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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

The waterlogging/salinity interaction in higher plants revisited – focusing on the hypoxia-induced disturbance to K+ homeostasis

Edward G. Barrett-Lennard A C and Sergey N. Shabala B
+ Author Affiliations
- Author Affiliations

A Centre for Ecohydrology, School of Plant Biology and Department of Agriculture and Food of Western Australia (M084), The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B School of Agricultural Science and Tasmanian Institute of Agriculture, Hobart, Tas. 7001, Australia.

C Corresponding author. Email: egbarrettlennard@agric.wa.gov.au

This paper originates from a presentation at the COST WG2 Meeting ‘Putting halophytes to work – genetics, biochemistry and physiology’ Hannover, Germany, 28–31 August 2012.

Functional Plant Biology 40(9) 872-882 https://doi.org/10.1071/FP12235
Submitted: 8 August 2012  Accepted: 19 November 2012   Published: 11 January 2013

Abstract

Salinity and waterlogging (root-zone hypoxia) are abiotic stresses that often occur together on saltland. It is widely recognised that these two factors interact to increase Na+ and/or Cl concentrations in shoots, which can have adverse effects on plant growth and survival. This review expands on this understanding, providing evidence that the adverse effects of the interaction are also associated with a disturbance to plant K+ homeostasis. This conclusion is based on a comparative analysis of changes in ion concentrations and growth reported in the literature between species (glycophytes vs halophytes) and within a single species (Hordeum marinum L.). Comparisons between species show that hypoxia under saline conditions causes simultaneous increases in Na+ and Cl concentrations and decreases in K+ concentrations in shoots and that these changes can all be related to changes in shoot dry mass. Comparisons between accessions of a single species (Hordeum maritima L.) strengthen the argument, with increases in Na+ and decreases in K+ being related to decreases in shoot relative growth rate.

Additional keywords: chloride transport, ion transport, flooding, potassium transport, salinity, sodium transport.


References

Atwell BJ, Kriedemann PE, Turnbull CGN (1999) ‘Plants in action: adaptation in nature, performance in cultivation.’ (MacMillan Publishers: Melbourne)

Barrett-Lennard EG (1986) Effects of waterlogging on the growth and NaCl uptake by vascular plants under saline conditions. Reclamation and Revegetation Research 5, 245–261.

Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant and Soil 253, 35–54.
The interaction between waterlogging and salinity in higher plants: causes, consequences and implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsbk%3D&md5=a46fbd122186d4e690bf50aab4cd8500CAS |

Barrett-Lennard EG, Leighton PD, McPharlin IR, Setter T, Greenway H (1986) Methods to experimentally control waterlogging and measure soil oxygen in field trials. Australian Journal of Soil Research 24, 477–483.
Methods to experimentally control waterlogging and measure soil oxygen in field trials.Crossref | GoogleScholarGoogle Scholar |

Barrett-Lennard EG, Leighton PD, Buwalda F, Gibbs J, Armstrong W, Thomson CJ, Greenway H (1988) Effects of growing wheat in hypoxic nutrient solutions and of subsequent transfer to aerated solutions I. Growth and carbohydrate status of shoots and roots. Australian Journal of Plant Physiology 15, 585–598.
Effects of growing wheat in hypoxic nutrient solutions and of subsequent transfer to aerated solutions I. Growth and carbohydrate status of shoots and roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtlCht7o%3D&md5=8f15a6c7c0cdd5e8f3cb089e0114c423CAS |

Barrett-Lennard EG, van Ratingen P, Mathie MH (1999) The developing pattern of damage in wheat (Triticum aestivum L.) due to the combined stresses of salinity and hypoxia: experiments under controlled conditions suggest a methodology for plant selection. Australian Journal of Agricultural Research 50, 129–136.
The developing pattern of damage in wheat (Triticum aestivum L.) due to the combined stresses of salinity and hypoxia: experiments under controlled conditions suggest a methodology for plant selection.Crossref | GoogleScholarGoogle Scholar |

Belford RK, Cannell RQ, Thomson RJ, Dennis CW (1980) Effects of waterlogging at different stages of development on the growth and yield of peas (Pisum sativum L.). Journal of the Science of Food and Agriculture 31, 857–869.
Effects of waterlogging at different stages of development on the growth and yield of peas (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar |

Benjamin LR, Greenway H (1979) Effects of a range of O2 concentrations on porosity of barley roots and on their sugar and protein concentrations. Annals of Botany 43, 383–391.

Bennett SJ, Barrett-Lennard EG, Colmer TD (2009) Salinity and waterlogging as constraints to saltland pasture production: a review. Agriculture, Ecosystems & Environment 129, 349–360.
Salinity and waterlogging as constraints to saltland pasture production: a review.Crossref | GoogleScholarGoogle Scholar |

Buwalda F, Thomson CJ, Steigner W, Barrett-Lennard EG, Gibbs J, Greenway H (1988a) Hypoxia induces membrane depolarization and potassium-loss from wheat roots but does not increase their permeability to sorbitol. Journal of Experimental Botany 39, 1169–1183.
Hypoxia induces membrane depolarization and potassium-loss from wheat roots but does not increase their permeability to sorbitol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFSj&md5=0095b8ae779ecae3c0dabed33c67acd0CAS |

Buwalda F, Barrett-Lennard EG, Greenway H, Davies BA (1988b) Effects of growing wheat in hypoxic nutrient solutions and of subsequent transfer to aerated solutions II. Concentrations and uptake of nutrients and sodium in shoots and roots. Australian Journal of Plant Physiology 15, 599–612.
Effects of growing wheat in hypoxic nutrient solutions and of subsequent transfer to aerated solutions II. Concentrations and uptake of nutrients and sodium in shoots and roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtlCht7s%3D&md5=4b5aff4ee15e32b02c0b19302b8d0e7aCAS |

Cakirlar H, Bowling DJF (1981) The effect of salinity on the membrane-potential of sunflower roots. Journal of Experimental Botany 32, 479–485.
The effect of salinity on the membrane-potential of sunflower roots.Crossref | GoogleScholarGoogle Scholar |

Carter JL, Colmer TD, Veneklaas E (2006) Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes. New Phytologist 169, 123–134.
Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVygtL0%3D&md5=8be05b75a3cf47a6379da9af1ff00e27CAS |

Cheeseman JM, Hanson JB (1979) Energy linked potassium influx as related to cell potential in corn roots. Plant Physiology 64, 842–845.
Energy linked potassium influx as related to cell potential in corn roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlsFegtQ%3D%3D&md5=943942b0d9a9c89670b6a1fdce17009bCAS |

Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant, Cell & Environment 28, 1230–1246.
Screening plants for salt tolerance by measuring K+ flux: a case study for barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitbnE&md5=d4a2866c723373b2bcc92dee0536e657CAS |

Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytologist 179, 964–974.
Flooding tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqurzM&md5=42000ad7cdadbc6b288c74a91150d853CAS |

Contardi PJ, Davis RF (1978) Membrane-potential in Phaeoceros laevis – effects of anoxia, external ions, light, and inhibitors. Plant Physiology 61, 164–169.
Membrane-potential in Phaeoceros laevis – effects of anoxia, external ions, light, and inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtlensbg%3D&md5=9087bde1fbfeb2c4c4b886f602ef30b0CAS |

Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany 59, 2697–2706.
A root’s ability to retain K+ correlates with salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1WisLg%3D&md5=e0d0cf73b70e7579f1cb388799ae340dCAS |

De Boer AH, Volkov V (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant, Cell & Environment 26, 87–101.
Logistics of water and salt transport through the plant: structure and functioning of the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKrtLk%3D&md5=af33c1a02a68e408fe74e192ac07d827CAS |

Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFSqs7w%3D&md5=e6d9d391cb0668058f9488556bf96e8aCAS |

Demidchik V, Tester M (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiology 128, 379–387.
Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVSrur0%3D&md5=0371828737cdaf60941e2d91a6e80504CAS |

Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+ and K+-permeable channels in plant root cells. Journal of Cell Science 116, 81–88.
Free oxygen radicals regulate plasma membrane Ca2+ and K+-permeable channels in plant root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtF2lsA%3D%3D&md5=5bd9e2f3d8e19975c31ee2a8392bb5ecCAS |

Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. The Plant Journal 49, 377–386.
Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVyisLk%3D&md5=252bc33c2375ea34e20f6298997548cdCAS |

Drew MC, Guenther J, Läuchli A (1988) The combined effects of salinity and root anoxia on growth and net Na+ and K+-accumulation in Zea mays grown in solution culture. Annals of Botany 61, 41–53.

English JP (2004) Ecophysiology of salt- and waterlogging-tolerance in selected species of Halosarcia. PhD thesis, University of Western Australia.

Felle HH (2005) pH regulation in anoxic plants. Annals of Botany 96, 519–532.
pH regulation in anoxic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitLnK&md5=a353d320ad27ff18dacecd85194c1345CAS |

Galloway R, Davidson NJ (1993) The response of Atriplex amnicola to the interactive effects of salinity and hypoxia. Journal of Experimental Botany 44, 653–663.
The response of Atriplex amnicola to the interactive effects of salinity and hypoxia.Crossref | GoogleScholarGoogle Scholar |

Ghassemi F, Jakeman AJ, Nix HA (1995) ‘Salinisation of land and water resources: human causes, extent, management, and case studies.’ (CAB International: Wallingford, UK)

Grable AR (1966) Soil aeration and plant growth. Advances in Agronomy 18, 57–106.
Soil aeration and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXpsVahtg%3D%3D&md5=16e29d5158759dec778c2ddaf897255fCAS |

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=c67a7b95a8761aa0d533df99ebe4cd38CAS |

Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. The Plant Journal 27, 129–138.
Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsVyjtrg%3D&md5=df650b840e7335a191fa7461bb6e8a20CAS |

Jenkins S, Barrett-Lennard EG, Rengel Z (2010) Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on saltland with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves. Plant and Soil 329, 91–104.
Impacts of waterlogging and salinity on puccinellia (Puccinellia ciliata) and tall wheatgrass (Thinopyrum ponticum): zonation on saltland with a shallow water-table, plant growth, and Na+ and K+ concentrations in the leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFGlu7Y%3D&md5=db7f170e1256c0050c3fce1ded4b9562CAS |

John CD, Limpinuntana V, Greenway H (1977) Interaction of salinity and anaerobiosis in barley and rice. Journal of Experimental Botany 28, 133–141.
Interaction of salinity and anaerobiosis in barley and rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXktF2jtLk%3D&md5=852105b4d9a0d4d0bef8fb1ddda9c505CAS |

Kemp PJ, Peers C (2007) Oxygen sensing by ion channels. Essays in Biochemistry 43, 77–90.
Oxygen sensing by ion channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGqtbbL&md5=d2cca4ea9fe341e418dc20e078f7c919CAS |

Kriedemann PE, Sands R (1984) Salt resistance and adaptation to root-zone hypoxia in sunflower. Australian Journal of Plant Physiology 11, 287–301.
Salt resistance and adaptation to root-zone hypoxia in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlvFSmsrk%3D&md5=ad47132c353c9394197015a39157e32fCAS |

Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. The Plant Journal 32, 139–149.
A role for HKT1 in sodium uptake by wheat roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFGqsLk%3D&md5=646447762c8662e67a92fe8f3cbce9baCAS |

Linthurst RA (1979) The effect of aeration on the growth of Spartina alterniflora Loisel. American Journal of Botany 66, 685–691.
The effect of aeration on the growth of Spartina alterniflora Loisel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltVGhtLc%3D&md5=c95fd83ba6c4a6505ab39e6b08317c53CAS |

Linthurst RA, Seneca ED (1981) Aeration, nitrogen and salinity as determinants of Spartina alterniflora Loisel. growth response. Estuaries 4, 53–63.
Aeration, nitrogen and salinity as determinants of Spartina alterniflora Loisel. growth response.Crossref | GoogleScholarGoogle Scholar |

Malik AI, English JP, Colmer TD (2009) Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined. Annals of Botany 103, 237–248.
Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFCktbc%3D&md5=2dfba4634434084198c78fff1a9e2ed0CAS |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=4b241e0ff1eba2f3fa3d1e323ab7e87aCAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=0ce1f7aad22c73fffb329d4603f0e836CAS |

Munns R, Greenway H, Kirst GO (1983) Halotolerant eukaryotes. In ‘Encyclopedia of plant physiology. Vol. 12C’. (Eds. OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 59–135. (Springer-Verlag: Berlin)

Naidoo G (1985) Effects of waterlogging and salinity on plant-water relations and on the accumulation of solutes in three mangrove species. Aquatic Botany 22, 133–143.
Effects of waterlogging and salinity on plant-water relations and on the accumulation of solutes in three mangrove species.Crossref | GoogleScholarGoogle Scholar |

Naidoo G, Kift J (2006) Responses of the saltmarsh rush Juncus kraussii to salinity and waterlogging. Aquatic Botany 84, 217–225.
Responses of the saltmarsh rush Juncus kraussii to salinity and waterlogging.Crossref | GoogleScholarGoogle Scholar |

Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. Journal of Experimental Botany 61, 1205–1213.
Intracellular consequences of SOS1 deficiency during salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1Wnsbo%3D&md5=f91c01cba744ca28c69c45818ed4f2b3CAS |

Ponnamperuma FN (1972) The chemistry of submerged soils. Advances in Agronomy 24, 29–96.
The chemistry of submerged soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXhtVOju7c%3D&md5=d8d7f894e2159a5a94014ca834ada1faCAS |

Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiology 132, 1041–1052.
Na+/H+ exchange activity in the plasma membrane of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslertbY%3D&md5=a359344236258319840a296b82b00275CAS |

Qureshi RH, Barrett-Lennard EG (1998) Saline agriculture for irrigated land in Pakistan: a handbook. Monograph No. 50. Australian Centre for International Agricultural Research, Canberra, ACT.

Roberts SK, Tester M (1995) Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. The Plant Journal 8, 811–825.
Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XosFaitQ%3D%3D&md5=52554f13ec19fd3d29848c57bc0cf2b3CAS |

Rozema J, Blom B (1977) Effects of salinity and inundation on the growth of Agrostis stolonifera and Juncus gerardii. Journal of Ecology 65, 213–222.
Effects of salinity and inundation on the growth of Agrostis stolonifera and Juncus gerardii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhs12qsLY%3D&md5=8f2a45f3911860b0ebc771bba7bfad60CAS |

Shabala S (2003) Regulation of potassium transport in leaves: from molecular to tissue level. Annals of Botany 92, 627–634.
Regulation of potassium transport in leaves: from molecular to tissue level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVOnsbw%3D&md5=15b8b0fc40a9e5f4f4012311ff4cce07CAS |

Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit70%3D&md5=b00298e506b7189fc2da0a5277d6448aCAS |

Shabala S, Mackay A (2011) Ion transport in halophytes. Advances in Botanical Research 57, 151–199.
Ion transport in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1Sit74%3D&md5=d86d24c3774e60f11dc40546278fcb8fCAS |

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 Physiology 141, 1653–1665.
Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitbo%3D&md5=9cf8fa017b3c4ebb820d7488c42c9af4CAS |

Shabala S, Cuin TA, Prismall L, Nemchinov LG (2007) Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 227, 189–197.
Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyku7zF&md5=7ed37a5336dc0d5deaae9a25fd9b7e23CAS |

Shi HZ, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences of the United States of America 97, 6896–6901.
The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFahtrs%3D&md5=55efc6e21ef49d2fa4b8ba59e5aa88d8CAS |

Smethurst CF, Rix K, Garnett T, Auricht G, Bayart A, Lane P, Wilson SJ, Shabala S (2008) Multiple traits associated with salt tolerance in lucerne: revealing the underlying cellular mechanisms. Functional Plant Biology 35, 640–650.
Multiple traits associated with salt tolerance in lucerne: revealing the underlying cellular mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrsrrN&md5=53741c8e22eb84b27f55e8737554cad2CAS |

Stelzer R, Läuchli A (1977) Salz- und Ǘberflutungstoleranz von Puccinellia peisonis. I. Der Einfluss von NaCl-und KCl-Salinität auf das Wachstum bei varitierter Sauerstoffversorgung der Würzel. Zeitschrift für Pflanzenphysiologie 83, 35–42.

Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis. Plant and Soil 289, 369–383.
Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1WnsrjP&md5=0add669e521ef3ae43938695817f2119CAS |

Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant, Cell & Environment 13, 395–403.
Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat.Crossref | GoogleScholarGoogle Scholar |

Trought MCT, Drew MC (1980) The development of waterlogging damage in young wheat plants in anaerobic solution cultures. Journal of Experimental Botany 31, 1573–1585.
The development of waterlogging damage in young wheat plants in anaerobic solution cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlKgt7o%3D&md5=a747f4c87bed83bb749e8a95ea2d4d62CAS |

Véry AA, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends in Plant Science 7, 168–175.
Cation channels in the Arabidopsis plasma membrane.Crossref | GoogleScholarGoogle Scholar |

Visser EJW, Voesenek L (2005) Acclimation to soil flooding – sensing and signal-transduction. Plant and Soil 274, 197–214.
Acclimation to soil flooding – sensing and signal-transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurfI&md5=32f984e46744ad917a9ee986bf57ff4dCAS |

Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant, Cell & Environment 32, 486–496.
Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVantbk%3D&md5=1ae1a2b5136cf9dfd43981cdc37fc5aeCAS |

Wegner LH, De Boer AH (1997) Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long-distance signaling. Plant Physiology 115, 1707–1719.

Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots – a procedure to isolate protoplasts from this tissue and a patch-clamp exploration of salt passageways into xylem vessels. Plant Physiology 105, 799–813.

Wesseling J, van Wijk WR (1957) Land drainage in relation to soils and crops. I. Soil physical conditions in relation to drain depth. In ‘Drainage of agricultural lands’. (Ed. JN Luthin) pp. 461–504. (American Society of Agronomy: Madison, WI)

West DW, Black JDF (1978) Irrigation timing – its influence on the effects of salinity and waterlogging stresses in tobacco plants. Soil Science 125, 367–376.
Irrigation timing – its influence on the effects of salinity and waterlogging stresses in tobacco plants.Crossref | GoogleScholarGoogle Scholar |

West DW, Taylor JA (1980a) The effect of temperature on salt uptake by tomato plants with diurnal and nocturnal waterlogging of salinized rootzones. Plant and Soil 56, 113–121.
The effect of temperature on salt uptake by tomato plants with diurnal and nocturnal waterlogging of salinized rootzones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlsVyqt7c%3D&md5=2ce0732e0c0ae58a14c4c7a43dc58495CAS |

West DW, Taylor JA (1980b) The response of Phaseolus vulgaris L. to root-zone anaerobiosis, waterlogging and high sodium chloride. Annals of Botany 46, 51–60.

West DW, Taylor JA (1984) Response of six grape cultivars to the combined effects of high salinity and rootzone waterlogging. Journal of the American Society for Horticultural Science 109, 844–851.

Wetson AM, Flowers TJ (2010) The effect of saline hypoxia on growth and ion uptake in Suaeda maritima. Functional Plant Biology 37, 646–655.
The effect of saline hypoxia on growth and ion uptake in Suaeda maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVGnsrY%3D&md5=956a633df337ba1d13c86991c28fc40eCAS |

Wetson AM, Zörb C, John EA, Flowers TJ (2012) High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis. Annals of Botany 109, 1029–1036.
High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis.Crossref | GoogleScholarGoogle Scholar |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbc%3D&md5=f20f5493d7e57fe0984b2dba9a510739CAS |