Skip to main content
Log in

Different mechanisms of ion homeostasis are dominant in the recretohalophyte Tamarix ramosissima under different soil salinity

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Total ion (Na+, K+, Ca2+, SO4 2− and Cl) accumulation by plants, ion contents in plant tissues and ion secretion by salt glands on the surface of shoots of Tamarix ramosissima adapted to different soil salinity, namely low (0.06 mmol Na+/g soil), moderate (3.14–4.85 mmol Na+/g soil) and strong (7.56 mmol Na+/g soil) were analyzed. There are two stages of interrelated and complementary regulation of ion homeostasis in whole T. ramosissima plants: (1) regulation of ion influx into the plant from the soil and (2) changing the secretion efficiency of salt glands on shoots. The secretion efficiency of salt glands was appraised by the ratio of ion secretion to tissue ion content. Independent of soil salinity, the accumulation of K+ and Ca2+ was higher than the contents of these ions in the soil. Furthermore, the accumulation of K+, Ca2+ and SO4 2− ions by plants was maintained within a narrow range of values. Under low soil salinity, Na+ was accumulated, whereas under moderate and strong salinity, the influxes of Na+ were limited. However, under strong salinity, the accumulation of Na+ was threefold higher than that under low soil salinity. This led to a change in the Na+/K+ ratio (tenfold), an increase in the activity of salt glands (tenfold) and a reduction in plant growth (fivefold). An apparently high Na+/K+ ratio was the main factor determining over-active functioning of salt glands under strong salinity. Principal component analysis showed that K+ ions played a key role in ion homeostasis at all levels of salinity. Ca2+ played a significant role at low salinity, whereas Cl and interrelated regulatory components (K+ and proline) played a role under strong salinity. Proline, despite its low concentration under strong salinity, was involved in the regulation of secretion by salt glands. Different stages and mechanisms of ion homeostasis were dominant in T. ramosissima plants adapted to different levels of salinity. These mechanisms facilitated the accumulation of Na+ in plants under low soil salinity, the limitation of Na+ under moderate salinity and the over-activation of Na+ secretion by salt glands under strong salinity, which are all necessary for maintaining ion homeostasis and water potential in the whole plant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aleman F, Nieves-Cordones M, Martınez V, Rubio F (2011) Root K+ acquisition in plants: the Arabidopsis thaliana Model. Plant Cell Physiol 52(9):1603–1612

    Article  CAS  PubMed  Google Scholar 

  • Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171(9):670–687

    Article  PubMed  Google Scholar 

  • Aslam R, Bostan N, Nabgha-e-Amen Maria M, Safdar W (2011) A critical review on halophytes: salt tolerant plants. J Med Plants Res 5:7108–7118

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Berry W (1970) Characteristics of salts secreted by Tamarix aphylla. Am J Bot 57(10):1226–1230

    Article  CAS  Google Scholar 

  • Berry WL, Thomson WW (1967) Composition of salt secreted by salt glands of Tamarix aphylla. Can J Bot 45:1774–1775

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H1-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot 115:481–494

    Article  PubMed  Google Scholar 

  • Carter JM, Nippert JB (2012) Leaf-level physiological responses of Tamarix ramosissima to increasing salinity. J Arid Environ 77:17–24

    Article  Google Scholar 

  • Chew M (2009) The monstering of tamarisk: how scientists made a plant into a problem. J Hist Biol 42:231–266

    Article  PubMed  Google Scholar 

  • Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumos J (2007) Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278–292

    Article  CAS  PubMed  Google Scholar 

  • Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol 46:1924–1933

    Article  CAS  PubMed  Google Scholar 

  • Cuin TA, Shabala S (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ 30(7):875–885

    Article  CAS  PubMed  Google Scholar 

  • Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59:2697–2706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Tian C, Zhang S, Song J, Zhang F, Mi G, Feng G (2010) Effects of NO3–N on the growth and salinity tolerance of Tamarix laxa Willd. Plant Soil 331(1):57–67

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  PubMed  Google Scholar 

  • Glenn EP, Tanner R, Mendez S, Kehret T, Moore D, Garcia J, Valdes C (1998) Growth rates, salt tolerance and water use characteristics of native and invasive riparian plants from the delta of the Colorado River delta, Mexico. J Arid Environ 40:281–294

    Article  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics. doi:10.1155/2014/701596

    PubMed  PubMed Central  Google Scholar 

  • Hagemeyer J, Waisel Y (1988) Excretion of ions (Cd2+, Li+, Na+, Cl) by Tamarix aphylla. Physiol Plant 73:541–546

    Article  CAS  Google Scholar 

  • Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, Long X (2013) Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One 8:e62085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imada S, Taniguchi T, Acharya K, Yamanaka N (2013) Vertical distribution of fine roots of Tamarix ramosissima in an arid region of southern Nevada. J Arid Environ 92:46–52

    Article  Google Scholar 

  • Jungk AO (2002) Dynamics of nutrient movement at the soil–root interface. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots. The hidden half, 3rd edn. Marcel Dekker, Inc., New York

    Google Scholar 

  • Kavi Kishore PB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    Google Scholar 

  • Kleinkopf G, Wallace A (1974) Physiological basis for salt tolerance in Tamarix ramosissima. Plant Sci Lett 3:157–163

    Article  CAS  Google Scholar 

  • Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324

    Article  CAS  PubMed  Google Scholar 

  • Kong XQ, Gao XH, Sun W, An J, Zhao YX, Zhang H (2011) Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1. Plant Mol Biol 75:567–578

    Article  CAS  PubMed  Google Scholar 

  • Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39(4):949–962

    Article  CAS  PubMed  Google Scholar 

  • Lv S, Jiang P, Chen X, Fan P, Wang X, Li Y (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol Biochem 51:47–52

    Article  CAS  PubMed  Google Scholar 

  • Ma HY, Tian CY, Feng G, Yuan JF (2011) Ability of multicellular salt glands in Tamarix species to secrete Na+ and K+ selectively. Sci China 54(3):282–289

    Article  CAS  Google Scholar 

  • Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao Ch, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63(1):305–317

    Article  CAS  PubMed  Google Scholar 

  • Maathuis FJM (2014) Sodium in plants: perception, signaling, and regulation of sodium fluxes. J Exp Bot 65(3):849–858

    Article  CAS  PubMed  Google Scholar 

  • Maathuis FJM, Antmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni FB, Carrascoc Martinez EA, Alnayef M, Marotti I, Bosi S, Biondi S (2011) Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol 38:818–831

    Article  CAS  Google Scholar 

  • Parida A, Das A (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Pesci P (1989) Involvement of Cl in the increase in proline induced by ABA and stimulated by potassium chloride in barley leaf segments. Plant Physiol 89:1226–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rejeb KB, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284

    Article  PubMed  Google Scholar 

  • Ruan X, Wang Q, Chen Y, Li W (2007) Physiological response of riparian plants to watering in hyper-arid areas of Tarim River, China. Front Biol China 2(1):54–61

    Article  Google Scholar 

  • Ruan X, Wang Q, Pan C, Chen Y, Jiang H (2009) Physiological acclimation strategies of riparian plants to environment change in the delta of the Tarim river, China. Environ Geol 57:1761–1773

    Article  CAS  Google Scholar 

  • Sanadhya P, Agarwal P, Agarwal PK (2015) Ion homeostasis in a salt-secreting halophytic grass. AoB Plants 7:lv055. doi:10.1093/aobpla/plv055

    Article  Google Scholar 

  • Shabala S, Cuin TA (2007) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669

    Article  Google Scholar 

  • Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151(3):257–279

    Article  CAS  PubMed  Google Scholar 

  • Shabala S, Shabala L (2011) Ion transport and osmotic adjustment in plants and bacteria. Biomol Concepts 2:407–419

    Article  CAS  PubMed  Google Scholar 

  • Solomon A, Beer S, Waisel Y, Jones G, Paleg L (1994) Effects of NaCl on the carboxylating activity of Rubisco from Tamarix jordanis in the presence and absence of proline-related compatible solutes. Physiol Plant 90:198–204

    Article  CAS  Google Scholar 

  • Sookbirsingh R, Castillo K, Gill TE, Chianelly RR (2010) Salt Separation Processes in the Saltcedar Tamarix ramosissima (Ledeb.). Commun Soil Sci Plant Anal 41:1271–1281

    Article  CAS  Google Scholar 

  • Storey R, Thomson WW (1994) An X-ray microanalysis study of the salt glands and intracellular calcium crystals of Tamarix. Ann Bot 73(3):307–313. doi:10.1006/anbo.1994.1036

    Article  CAS  Google Scholar 

  • Teakle NL, Tyerman SD (2010) Mechanisms of Cl(−) transport contributing to salt tolerance. Plant Cell Environ 33(4):566–589

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomson WW, Liu LL (1967) Ultrastructural features of the salt gland of Tmarix aphylia L. Planta (Berl.) 73:201–220

    Article  CAS  Google Scholar 

  • Thomson WW, Faraday CC, Gross JW (1988) Salt glands. In: Baker DA, Hall JA (eds) Solute transport in plant cells. Longman, Essex, p 498

    Google Scholar 

  • Vorob’eva LA (1998) Chemical analysis of soils. Mosk Gos Univ, Moscow

    Google Scholar 

  • Wang B, Davenport RJ, Volkov V, Amtmann A (2006) Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. J Exp Bot 57(5):1161–1170

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Wang H, Han B, Wang B, Guo A, Zheng D, Liu C, Chang L, Peng M, Wang X (2012) Sodium instead of potassium and chloride is an important macronutrient to improve leaf succulence and shoot development for halophyte Sesuvium portulacastrum. Plant Physiol Biochem 51:53–62

    Article  CAS  PubMed  Google Scholar 

  • Widado JJ, Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60:4089–4103

    Article  Google Scholar 

  • World Reference Base for Soil Resources (2014) International soil classification system for naming soils and creating legends for soil maps. In: FAO (ed) World soil resources reports No 106. FAO, Rome

  • Yuan F, Leng B, Wang B (2016a) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci 30(7):977. doi:10.3389/fpls.2016.00977

    Google Scholar 

  • Yuan F, Lyu MJA, Leng BY, Zhu XG, Wang BS (2016b) The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Mol Biol 91:241–256. doi:10.1007/s11103-016-0460-0

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Yin L, Pan B (2002) Biological and ecological characteristics of Tamarix L. and its effect on the ecological environment. Sci China 45:18–22

    Article  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the Russian Foundation for Basic Research (Project No. 15-04-00918a). The authors would like to thank Enago (http://www.enago.com) for the English language review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. V. Shuyskaya.

Additional information

Communicated by R. Aroca.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shuyskaya, E.V., Rakhamkulova, Z.F., Lebedeva, M.P. et al. Different mechanisms of ion homeostasis are dominant in the recretohalophyte Tamarix ramosissima under different soil salinity. Acta Physiol Plant 39, 81 (2017). https://doi.org/10.1007/s11738-017-2379-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-017-2379-8

Keywords

Navigation