Skip to main content
Log in

Salinity and waterlogging tolerances in three stem-succulent halophytes (Tecticornia species) from the margins of ephemeral salt lakes

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Tecticornia species are stem-succulent, perennial halophytes (sub-family Salicornioideae; Chenopodiaceae) that inhabit saline areas including the margins of ephemeral salt lakes in Australia. Based on zonation observed at salt lakes, species were hypothesised to differ in tolerances to salinity and/or waterlogging.

Methods

Three Tecticornia species were grown in sub-irrigated or waterlogged sand culture with treatments from 10 to 800 mM NaCl, for 60 d in a glasshouse. Growth, tissue solutes, root porosity, root radial O2 loss, and ethanol production, were assessed.

Results

The three species were salt tolerant; at 800 mM NaCl shoot RGR (ash-free) was reduced by 9% in T. indica, 22% in T. pergranulata and 39% in T. mellaria. Na+ and Cl were the predominant osmotica in succulent stem tissues. Glycinebetaine was a major organic solute. T. pergranulata and T. indica were waterlogging tolerant; shoot RGR was reduced by at most 29% irrespective of salinity. Waterlogging tolerance in T. mellaria was variable (shoot RGR 8%–56% of controls) and some individuals died. T. pergranulata formed adventitious roots with aerenchyma, but the two other species did not. Anoxic tips of lateral roots produced ethanol.

Conclusion

The three Tecticornia species are salt tolerant. T. pergranulata is also waterlogging tolerant and formed adventitious roots containing aerenchyma, traits consistent with growth on mud flats of salt lakes. T. indica was unexpectedly tolerant of waterlogging, whereas T. mellaria was less tolerant. Future work is needed to evaluate tolerances of inundation (i.e. submergence) and to higher salinity treatments.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:226–332

    Google Scholar 

  • Armstrong W (1994) Polarographic electrodes and their use in plant aeration studies. Proc Roy Soc Edinb B 102B:511–527

    Google Scholar 

  • Armstrong W, Wright EJ (1975) Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiol Plant 35:21–26

    Article  Google Scholar 

  • Ayala F, O’Leary JW (1995) Growth and physiology of Salicornia bigelovii Torr. at suboptimal salinity. Int J Plant Sci 156:197–205

    Article  Google Scholar 

  • Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant Soil 253:35–54

    Article  CAS  Google Scholar 

  • Beutler HO (1983) Ethanol. In: Bergmeier HU, Bergmeyer J, Graß M (eds) Methods of enzymatic analysis, volume VI, metabolites 1: carbohydrates. Verlag-Chemie, Weinheim, pp 598–607

    Google Scholar 

  • Blom CWPM, Voesenek LACJ, Banga M, Engelaar WMHG, Rijnders JHGM, Van de Steeg HM, Visser EJW (1994) Physiological ecology of riverside species: adaptive responses of plants to submergence. Ann Bot 74:253–263

    Article  Google Scholar 

  • Briens M, Larher F (1982) Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell Environ 5:287–292

    CAS  Google Scholar 

  • Cantero JJ, Leon R, Cisneros JM, Cantero A (1998) Habitat structure and vegetation relationships in central Argentina salt marsh landscapes. Plant Ecol 137:79–100

    Article  Google Scholar 

  • Cavalieri AJ, Huang AHC (1979) Evaluation of proline accumulation in the adaptation of diverse species of marsh halophytes to the saline environment. Am J Bot 66:307–312

    Article  CAS  Google Scholar 

  • Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytol 179:964–974

    Article  PubMed  CAS  Google Scholar 

  • Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. J Exp Bot 62:39–57

    Article  PubMed  CAS  Google Scholar 

  • Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681

    Article  Google Scholar 

  • Colmer TD, Vos H, Pedersen O (2009) Tolerance of combined submergence and salinity in the halophytic stem-succulent Tecticornia pergranulata. Ann Bot 103:303–312

    Article  PubMed  CAS  Google Scholar 

  • Datson B (2002) Samphires in Western Australia. Department of Conservation and Land Management, Perth

    Google Scholar 

  • de Fraine E (1912) The anatomy of the genus Salicornia. Bot J Linn Soc 41:317–348

    Google Scholar 

  • Fan TWM, Colmer TD, Lane AN, Higashi RM (1993) Determination of metabolites by 1H-NMR and GC: analysis for organic osmolytes in crude tissue extracts. Anal Biochem 214:260–271

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Ann Rev Plant Physiol 28:89–121

    Article  CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–337

    Article  Google Scholar 

  • Galloway R, Davidson J (1993) The response of Atriplex amnicola to the interactive effects of salinity and hypoxia. J Exp Bot 44:653–663

    Article  Google Scholar 

  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Glenn EP, O’Leary JW (1984) Relationship between salt accumulation and water content of dicotyledenous halophytes. Plant Cell Environ 7:253–261

    CAS  Google Scholar 

  • Gorham J, Hughes LL, Wyn Jones RG (1980) Chemical composition of salt-marsh plants from Ynys Mon (Anglesey): the concept of physiotypes. Plant Cell Environ 3:309–318

    Article  CAS  Google Scholar 

  • Greenway H, Munns R (1983) Interactions between growth, uptake of Cl and Na+, and water relations of plants in saline environments. II. Highly vacuolated cells. Plant Cell Environ 6:575–589

    Article  CAS  Google Scholar 

  • Guy RD, Warne P, Reid DM (1984) Glycinebetaine content of halophytes: improved analysis by liquid chromatography and interpretation of results. Physiol Plant 61:195–202

    Article  CAS  Google Scholar 

  • Hole DJ, Cobb BG, Hole PS, Drew MC (1992) Enhancement of anaerobic respiration in root tips of Zea mays following low-oxygen (hypoxic) acclimation. Plant Physiol 99:213–218

    Article  PubMed  CAS  Google Scholar 

  • Howes Keiffer C, McCarthy BC, Ungar IA (1994) Effect of salinity and waterlogging on growth and survival of Salicornia europaea L., an inland halophyte. Ohio Sci 94:70–73

    Google Scholar 

  • Hunt J (1982) Dilute hydrochloric acid extraction of plant material for routine cation analysis. Comm Soil Sci Plant Anal 13:49–55

    Google Scholar 

  • Jackson MB, Drew MC (1984) Effects of flooding on growth and metabolism of herbaceous plants. In: Kozlowski TT (ed) Flooding and plant growth. Academic, London, pp 47–128

    Google Scholar 

  • Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Article  Google Scholar 

  • Keppel G (1973) Design and analysis: a researcher’s handbook. Prentice-Hall, New Jersey

    Google Scholar 

  • Keppel G (1991) Design and analysis: a researcher’s handbook, 3rd edn. Prentice-Hall, New Jersey

    Google Scholar 

  • Khan MA, Ungar IA, Showalter AM (2000) The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. J Arid Environ 45:73–84

    Article  Google Scholar 

  • Laan P, Berrevoets MJ, Lythe S, Armstrong W, Blom CWPM (1989) Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species. J Ecol 77:693–703

    Article  Google Scholar 

  • Lang ARG (1967) Osmotic coefficients and water potentials of sodium chloride solutions from 0 to 40°C. Aust J Chem 20:2017–2023

    Article  CAS  Google Scholar 

  • Malcolm CV (1964) Effect of salt, temperature and seed scarification on germination of two varieties of Arthrocnemum halocnemoides. J Roy Soc West Aust 47:72–74

    Google Scholar 

  • McDonald M, Galwey NW, Ellneskog-Staam P, Colmer TD (2001) Evaluation of Lophopyrum elongatum as a source of genetic diversity to increase the waterlogging tolerance of hexaploid wheat (Triticum aestivum). New Phytol 151:369–380

    Article  Google Scholar 

  • Naidu BP (1998) Separation of sugars, polyols, proline analogues, and betaines in stressed plant extracts by high performance liquid chromatography and quantification by ultraviolet detection. Aust J Plant Physiol 25:793–800

    Article  CAS  Google Scholar 

  • O’Callaghan MO (1992) The ecology and identification of the southern African Salicornieae (Chenopodiaceae). S Afr J Bot 58:430–439

    Google Scholar 

  • Pedersen O, Vos H, Colmer TD (2006) Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata. Plant Cell Environ 29:1388–1399

    Article  PubMed  CAS  Google Scholar 

  • Poljakoff-Mayber A, Symon DE, Jones GP, Naidu BP, Paleg LG (1987) Nitrogenous compatible solutes in native South Australian plants. Aust J Plant Physiol 14:341–350

    CAS  Google Scholar 

  • Pujol JA, Calvo JF, Ramirez-Diaz L (2001) Seed germination, growth, and osmotic adjustment in response to NaCl in a rare succulent halophyte from southeastern Spain. Wetlands 21:256–264

    Article  Google Scholar 

  • Raskin I (1983) A method for measuring leaf volume, density, thickness and internal gas volume. HortSci 18:698–699

    Google Scholar 

  • Rich SM, Ludwig M, Colmer TD (2008) Photosynthesis in aquatic adventitious roots of the halophytic stem-succulent Tecticornia pergranulata (formerly Halosarcia pergranulata). Plant Cell Environ 31:1007–1016

    Article  PubMed  CAS  Google Scholar 

  • Rozema J, Van Der List JC, Schat H, Van Diggelin J, Broekman RA (1987) Ecophysiological response of Salicornia dolichostachya and Salicornia brachystachya to seawater inundation. In: Huiskes AHL, Blom CWPM, Rozema J (eds) Vegetation between land and sea. Dr. W. Junk Publishers, Dordrecht, pp 180–186

    Chapter  Google Scholar 

  • SaadEddin R, Doddema T (1986) Anatomy of the ‘extreme’ halophyte Arthrocnemum fruticosum (L.) Moq. in relation to its physiology. Ann Bot 57:531–544

    Google Scholar 

  • Schat H, Van Der List JC, Rozema J (1987) Ecological differentiation of the microspecies Salicornia dolichostachya Moss and Salicornia ramosissima J. Woods. In: Huiskes AHL, Blom CWPM, Rozema J (eds) Vegetation between land and sea. Dr. W. Junk Publishers, Dordrecht, pp 164–178

    Chapter  Google Scholar 

  • Shepherd K (2007) Three new species of Tecticornia (formerly Halosarcia) (Chenopodiaceae: Salicornioideae) from the Eremaean Botanical Province, Western Australia. Nuytsia 17:353–366

    Google Scholar 

  • Shepherd KA, Wilson PG (2007) Incorporation of the Australian genera Halosarcia, Pachycornia, Sclerostegia and Tegicornia into Tecticornia (Salicornioideae, Chenopodiaceae). Aust Syst Bot 20:319–331

    Article  Google Scholar 

  • Short DC, Colmer TD (1999) Salt tolerance in the halophyte Halosarcia pergranulata subsp. pergranulata. Ann Bot 83:207–213

    Article  CAS  Google Scholar 

  • Smith AM, Hylton CM, Koch L, Woolhouse HW (1986) Alcohol dehydrogenase activity in the roots of marsh plants in naturally waterlogged soils. Planta 168:130–138

    Article  CAS  Google Scholar 

  • Storey R, Wyn Jones RG (1979) Responses of Atriplex spongiosa and Suaeda monoica to salinity. Plant Physiol 63:156–162

    Article  PubMed  CAS  Google Scholar 

  • Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant Cell Environ 13:395–403

    Article  Google Scholar 

  • Ungar IA, Benner DK, McGraw DC (1979) The distribution and growth of Salicornia europaea on an inland salt pan. Ecology 60:329–336

    Article  Google Scholar 

  • Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledenous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245

    Article  Google Scholar 

  • Waters I, Morrell S, Greenway H, Colmer TD (1991) Effects of anoxia on wheat seedlings II. Influence of O2 supply prior to anoxia on tolerance to anoxia, alcoholic fermentation, and sugar levels. J Exp Bot 42:1437–1447

    Article  CAS  Google Scholar 

  • Western Australian Herbarium (1998–) FloraBase—The Western Australian Flora. Department of Environment and Conservation. http://florabase.dec.wa.gov.au/ (Accessed March 2011)

  • Wilson PG (1980) A revision of the Australian species of Salicornieae (Chenopodiaceae). Nuytsia 3:3–154

    Google Scholar 

Download references

Acknowledgements

Financial support for this research was provided by Normandy Mining Ltd, Placer Dome Inc, Acacia Resources Ltd, Kalgoorlie Consolidated Gold Mines (KCGM), Mineral and Energy Research Institute of Western Australia, and the Australian Research Council. Greg Barrett (formerly of KCGM) is thanked for suggesting studies of Tecticornia species at Hannan Lake and other ‘nearby’ salt lakes, and for enthusiastic support of this research. We thank Kelly Shepherd (WA Herbarium) for identification of Tecticornia plants used as seed parents in our research, and for comments on a draft of our manuscript. David Jasper is thanked for advice during this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy D. Colmer.

Additional information

Responsible Editor: Hans Lambers.

Appendix

Appendix

Table 3 P values and trends in variate responses determined via analysis of variance (one- and two-way, as appropriate), for Tecticornia pergranulata, T. indica and T. mellaria, grown in sub-irrigated or waterlogged sand culture at 10–800 mM NaCl for 60 d. Water-level treatments (WT) were sub-irrigated (SI) or waterlogging (WL)

Rights and permissions

Reprints and permissions

About this article

Cite this article

English, J.P., Colmer, T.D. Salinity and waterlogging tolerances in three stem-succulent halophytes (Tecticornia species) from the margins of ephemeral salt lakes. Plant Soil 348, 379–396 (2011). https://doi.org/10.1007/s11104-011-0924-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0924-6

Keywords

Navigation