCl. Indicating that low to moderate salinity had a stimulating effect on root and stem growth of these xero-halophytic species. At higher salinities, root and stem structures were altered significantly, and their percentages of reduction were higher in A. halimus than in N. retusa whereas, in M. arborea, they were strongly altered as salinity rose. NaCl (100–300 mM) reduced leaf water content by 21.2–56.2% and specific leaf area by 51–88.1%, while increased leaf anatomical parameters in M. arborea (e.g. increased thickness of upper and lower epidermis, palisade and spongy mesophyll, entire lamina, and increased palisade to spongy mesophyll ratio). Similar results were evidenced in A. halimus leaves with salinity exceeding 100 mM NaCl. Leaves of N. retusa were thinner in salt-stressed plants while epidermis thickness and water content was unaffected by salinity. The size of xylem vessel was unchanged under salinity in the leaf’s main vein of the three species while we have increased number in M. arborea leaf main vein in the range of 200–300 mM NaCl. A longer distance between leaf vascular bundle, a reduced size and increased number of xylem vessel especially in stem than in root vascular system was evidenced in M. arborea treated plants and only at (400–800 mM) in the xero-halophytic species. The effects of NaCl toxicity on leaf, stem and root ultrastructure are discussed in relation to the degree of salt resistance of these three species. Our results suggest that both N. retusa and A. halimus show high tolerance to salinity while M. arborea was considered as a salt tolerant species.

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References

  • Abdelly C, Zid E, Hajji M, Grignon C (1995) Biomass production and nutrition of Medicago species associated to halophytes on the edge of a sebkha in Tunisia. In: Chouk-Allah, Hamdy, Malcolm (eds) Halophytes and Biosaline Agriculture. Dekker Inc, New York, pp 313–324

  • Alegre J, Navarrete L, Ceresuela JL, Hornero J (1991) La alfalfa leñosa de Creta (Medicago strasseri, Matthäs. Greuter y Risse) primeros datos acerca de su potencial interés forrajero, XXXI Reunión Científica de la Sociedad Española para el Estudio de los Pastos, Murcia, pp 76–80

  • Bajji M, Kinet JM, Lutts S (1998) Salt stress effects on roots and leaves of Atriplex halimus L. and their corresponding callus cultures. Plant Sci 137:131–142. doi:10.1016/S0168-9452(98)00116-2

    Article  CAS  Google Scholar 

  • Barhoumi Z, Djebali W, Chaïbi W, Abdelly C, Smaoui A (2007) Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. J Plant Res 120:529–537. doi:10.1007/s10265-007-0094-z

    Article  PubMed  CAS  Google Scholar 

  • Bongi G, Loreto F (1989) Gas-exchange properties of salt-stressed olive (Olea europea L.) leaves. Plant Physiol 90:1408–1416. doi:10.1104/pp.90.4.1408

    Article  PubMed  CAS  Google Scholar 

  • Çavuşoğlu K, Kılıç S, Kabar K (2007) Some morphological and anatomical observations during alleviation of salinity (NaCl) stress on seed germination and seedling growth of barley by polyamines. Acta Physiol Plant 29:551–557. doi:10.1007/s11738-007-0066-x

    Article  Google Scholar 

  • Çavuşoğlu K, Kılıç S, Kabar K (2008) Effects of some plant growth regulators on leaf anatomy of radish seedlings grown under saline conditions. J Appl Biol Sci 2:47–50

    Google Scholar 

  • Choat B, Ball MC, Luly JG, Holtum JAM (2005) Hydraulic architecture of deciduous and evergreen dry forest tree species from north-eastern Australia. Trees (Berl) 19:305–311. doi:10.1007/s00468-004-0392-1

    Article  Google Scholar 

  • Colmer TD, Epstein E, Dvorak J (1995) Differential solute regulation in leaf blades of various ages in salt-sensitive wheat and a salt-tolerant wheat X Lophopyrum elongatum (Host) A. Love Amphiploid. Plant Physiol 108:1715–1724

    PubMed  CAS  Google Scholar 

  • Curtis PS, Lauchli A (1987) The effect of moderate salt stress on leaf anatomy in Hibiscus cannabinus (Kenaf) and its relation to leaf area. Am J Bot 74:538–542. doi:10.2307/2443833

    Article  CAS  Google Scholar 

  • De Araújo SAM, Silveiral JAG, Almeidal TD, Rochal IMA, Morais DL, Viégas RA (2006) Salinity tolerance of halophyte Atriplex nummularia L. grown under increasing NaCl levels. R Bras Eng Agríc Ambiental 10:848–854

    Google Scholar 

  • Debez A, Hamed KB, Grignon C, Abdelly C (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant Soil 262:179–189. doi:10.1023/B:PLSO.0000037034.47247.67

    Article  CAS  Google Scholar 

  • Debez A, Saadaoui D, Ramanib B, Ouerghi Z, Koyro HW, Huchzermeyer B, Abdelly C (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 57:285–295. doi:10.1016/j.envexpbot.2005.06.009

    Article  CAS  Google Scholar 

  • Dengler NG, Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 133–172

    Chapter  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190. doi:10.1146/annurev.pp.31.060180.001053

    Article  CAS  Google Scholar 

  • Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701

    PubMed  Google Scholar 

  • Hajibagheri MA, Yeo AR, Flowers TJ (1985) Salt tolerance in Suaeda maritima (L.) Dum.: fine structure and ion concentrations in the apical region of roots. New Phytol 99:331–343. doi:10.1111/j.1469-8137.1985.tb03661.x

    Article  Google Scholar 

  • Heneidy SZ (1996) Palatability and nutritive value of some common plant species from the Aqaba Gulf area of Sinai, Egypt. J Arid Environ 34:115–123. doi:10.1006/jare.1996.0097

    Article  Google Scholar 

  • Hoagland DR, Amon DI (1950) The water culture method for growing plants without soil. In: Circular No. 347, University of Calif. Agric. Exp. Stn, Berkeley, Canada, pp 1–39

  • Hu Y, Schmidhalter U (2001) Reduced cellular cross-sectional area in the leaf elongation zone of wheat causes a decrease in dry weight deposition under saline conditions. J Plant Physiol 28:165–170

    Google Scholar 

  • Hu Y, Fromm J, Schmidhalter U (2005) Effect of salinity on tissue architecture in expanding wheat leaves. Planta 220:838–848. doi:10.1007/s00425-004-1401-8

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Redmann RE (1995) Responses of growth, morphology, and anatomy to salinity and calcium supply in cultivated and wild barley. Can J Bot 73:1859–1866. doi:10.1139/b95-198

    Article  CAS  Google Scholar 

  • Hwang YH, Chen SC (1995) Anatomical responses in Kandelia candel (L.) druce seedlings growing in the presence of different concentrations of NaCI. Bot Bull Acad Sin 36:181–188

    CAS  Google Scholar 

  • Isla R, Agragues R, Royo A (1998) Validity of various physiological traits as screening criteria for salt tolerance in barley. Field Crops Res 58:97–107. doi:10.1016/S0378-4290(98)00088-4

    Article  Google Scholar 

  • Joly RJ (1989) Effect of sodium chloride on the hydraulic conductivity of soybean root system. Plant Physiol 91:1262–1265. doi:10.1104/pp.91.4.1262

    Article  PubMed  CAS  Google Scholar 

  • Kiliç S, Çavuşoğlu K, Kabar K (2007) Effects of 24-epibrassinolide on salinity stress induced inhibition of seed germination, seedling growth and leaf anatomy of barley. Suleyman Demirel Univ Fac Arts Sci J Sci 2:41–52

    Google Scholar 

  • Klee HJ, Estelle M (1991) Molecular genetic approaches to plant hormone biology. Annu Rev Plant Physiol Mol Biol 42:529–551. doi:10.1146/annurev.pp.42.060191.002525

    Article  CAS  Google Scholar 

  • Lauchli A, Epstein E (1990) Plant responses to saline and sodic conditions. In: Tanji KK (ed) Agricultural salinity assessment and management. ASCE manuals and reports on engineering practice No. 71. Soc Civil Eng, New York, pp 113–137

    Google Scholar 

  • Le Houerou HN (2000) Utilization of fodder trees and shrubs in the arid and semiarid zones of west Asia and North Africa. Arid Soil Res Rehabil 14:101–135. doi:10.1080/089030600263058

    Article  Google Scholar 

  • Lev-Yadun S, Aloni R (1995) Differentiation of the ray system in woody plants. Bot Rev 61:45–84. doi:10.1007/BF02897151

    Article  Google Scholar 

  • Longstreth DJ, Nobel PS (1979) Salinity effects on leaf anatomy. Plant Physiol 63:700–703. doi:10.1104/pp.63.4.700

    Article  PubMed  Google Scholar 

  • Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of the mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443. doi:10.1104/pp.98.4.1437

    Article  PubMed  Google Scholar 

  • Medina E, Francisco M (1997) Osmolality and delta-13C of leaf tissue of mangrove species from environments of contrasting rainfall and salinity. Estuar Coast Shelf Sci 45:337–344. doi:10.1006/ecss.1996.0188

    Article  CAS  Google Scholar 

  • Moghaieb REA, Saneoka H, Fujita K (2004) Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritime. Plant Sci 166:1345–1349. doi:10.1016/j.plantsci.2004.01.016

    Article  CAS  Google Scholar 

  • Mozafar A, Goodin JR (1970) Vesiculated hairs: a mechanism for salt tolerance in Atriplex halimus L. Plant Physiol 45:62–65. doi:10.1104/pp.45.1.62

    Article  PubMed  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. doi:10.1046/j.0016-8025.2001.00808.x

    Article  PubMed  CAS  Google Scholar 

  • Osmond CB, Bjorkman O, Anderson DJ (eds) (1980) Physiological processes in plant ecology. Springer, Berlin

    Google Scholar 

  • Popp M (1995) Salt resistance in herbaceous halophytes and mangroves. In: Behnke HD, Luttge U, Esser K, Kadereit JW, Runge M (eds) Progress in botany. Springer, Berlin, pp 416–429

    Google Scholar 

  • Rabhi M, Barhoumi Z, Ksouri R, Abdelly C, Gharsalli M (2007) Interactive effects of salinity and iron deficiency in Medicago ciliaris. C R Biol 330:779–788. doi:10.1016/j.crvi.2007.08.007

    Article  PubMed  CAS  Google Scholar 

  • Reinoso H, Sosa L, Ramírez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628. doi:10.1139/b04-040

    Article  Google Scholar 

  • Reinoso H, Sosa L, Reginato M, Luna V (2005) Histological alterations induced by sodium sulfate in the vegetative anatomy of Prosopis strombulifera (Lam.) Benth. World J Agric Sci 1:109–119

    Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370. doi:10.1111/j.1469-8137.2004.00974.x

    Article  CAS  Google Scholar 

  • Serrato Valenti G, Ferro M, Ferraro D, Riveros F (1991) Anatomical changes in Prosopis tamarugo Phil. seedlings growing at different levels of NaCl salinity. Ann Bot (Lond) 68:47–53

    Google Scholar 

  • Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:76–119

    Google Scholar 

  • Shannon MC, Grieve CM, François LE (1994) whole plant response to salinity In: Wilkinson RE, Dekker M (eds) Plant environment interaction, New York, pp 199–244

  • Shennan C, Hunt R, Macrobbie EAC (1987) Salt tolerance in Aster tripolium L. I. the effect of salinity on growth. Plant Cell Environ 10:59–65. doi:10.1111/j.1365-3040.1987.tb02080.x

    Article  Google Scholar 

  • Sibole JC, Cabot C, Poschenrieder C, Barceló J (2003) Ion allocation in two different salt-tolerant Mediterranean Medicago species. J Plant Physiol 160:1361–1365. doi:10.1078/0176-1617-00811

    Article  PubMed  CAS  Google Scholar 

  • Sibolel JV, Cabot C, Poschenrieder C, Barceló J (2005) Efficient leaf ion partitioning, an overriding condition for abscisic acid-controlled stomatal and leaf growth responses to NaCl salinization in two legumes. J Exp Bot 54:2111–2119

    Article  Google Scholar 

  • Sobrado MA (2005) Leaf characteristics and gas exchange of the mangrove Laguncularia racemosa as affected by salinity. Photosynthetica 43:217–221. doi:10.1007/s11099-005-0036-8

    Article  Google Scholar 

  • Sobrado MA (2007) Relationship of water transport to anatomical features in the mangrove Laguncularia racemosa grown under contrasting salinities. New Phytol 173:584–591. doi:10.1111/j.1469-8137.2006.01927.x

    Article  PubMed  CAS  Google Scholar 

  • Sperry JS, Tyree MT (1990) Water-stress-induced xylem embolism in three species of conifers. Plant Cell Environ 13:427–436. doi:10.1111/j.1365-3040.1990.tb01319.x

    Article  Google Scholar 

  • Strogonov BP (1962) Physiological basis of salt tolerance of plants. Israel program for Scientific Translations, Jerusalem. Translated from Russian, 1964

  • Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18:149–157. doi:10.1111/j.1365-3040.1995.tb00348.x

    Article  Google Scholar 

  • Tyree MT, Davies SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction. IAWA J 15:335–360

    Google Scholar 

  • Vijayan K, Chakraborti SP, Ercisli S, Ghosh PD (2008) NaCl induced morpho-biochemical and anatomical changes in mulberry (Morus spp.). Plant Growth Regul 56:61–69. doi:10.1007/s10725-008-9284-5

    Article  CAS  Google Scholar 

  • Waisel Y (1972) Biology of halophytes. Academic Press, New York

    Google Scholar 

  • Zeng L, Shannon MC (2000) Effect of salinity on grain yield and yield components of rice at different seedling densities. Agron J 92:418–423

    Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71. doi:10.1016/S1360-1385(00)01838-0

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge all the technical staff of the superior agricultural institute (ISA) and the Superior Institute of Biotechnology (ISBM) for their help to conducting these experiments.

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Authors and Affiliations

  1. Laboratoire de Physiologie Végétale, Institut Supérieur Agronomique de Chott Mériem (ISA-CM), BP 47, 4042, Chott-Mériem (Sousse), Tunisia

    Fayçal Boughalleb & Mounir Denden

  2. Laboratoire de Biologie Végétale, Institut Supérieur Agronomique de Chott Mériem (ISA-CM), BP 47, 4042, Chott-Mériem (Sousse), Tunisia

    Bechir Ben Tiba

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  1. Fayçal Boughalleb
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  2. Mounir Denden
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  3. Bechir Ben Tiba
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Correspondence to Fayçal Boughalleb.

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Communicated by J. Zwiazek.

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Boughalleb, F., Denden, M. & Tiba, B.B. Anatomical changes induced by increasing NaCl salinity in three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea . Acta Physiol Plant 31, 947–960 (2009). https://doi.org/10.1007/s11738-009-0310-7

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