Plant and Soil

, Volume 372, Issue 1–2, pp 523–539 | Cite as

Ionic relationships in some halophytic Iranian Chenopodiaceae and their rhizospheres

  • Zeinab Matinzadeh
  • Siegmar-W. Breckle
  • Massoud Mirmassoumi
  • Hossein Akhani
Regular Article


Previous studies on the identification of ion relations in halophytes have revealed that many members of Chenopodiaceae accumulate high amounts of sodium and chloride even in soils with low salinity, indicating a typical pattern which is genetically fixed. In this study, we followed up with the question of ion relations in different halophyte species with different photosynthetic pathways and different salt tolerance strategies over a complete growing season. Soil and plant samples from five species Climacoptera turcomanica (Litv.) Botsch. (leaf succulent-C4), Salicornia persica Akhani subsp. rudshurensis Akhani (stem succulent-C3), Halimocnemis pilifera Moq. (leaf succulent-C4), Petrosimonia glauca (Pall.) Bunge (leaf succulent-C4) and Atriplex verrucifera M. Bieb. (recreto-halophyte-C3) were collected over a complete growing season from a salt flat 60 km W of Tehran. The contents of main cations (Na+, K+, Ca2+, and Mg2+) and chloride were determined in plant and soil samples. Na+ and Cl concentration in the shoots of two hygro-halophytes Climacoptera turcomanica and Salicornia persica subsp. rudshurensis were constant over the period of the growing season. In contrast, sodium and chloride in the shoots of Halimocnemis pilifera and Petrosimonia glauca showed respectively an increasing and, in the shoots of Atriplex verrucifera, a decreasing, trend. We did not notice any decreasing trend of K+ together with increasing trend of Na+ in the shoots of the studied species; however K+ in the shoots of all examined species was considerably lower than Na+ and Cl. It was observed that Climacoptera and Salicornia could absorb and retain calcium even in high salinity conditions, while Halimocnemis and Petrosimonia could not. Na+, K+, Cl, Ca2+, and Mg2+ contents in the shoots of different types of halophytes (stem-succulent, leaf-succulent and excreting halophyte) or different type of photosynthesis (C3, C4) are independent of those in their rhizosphere. We concluded that it is controlled by the genetic characteristic of the specific taxon rather than by the environment.


Atriplex C3-C4 plants Halophytes of Iran NaCl Physiotype Recreto-halophytes Salicornia Salsoleae Saline soils Succulent halophytes 



This paper is the result of a research project supported by Iranian National Science Foundation (INSF) under Project No. 842951 and “Geobotanical Studies in Different Parts of Iran VI” supported by the Research Council University of Tehran under project number 6104037/1. The soil and water analysis were carried out in part in the Plant Physiology Laboratory of the School of Biology, Laboratory of Geology of the School of Geology and the Soil and Water Research Institute, Ministry of Jihade Agriculture. We thank the directors and staffs of these laboratories in particular Dr. V. Niknam and Dr. K. Bazargani for their generous help and the useful comments by two anonymous referees.

Supplementary material

11104_2013_1744_MOESM1_ESM.docx (121 kb)
ESM 1 (DOCX 121 kb)


  1. Akhani H (2006) Biodiversity of halophytic and sabkha ecosystems in Iran. In: Ajmal Khan M et al (eds.) (ed) Sabkha Ecosystems Volume II: West and Central Asia. Springer, pp 71–88Google Scholar
  2. Akhani H (2008) Taxonomic revision of the genus Salicornia L. (Chenopodiaceae) in Central and Southern Iran. Pak J Bot 40(4):1635–1655Google Scholar
  3. Akhani H, Trimborn P, Ziegler H (1997) Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol 206(1–4):187–221CrossRefGoogle Scholar
  4. Akhani H, Ghobadnejhad M, Hashemi SMH (2003) Ecology, biogeography and pollen morphology of Bienertia cycloptera Bunge ex Boiss. (Chenopodiaceae), an Enigmatic C4 plant without Kranz anatomy. Plant Biol 5(2):167–178CrossRefGoogle Scholar
  5. Akhani H, Edwards G, Roalson EH (2007) Diversification of the Old World Salsoleae s.l. (Chenopodiaceae): molecular phylogenetic analysis of nuclear and chloroplast data sets and a revised classification. Int J Plant Sci 168(6):931–956CrossRefGoogle Scholar
  6. Akhani H, Lara MV, Ghasemkhani M, Ziegler H, Edwards GE (2009) Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of delta C-13 values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system? Photosynth Res 99(1):23–36PubMedCrossRefGoogle Scholar
  7. Albert R (1982) Halophyten. In: Kinzel H (ed) Pflanzenökologie und Mineralstoffwechsel. Ulmer, Stuttgart, pp 33–204Google Scholar
  8. Albert R, Popp M (1977) Chemical composition of Halophytes from Neusiedler Lake Region in Austria. Oecologia 27(2):157–170CrossRefGoogle Scholar
  9. Aronson JA (1989) HALOPH, a database of salt tolerant plants of the world. Office of Arid Lands Studies. University of Arizona, TucsonGoogle Scholar
  10. Arruda SCC, Rodriguez APM, Arruda MAZ (2003) Ultrasound-assisted extraction of Ca, K and Mg from in vitro citrus culture. J Braz Chem Soc 14(3):470–474CrossRefGoogle Scholar
  11. Ayala F, Oleary JW, Schumaker KS (1996) Increased vacuolar and plasma membrane H+ −ATPase activities in Salicornia bigelovii Torr in response to NaCl. J Exp Bot 47(294):25–32Google Scholar
  12. Balnokin YV, Myasoedov NA, Shamsutdinov ZS, Shamsutdinov NZ (2005) Significance of Na + and K + for sustained hydration of organ tissues in ecologically distinct halophytes of the family Chenopodiaceae. Russ J Plant Physiol 52(6):779–787CrossRefGoogle Scholar
  13. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12(4):431–434PubMedCrossRefGoogle Scholar
  14. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. BBA-Rev Biomembr 1465(1–2):140–151Google Scholar
  15. Breckle S-W (1975) Ionengehalte halophiler Pflanzen Spaniens. Decheniana (Bonn) 127:221–228Google Scholar
  16. Breckle S-W (1976) Zur Ökologie und den Mineralstoffverhältnissen absalzender und nicht absalzender Xerohalophyten (unter besonderer Berücksichtigung von Untersuchungen an Atriplex confertifolia und Ceratoides lanata in Utah/USA). Diss Bot 35:169ppGoogle Scholar
  17. Breckle S-W (1986) Studies on halophytes from Iran and Afghanistan.2. Ecology of halophytes along salt gradients. Proc R Soc Edinb B 89:203–215Google Scholar
  18. Breckle S-W (1990) Salinity tolerance of different halophyte types. Plant Soil 148:167–175Google Scholar
  19. Breckle S-W (1995) How do halophytes overcome salinity? In: Khan MA, Ungar IA (eds) Biology of salt tolerant plants. Book Graffers, Chelsea, pp 199–213Google Scholar
  20. Breckle S-W (1996) Root growth and root architecture of non-halophytes under saline soil conditions. Acta Phytogeogr Suec 81:44–47Google Scholar
  21. Breckle S-W (2002) Salinity, halophytes and salt affected natural ecosystems. In: Läuchli A, Lüttge U (eds) Salinity: environment -plant –molecules. Kluwer Academic Publishers, Dordrecht, pp 53–77Google Scholar
  22. Breckle S-W (2003) Rehabilitation of the Aral Sea environment, Kazakhstan. In: Proceedings of the International workshop (Aleppo, May 2002): “Combating desertification – rehabilitation of degraded drylands and biosphere reserves”. UNESCO-MAB dryland series No.2, pp 47–57Google Scholar
  23. Breckle S-W (2009) Is sustainable agriculture with seawater irrigation realistic? In: Ashraf M, Oztürk M, Athar H-R (eds) Salinity and water Stress. Springer, pp 187–196Google Scholar
  24. Breckle S-W (2013) From Aral Sea to Aralkum – an ecological disaster or halophytes’ paradise. Prog Bot 74:351–398CrossRefGoogle Scholar
  25. Breckle S-W, Wucherer W (2012) Halophytes and salt desertification in the Aralkum Area. In: Breckle S-W, Dimeyeva L, Wucherer W, Ogar NP (ed) Aralkum – a man-made desert: the desiccated floor of the Aral Sea (Central Asia). Ecol Stud 218. Springer, pp 271–299Google Scholar
  26. Breckle S-W, Freitas H, Reimann C (1990) Sampling Atriplex Bladders: a comparison of methods. Plant Cell Environ 13:871–873CrossRefGoogle Scholar
  27. Brownell PF, Crosslan C (1972) Requirement for sodium as a micronutrient by species having C4 dicarboxylic photosynthetic pathway. Plant Physiol 49(5):794–797PubMedCrossRefGoogle Scholar
  28. Chen ZH, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou MX, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na + homeostasis in salt-stressed barley. Plant Physiol 145(4):1714–1725PubMedCrossRefGoogle Scholar
  29. Dajic Z (2006) Salt sterss. In: Madhava Rao KV, Raghavendra AS, Janardhan KR (eds) Physiology and molecular biology of stress tolerance in plants. Springer, Dordrecht, pp 41–99CrossRefGoogle Scholar
  30. Dimeyeva L, Breckle S-W, Wucherer W (2012) Flora of the Aralkum. In: Breckle S-W, Dimeyeva L, Wucherer W, Ogar NP (ed) Aralkum – a man-made desert: the desiccated floor of the Aral Sea (Central Asia). Ecol Stud 218, vol 218. Springer, pp 109–126Google Scholar
  31. Donovan LA, Richards JH, Schaber EJ (1997) Nutrient relations of the halophytic shrub, Sarcobatus vermiculatus, along a soil salinity gradient. Plant Soil 190(1):105–117CrossRefGoogle Scholar
  32. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefGoogle Scholar
  33. Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61(3):313–337CrossRefGoogle Scholar
  34. Freitas H, Breckle S-W (1992) Importance of bladder hairs for salt tolerance of field-grown Atriplex-species from a Portuguese salt marsh. Flora 187:283–297Google Scholar
  35. Frey W, Kürschner H, Stichler W (1985) Photosynthetic pathways and ecological distribution of halophytes from four littoral salt marshes (Egypt/Sinai, Saudi Arabia, Oman and Iran). Flora 177:107–130Google Scholar
  36. Gautier H, Lopez-Lauri F, Massot C, Murshed R, Marty I, Grasselly D, Keller C, Sallanon H, Génard M (2009) Impact of ripening and salinity on tomato fruit ascorbate content and enzymatic activities related to ascorbate recycling. Func Plant Sci Biotech 4 (special issue 1) 66–75Google Scholar
  37. Ghnaya T, Slama I, Messedi D, Grignon C, Ghorbel MH, Abdelly C (2007) Effects of Cd2+ on K+, Ca2+ and N uptake in two halophytes Sesuvium portulacastrum and Mesembryanthemum crystallinum: consequences on growth. Chemosphere 67(1):72–79PubMedCrossRefGoogle Scholar
  38. Grigore MN, Toma C (2008) Ecological anatomy investigations related to some halophyte species from Moldavia. Rom J Biol - Plant Biol 53:23–30Google Scholar
  39. Han N, Shao Q, Lu CM, Wang BS (2005) The leaf tonoplast V-H+-ATPase activity of a C3 halophyte Suaeda salsa is enhanced by salt stress in a Ca-dependent mode. J Plant Physiol 162:267–274PubMedCrossRefGoogle Scholar
  40. Hawker JS, Walker RR (2010) The effect of sodium chloride on the growth and fruiting of Cabernet Sauvignon Vines. Am J Enol Vitic 6:498–505Google Scholar
  41. Hedge IC, Akhani H, Freitag H, Kothe-Heinrich G, Podlech D, Rilke S, Uoltila P (1997) Chenopodiaceae. In: Rechinger KH (ed) Flora Iranica, vol 172. Akademische Druck- u. Verlagsanstalt, GrazGoogle Scholar
  42. Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136(1):2457–2462PubMedCrossRefGoogle Scholar
  43. Keller BA (1925) Halophyten- und Xerophytenstudien. J Ecol 13:224–255CrossRefGoogle Scholar
  44. Khan MA, Weber DJ (1986) Factors influencing seed-germination in Salicornia-pacifica var. utahensis. Am J Bot 73(8):1163–1167Google Scholar
  45. Kinzel H (1982) Pflanzenökologie und Mineralstoffwechsel. Ulmer, Stuttgart, p 534Google Scholar
  46. Koyro H-W, Geißler N, Hussin S, Huchzermeyer B (2008) Survival at extreme locations: Life strategies of halophytes - The long way from system ecology, whole plant physiology, cell biochemistry and molecular aspects back to sustainable utilization at field sites In: Abdelly C., Oztürk M, Ashraf M, Grignon C (eds) Biosaline agriculture and high salinity tolerance. Springer, pp 2–20Google Scholar
  47. Krinsley DB (1970) A geomorphological and palaeoclimatological study of the playas of Iran. U. S. Government Printing Office, WashingtonGoogle Scholar
  48. Liangpeng Y, Jian M, Yan L (2007) Soil salt and nutrient concentration in the rhizosphere of desert halophytes. Acta Ecol Sin 27:3565–3571CrossRefGoogle Scholar
  49. Lianngxue L (1998) Determination of chloride in plant tissue. In: Yash KP (ed) Handbook of reference methods for plant analysis. 14. Soil and plant analysis council. CRC press, Florida, pp 111–113Google Scholar
  50. Libert B, Franceschi VR (1987) Oxalate in crop plants. J Agric Food Chem 35(6):926–938CrossRefGoogle Scholar
  51. Maathuis FJM (2006) The role of monovalent cation transporters in plant responses to salinity. J Exp Bot 57(5):1137–1147PubMedCrossRefGoogle Scholar
  52. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84(2):123–133CrossRefGoogle Scholar
  53. Mozafar A, Goodin JR (1970) Vesiculated hairs - a mechanism for salt tolerance in Atriplex-halimus L. Plant Physiol 45(1):62–65PubMedCrossRefGoogle Scholar
  54. Munns R, Rawson HM (1999) Effect of salinity on salt accumulation and reproductive development in the apical meristem of wheat and barley. Aust J Plant Physiol 26(5):459–464CrossRefGoogle Scholar
  55. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  56. Ohnishi J, Kanai R (1990) Pyruvate uptake induced by a Ph Jump in Mesophyll Chloroplasts of Maize and Sorghum, Nadp-Malic Enzyme Type-C4 species. FEBS Lett 269(1):122–124PubMedCrossRefGoogle Scholar
  57. Osmond CB (1963) Oxalates and ionic equilibrium in Australian saltbushes (Atriplex). Nature 198:503–504CrossRefGoogle Scholar
  58. Osmond CB (1974) Leaf anatomy of Australian saltbushes in relation to photosynthetic pathways. Aust J Bot 22:39–44CrossRefGoogle Scholar
  59. Pandolfi C, Mancuso S, Shabala S (2012) Physiology of acclimation to salinity stress in pea (Pisum sativum). Environ Exp Bot 84:44–51CrossRefGoogle Scholar
  60. Reimann C, Breckle S-W (1988) Salt secretion in some Chenopodium species. Flora 180:289–296Google Scholar
  61. Reimann C, Breckle S-W (1993) Sodium relations in Chenopodiaceae, a comparative approach. Plant Cell Environ 16:323–328CrossRefGoogle Scholar
  62. Reimann C, Breckle S-W (1995) Salt tolerance and ion relations of Salsola kali L.: difference between ssp. tragus (L.) Nyman and ssp. ruthenica (Iljin) Soo. New Phytol 130:37–45CrossRefGoogle Scholar
  63. Sahrawat KL (1987) Determination of calcium, magnesium, zinc and manganese in plant-tissue using a dilute Hcl extraction method. Commun Soil Sci Plant 18(9):947–962CrossRefGoogle Scholar
  64. Schirmer U, Breckle S-W (1982) The role of bladders for salt removal in some Chenopodiaceae (mainly Atriplex species). In: Sen DN, Rajpurohit KS (eds) Contributions to the ecology of halophytes: tasks for vegetation science. Junk, Den Haag, pp 215–231Google Scholar
  65. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141(4):1653–1665PubMedCrossRefGoogle Scholar
  66. Soil and Plant Analysis Council I (2000) Soil analysis: handbook of reference methods. CRC Press, Boca RatonGoogle Scholar
  67. Steiner M (1939) Die Zusammensetzung des Zellsaftes bei höheren Pflanzen in ihrer ökologischen Bedeutung. Erg Biol 17:151–254Google Scholar
  68. Teakle NL, Bazihizina N, Shabala S, Colmer TD, Barrett-Lennard EG, Rodrigo-Moreno A, Läuchli AE (2013) Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K + retention in roots. Environ Exp Bot 87:69–78CrossRefGoogle Scholar
  69. Uchiyama Y, Sugimura Y (1985) Salt-excreting function of vesiculated hairs of Atriplex nummularia. Jpn J Crop Sci 54(1):39–46CrossRefGoogle Scholar
  70. Ushakova SA, Kovaleva NP, Gribovskaya TV, Dolgushev VA, Tikhomirova NA (2005) Effect of NaCl concentration on productivity and mineral composition of Salicornia europaea as a potential crop for utilization NaCl in LSS. In: Space life sciences: gravity-related effects on plants and spaceflight and man-made environments on biological systems, vol 36. Adv Space Res. pp 1349–1353Google Scholar
  71. Veste M, Sartorius U, Breckle SW (2008) Ion relations of plants and soil patterns. In: Breckle S-W, Yair A, Veste M (eds) Ecological studies, arid dune ecosystems, vol 200. Ecological studies. Springer, Berlin, pp 353–365CrossRefGoogle Scholar
  72. Walker RR, Kriedemann PE, Maggs DH (1979) Growth, leaf physiology and fruit development in salt-stressed guavas. Aust J Agric Res 30:477–488CrossRefGoogle Scholar
  73. Walter H, Lieth H (1967) Klimadiagram-Weltatlas. VEB Gustav Fischer Verlag, JenaGoogle Scholar
  74. Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56(3):525–539CrossRefGoogle Scholar
  75. Welkie GW, Caldwell MM (1970) Leaf anatomy of species in some dicotyledon families as related to the C3 and C4 pathways of carbon fixation. Can J Bot 48:2135–2146CrossRefGoogle Scholar
  76. Wiebe HH, Walter H (1972) Mineral ion composition of halophytic species from Northern Utah. Am Midl Nat 87(1):241–245CrossRefGoogle Scholar
  77. Wucherer W, Veste M, Bonilla OH, Breckle S-W (2005) Halophytes as useful tools for rehabilitation of degraded lands and soil protection. In: Proceeding International forum on ecological construction of the western Baijing, Baijing, pp 87–94Google Scholar
  78. Wucherer W, Breckle S-W, Kaverin VS, Dimeyeva L, Zhamantikov K (2012) Phytomelioration in the Northern Aralkum. In: Breckle S-W, Dimeyeva L, Wucherer W, Ogar NP (ed) Aralkum – a man-made desert: the desiccated floor of the Aral Sea (Central Asia). Ecol Stud 218, vol 218. Springer, pp 343–386Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Zeinab Matinzadeh
    • 1
  • Siegmar-W. Breckle
    • 2
  • Massoud Mirmassoumi
    • 1
  • Hossein Akhani
    • 1
  1. 1.Department of Plant Sciences, School of Biology, Center of Excellence of Phylogeny of Living OrganismsUniversity of TehranTehranIran
  2. 2.Department EcologyUniversity of BielefeldBielefeldGermany

Personalised recommendations