Abstract
Three differently adapted populations of sewan grass (Lasiurus scindicus Henr.) were evaluated for structural and functional adaptations to high salinity. The habitats were Derawar Fort (DF, least saline, ECe 15.21), Bailahwala Dahar (BD, moderately saline, ECe 27.56 dS m−1) and Ladam Sir (LS, highly saline, ECe 39.18 dS m−1) from within the Cholistan Desert. The adaptive components of salt tolerance in sewan grass were assessed by determining various morpho–anatomical and physiological attributes. The degree of salt tolerance of all three ecotypes of L. scindicus from the saline habitats was compared in a controlled hydroponic system to evaluate the adaptive components that are expected to be genetically fixed during a long evolutionary process. Salinity tolerance in the most tolerant LS population relied on increased root length and total leaf area, restricted uptake of toxic Cl−, increased uptake of Ca2+, high excretion of Na+, accumulation of organic osmolytes, high water use efficiency, increased root, thicker leaf and cortical region, intensive sclerification, large metaxylem vessels, and dense pubescence on abaxial leaf surface. The BD population (from moderately saline soil) relied on high Ca2+ uptake, Na+ excretion, epidermal thickness, large cortical cells, thick endodermis and large vascular tissue. The DF population (from less saline soil) showed a significant decrease in all morphological characteristics; however, it accumulated organic osmolytes for its survival under high salinities. Structural modifications in all three populations were crucial for checking undue water loss under physiological stress that is caused by high amounts of soluble salts in the soil.
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Abernethy GA, Fountain DW, Manus MT (1998) Observations on the leaf anatomy of Festuca novae–zelandiae and biochemical responses to a water deficit. New Zeal J Bot 36:113–123
Alvarez JM, Rocha JF, Machado SR (2008) Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): structure in relation to function. Braz Arch Biol Technol 51:113–119
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15
Arshad M, Hussan AU, Ashraf MY, Noureen S, Moazzam M (2008) Edaphic factors and distribution of vegetation in the Cholistan desert, Pakistan. Pak J Bot 40:1923–1931
Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376
Aslam T, Bostan N, Amen N, Maria M, Safdar W (2011) A critical review on halophytes: salt tolerant plants. J Med Plants Res 5:7108–7118
Awasthi OP, Pathak RK, Pandey SD (1999) Anatomical variation in leaf lamina of ber seedling and budded plants grown at different sodicity levels. Ind J Hort 56:29–33
Azizian A, Sepaskhah AR (2014) Maize response to water, salinity and nitrogen levels: physiological growth parameters and gas exchange. Int J Plant Prod 8:131–162
Azmi AR, Alam SM (1990) Effect of salt stress on germination, growth, leaf anatomy and mineral element composition of wheat cultivars. Acta Physiol Plant 12:215–224
Bagniewska ZA, Zenkteler E (2006) Ultrastructure of endodermis and stele cells of dehydrated Polypodium vulgare L. rhizomes. Acta Biol Crac Ser Bot 48:73–81
Bahaji A, Mateu I, Sanz A, Cornejo MJ (2002) Common and distinctive responses of rice seedlings to saline and osmotically generated stress. Plant Growth Regul 38:83–94
Balsamo RA, Willigen CV, Bauer AM, Farrant J (2006) Drought tolerance of selected Eragrostis species correlates with leaf tensile properties. Ann Bot 97:985–991
Basal H (2010) Response of cotton (Gossypium hirsutum L.) genotypes to salt stress. Pak J Bot 42:505–511
Bates LS, Waldern RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Baum SF, Tran PN, Silk WK (2000) Effects of salinity on xylem structure and water use in growing leaves of sorghum. New Phytol 146:119–127
Bohnert HJ, Jensen RG (1996) Strategies for engineering water stress tolerance in plants. Trends Biotechnol 14:89–97
Boughalleb F, Denden M, Tiba BB (2009) Anatomical changes induced by increasing NaCl salinity in three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea. Acta Physiol Plant 31:947–960
Breckle SW (2004) Flora, vegetation und Ökologie der alpinnivalen Stufe des Hindukusch (Afghanistan). In: Breckle SW, Schweizer B, Fangmeier A (eds) Proceedings of 2nd symposium A. F. W. Schimper–Foundation: results of worldwide ecological studies. Stuttgart–Hohenheim, Stuttgart, pp 97–117
Chandramony D, George MK (1975) Nutritional effects of calcium, magnesium, silica and sodium chloride on certain anatomical characters of rice plant related to lodging. Agric Res J Kerala 13:39–42
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
Dolatabadian A, Sanavy SAMM, Ghanati F (2011) Effect of Salinity on growth, xylem structure and anatomical characteristics of soybean. Not Sci Biol 3:41–45
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
Gielwanowska I, Szczuka E, Bednara J, Gorecki R (2005) Anatomical features and ultrastructure of Deschampsia Antarctica (Poaceae) leaves from different growing habitats. Ann Bot 96:1109–1119
Grigore MN, Toma C (2007) Histo-anatomical strategies of Chenopodiaceae halophytes: adaptive, ecological and evolutionary implications. WSEAS Trans Biol Biomed 12:204–218
Guo ZH, Miao XF (2010) Growth changes and tissues anatomical characteristics of giant reed (Arundo donax L.) in soil contaminated with arsenic, cadmium and lead. J Central South Uni Technol 17:770–777
Hameed M, Ashraf M (2008) Physiological and biochemical adaptations of Cynodon dactylon (L.) Pers. from the Salt Range (Pakistan) to salinity stress. Flora 203:683–694
Hameed M, Naz N, Ahmad MSA, Shazad ID, Riaz A (2008) Morphological adaptations of some grasses from the salt range, Pakistan. Pak J Bot 40:1571–1578
Hameed M, Ashraf M, Naz N (2009) Anatomical adaptations to salinity in cogon grass [Imperata cylindrica (L.) Raeuschel] from the Salt Range, Pakistan. Plant Soil 322:229–238
Hameed M, Ashraf M, Naz N, Qurainy FA (2010) Anatomical adaptations of Cynodon dactylon (L.) Pers. from the Salt Range Pakistan to salinity stress. I. Root and stem anatomy. Pak J Bot 42:279–289
Hameed M, Ashraf M, Naz N (2011) Anatomical and physiological characteristics relating to ionic relations in some salt tolerant grasses from the Salt Range, Pakistan. Acta Physiol Plant 33:1399–1409
Hameed M, Nawaz T, Ashraf M, Tufail A, Kanwal H, Ahmad MSA, Ahmad I (2012) Leaf anatomical adaptations of some halophytic and xerophytic sedges of the Punjab. Pak J Bot 44:159–164
Hameed M, Ashraf M, Naz N, Nawaz T, Batool R, Riaz A (2013) Physio-anatomical adaptations in response to salt stress in a potential forage grass Sporobolus arabicus Boiss. from a salt-affected sub-mountainous region. Turk J Bot 37:715–724
Hariadi Y, Marandon K, Tian Y, Jacobsen S, Shabala S (2011) Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J Exp Bot 62:85–193
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32
Hose E, Clarkson DT, Steudle E (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52:2245–2264
Jiang CD, Jiang GM, Wang X, Li LH, Biswas DK, Li YG (2006) Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP. Environ Exp Bot 58:261–268
Jianjing MA, Chengjun JI, Mei H, Tingfang Z, Xuedong Y, Dong H, Hui Z, Jinsheng H (2012) Comparative analyses of leaf anatomy of dicotyledonous species in Tibetan and Inner Mongolian grassland. Sci China Life Sci 55:68–79
Khan MA, Gul B, Weber DJ (2000) Germination responses of Salicornia rubra to temperature and salinity. J Arid Environ 45:207–214
Lacerda CF, Cambraia J, Oliva MA, Ruiz HA, Prisco JT (2003) Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environ Exp Bot 49:107–120
Liu DH, Wang M, Zou JH, Jiang WS (2006) Uptake and accumulation of cadmium and some nutrient ions by roots and shoots of maize. Pak J Bot 38:701–709
Lo TY, Cui HZ, Tang PWC, Leung HC (2008) Strength analysis of bamboo by microscopic investigation of bamboo fibre. Cons Build Mat 22:1532–1535
Lowry LH, Rosebrough NJ, Farra L, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Majeed A, Mansoor SA (2010) Morphological variations in Panicum antidotale Retz. against salt stress. Biol E-J Life Sci 1:1–6
Malibari AA, Zidan MA, Heikal MM, Shamary SE (1993) Effect of salinity on germination and growth of alfalfa, sunflower and sorghum. Pak J Bot 25:156–160
Marcum KB, Pessarakli M (2006) Relative salinity tolerance and salt gland excretion activity of Bermuda grass turf cultivars. Crop Sci 46:2571–2574
Marcum KB, Anderson SJ, Engelke MC (1998) Salt gland ion secretion: A salinity tolerance mechanism among five zoysia grass species. Crop Sci 38:806–810
Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: Photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26
Monteverdi CM, Lauteri M, Valentini R (2008) Biodiversity of plant species and adaptation to drought and salt conditions. Selection of species for sustainable reforestation activity to combat desertification. In: Abdelly C, Öztürk M, Ashraf M, Grignon C (eds) Biosaline agriculture and high salinity tolerance. Birkhaüser Verlag, Switzerland, pp 197–206
Moor S, Stein WH (1948) Photometric ninhydrin method for use in the chromatography of amino acids. J Biol Chem 176:367–388
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
Naidoo L, Cho MA, Mathieu R, Asner G (2012) Classification of savanna tree species, in the Greater Kruger National Park region, by integrating hyperspectral and Li-DAR data in a Random Forest data mining environment. J Photogram Remote Sensing 69:167–179
Nawaz K, Hussain K, Majeed A, Khan F, Afghan S, Ali K (2010) Fatality of salt stress to plants: morphological, physiological and biochemical aspects. Afr J Biotechnol 34:5475–5480
Nawazish S, Hameed M, Naurin S (2006) Leaf anatomical adaptations of Cenchrus ciliaris L. from the Salt Range, Pakistan against drought stress. Pak J Bot 38:1723–1730
Naz N, Hameed M, Ashraf M, Ahmad R, Arshad M (2009a) Eco-morphic variation for salt tolerance in some grasses from Cholistan Desert, Pakistan. Pak J Bot 41:1707–1714
Naz N, Hameed M, Wahid A, Arshad M, Ahmad MSA (2009b) Patterns of ion excretion and survival in two stoloniferous arid zone grasses. Physiol Plant 135:185–195
Naz N, Hameed M, Ashraf M, Arshad M, Ahmad MSA (2010) Impact of salinity on species association and phytosociology of halophytic plant communities in the Cholistan desert, Pakistan. Pak J Bot 42:2359–2367
Naz N, Hameed M, Nawaz T, Batool R, Ashraf M, Ahmad F, Ruby T (2013) Structural adaptations in the desert halophyte Aeluropus lagopoides (Linn.) Trin. ex Thw. under high salinity. J Biol Res-Thessaloniki 19:150–164
Nilson SE, Assmann SM (2007) The control of transpiration: insights from Arabidopsis. Plant Physiol 143:19–27
Rashid P, Ahmed A (2011) Anatomical adaptations of Myriostachya wightiana hook. F. to salt stress. Dhaka Uni J Biol Sci 20:205–208
Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, Oxford, p 322
Saqib M, Akhtar J, Qureshi RH (2005) Na+ exclusion and salt resistance of wheat (Triticum aestivum) in saline–waterlogged conditions are improved by the development of adventitious nodal roots and cortical root aerenchyma. Plant Sci 169:125–130
Shabala S, Lew RR (2002) Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol 129:290–299
Shabala S, Munns R (2012) Salinity stress: physiological constraints and adaptive mechanisms. Plant Stress Physiology. CAB International, Oxford, pp 59–93
Taleisnik E, Peyrano G, Córdoba A, Arias C (1999) Water retention capacity in root segments differing in the degree of exodermis development. Ann Bot 83:19–27
Valenti GS, Ferro M, Ferraro D, Riveros F (1991) Anatomical changes in Prosopis tamarugo Phil. seedlings growing at different levels of NaCl salinity. Ann Bot 68:47–53
Voltolini CH, Reis A, Santos M (2009) Leaf morpho-anatomy of the rheophyte Dyckia distachya Hassler (Bromeliaceae). Revista Bras de Biosci 7:335–343
Weber DJ (2009) Adaptive mechanisms of halophytes in desert regions. In: Ashraf M, Ozturk M, Athar HR (eds) Salinity and water stress. Springer-Verlag, Berlin, pp 179–186
Wolf B (1982) An improved universal extracting solution and its use for diagnosing soil fertility. Commun Soil Sci Plant Anal 13:1005–1033
Wu QS, Zou YN, Liu W, Ye XF, Zai HF, Zhao LJ (2010) Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ 56:470–475
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514
Yoshiba Y, Kiyosue T, Nakashima K, Shinozaki KYY, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102
YuJing Z, Yong Z, ZiZhi H, ShunGuo Y (2000) Studies on microscopic structure of Puccinellia tenuiflora stem under salinity stress. Grassland China 5:6–9
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We are thankful to Prof. Phil Harris (Department of Plant Sciences, Centre for Agroecology and Food Security, Coventry University, Priory Street, Coventry CV1 5FB, UK), who read and corrected the manuscript.
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Naz, N., Rafique, T., Hameed, M. et al. Morpho-anatomical and physiological attributes for salt tolerance in sewan grass (Lasiurus scindicus Henr.) from Cholistan Desert, Pakistan. Acta Physiol Plant 36, 2959–2974 (2014). https://doi.org/10.1007/s11738-014-1668-8
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DOI: https://doi.org/10.1007/s11738-014-1668-8