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Plant function and evolutionary biology
RESEARCH ARTICLE

Linking osmotic adjustment and stomatal characteristics with salinity stress tolerance in contrasting barley accessions

Min Zhu A , Meixue Zhou A , Lana Shabala A and Sergey Shabala A B
+ Author Affiliations
- Author Affiliations

A School of Land and Food, University of Tasmania, Private Bag 54, Hobart, Tas. 7001, Australia.

B Corresponding author. Email: sergey.shabala@utas.edu.au

Functional Plant Biology 42(3) 252-263 https://doi.org/10.1071/FP14209
Submitted: 30 July 2014  Accepted: 25 October 2014   Published: 27 November 2014

Abstract

Salinity tolerance is a complex trait – both physiologically and genetically – and the issue of which mechanism or trait has bigger contribution towards the overall plant performance is still hotly discussed in the literature. In this work, a broad range of barley (Hordeum vulgare L. and Hordeum spontaneum L.) genotypes contrasting in salinity stress tolerance were used to investigate the causal link between plant stomatal characteristics, tissue ion relations, and salinity tolerance. In total, 46 genotypes (including two wild barleys) were grown under glasshouse conditions and exposed to moderate salinity stress (200 mM NaCl) for 5 weeks. The overall salinity tolerance correlated positively with stomata density, leaf K+ concentration and the relative contribution of inorganic ions towards osmotic adjustment in the shoot. At the same time, no correlation between salinity tolerance and stomatal conductance or leaf Na+ content in the shoot was found. Taken together, these results indicate the importance of increasing stomata density as an adaptive tool to optimise efficiency of CO2 assimilation under moderate saline conditions, as well as benefits of the predominant use of inorganic osmolytes for osmotic adjustment in barley. Another finding of note was that wild barleys showed rather different strategies dealing with salinity, as compared with cultivated varieties.

Additional keywords: inorganic osmolytes, organic osmolytes, potassium, stomatal conductance, stomatal density, sodium.


References

Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R (2000) GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel. FEBS Letters 486, 93–98.
GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslGiu7c%3D&md5=afa326f834f369947474522f33a6e26cCAS | 11113445PubMed |

Adem GD, Rov SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biology 14, 113
Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 24774965PubMed |

Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. Journal of Plant Physiology 171, 670–687.
Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment.Crossref | GoogleScholarGoogle Scholar | 24635902PubMed |

Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sju7s%3D&md5=a1c4608d508967e7e35bb983cddc111cCAS | 10455050PubMed |

Asch F, Dingkuhn M, Dorffling K, Miezan K (2000) Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice. Euphytica 113, 109–118.
Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice.Crossref | GoogleScholarGoogle Scholar |

Bose J, Rodrigo-Moreno A, Shabala S (2014a) ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany 65, 1241–1257.
ROS homeostasis in halophytes in the context of salinity stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htbY%3D&md5=b93418d2e5beb62dab754351edae3988CAS | 24368505PubMed |

Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendia AM, Massart A, Poschenrieder C, Hariadi Y, Shabala S (2014b) Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+ –permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. Plant, Cell & Environment 37, 589–600.
Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+ –permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaksL4%3D&md5=b147ef0d2d53c89c323c88136c3b2236CAS |

Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L) and salt-sensitive (Phaseolus vulgaris L) C3 non-halophytes. Plant Physiology 95, 628–635.
Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L) and salt-sensitive (Phaseolus vulgaris L) C3 non-halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhsVSjtbw%3D&md5=407f22aaefd7afc57fbde57ad59b1b84CAS | 16668029PubMed |

Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science 168, 521–530.
The role of potassium in alleviating detrimental effects of abiotic stresses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFCntL8%3D&md5=4d34ccafd2d8c10326385055f036cbbaCAS |

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=d518f699f513ce256009b2ab5e133f11CAS |

Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shiabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. Journal of Experimental Botany 58, 4245–4255.
Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymurg%3D&md5=0f3f613e4f7400a80ade363670f5a4ddCAS | 18182428PubMed |

Chen Z, Shabala S, Mendham N, Newman I, Zhang G, Zhou M (2008) Combining ability of salinity tolerance on the basis of NaCl-induced K+ flux from roots of barley. Crop Science 48, 1382–1388.
Combining ability of salinity tolerance on the basis of NaCl-induced K+ flux from roots of barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslWqu7Y%3D&md5=c86f74fb18af89003ba399eae567d68aCAS |

Chérel I, Lefoulon C, Beoglin M, Sentenac H (2014) Molecular mechanisms involved in plant adaption to low K+ availability. Journal of Experimental Botany 65, 833–848.
Molecular mechanisms involved in plant adaption to low K+ availability.Crossref | GoogleScholarGoogle Scholar | 24293613PubMed |

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=683fdd9da07e2a7346c3f2878a1f5a95CAS | 18495637PubMed |

Ding MQ, Hou PC, Shen X, Wang MJ, Deng SR, Sun J, Xiao F, Wang RG, Zhou XY, Lu CF, Zhang DQ, Zheng XJ, Hu ZM, Chen SL (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Molecular Biology 73, 251–269.
Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKqsbs%3D&md5=391f4e703ba64f8258987397f75c6a2bCAS |

Dreyer I, Uozumi N (2011) Potassium channels in plant cells. The FEBS Journal 278, 4293–4303.
Potassium channels in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaksrbO&md5=33db5b7974763e41bdda7ddce4142ec1CAS | 21955642PubMed |

El-Hendawy SE, Ruan Y, Hu Y, Schmidhalter U (2009) A comparison of screening criteria for salt tolerance in wheat under field and controlled environmental conditions. Journal Agronomy & Crop Science 195, 356–367.
A comparison of screening criteria for salt tolerance in wheat under field and controlled environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WqsbvK&md5=35784647cc05a77546fa7ea0d009da52CAS |

FAO (2008) FAO land and plant nutrition management service. Available at http:www.fao.org/ag/agl/agll/spush [Verified 7 November 2014]

Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T, Struik PC (2012) The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Molecular Biology Reports 39, 6387–6397.
The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVCgsrc%3D&md5=43c48dc9296234d52912372e610e5a9cCAS | 22297690PubMed |

Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=5be89aeb6924a58f5526ed228831987eCAS | 18565144PubMed |

Freundl E, Steudle E, Hartung W (2000) Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis. Planta 210, 222–231.
Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVWqtQ%3D%3D&md5=b4f196a7e9af14158c3f5a956fd41315CAS | 10664128PubMed |

Garthwaite AJ, von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl– into the shoots. Journal of Experimental Botany 56, 2365–2378.
Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl into the shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahtLvJ&md5=fdcc50f3359189d3c9e4d7c1d9f1e602CAS | 16014366PubMed |

Greenway H (1963) Plant response to saline substrates. Australian Journal of Biological Sciences 16, 616–628.

Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annual Review of Plant Physiology and Plant Molecular Biology 31, 149–190.
Mechanisms of salt tolerance in non-halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWntb4%3D&md5=5d262e876e86d85e0964e30433f59621CAS |

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=15b93d8ee549d5d2cbe8070ed1f97468CAS | 15012199PubMed |

Hedrich R, Moran O, Conti F, Busch H, Becker D, Gambale F, Dreyer I, Kuch A, Neuwinger K, Palme K (1995) Inward rectifier potassium channels in plants differ from their animal counterparts in response to voltage and channel modulators. European Biophysics Journal 24, 107–115.
Inward rectifier potassium channels in plants differ from their animal counterparts in response to voltage and channel modulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtFyitA%3D%3D&md5=7e788502217725850aeaacaad7de919fCAS | 8582318PubMed |

Hose E, Steudle E, Hartung W (2000) Abscisic acid and hydraulic conductivity of maize root: a study using cell- and root-pressure probes. Planta 211, 874–882.
Abscisic acid and hydraulic conductivity of maize root: a study using cell- and root-pressure probes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVKnt7k%3D&md5=fd9ed0d1f5eeb25f50e78c4e476dee68CAS | 11144273PubMed |

Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. The Plant Journal 29, 649–659.
Salt causes ion disequilibrium-induced programmed cell death in yeast and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XislOhtr8%3D&md5=def78574e22296c36d27ef0cab2e0283CAS | 11874577PubMed |

Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard-cells precede stomatal movements. Proceedings of the National Academy of Sciences of the United States of America 89, 1790–1794.
Changes in cytosolic pH and calcium of guard-cells precede stomatal movements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xitlaitb0%3D&md5=68922bd7947ea1848d1fef5e1e57b235CAS | 11607281PubMed |

Islam S, Malik AI, Islam A, Colmer TD (2007) Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. Journal of Experimental Botany 58, 1219–1229.
Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlWjsbs%3D&md5=aeff094ca2dc6e415a2906331d2ef6dcCAS | 17283374PubMed |

James RA, Rivelli AR, Munns R, von Caemmerer S (2002) Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. Functional Plant Biology 29, 1393–1403.
Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFWhsA%3D%3D&md5=41ce6c9c5fd043184f493547f0d2606eCAS |

James RA, von Caemmerer S, Condon AGT, Zwart AB, Munns R (2008) Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Functional Plant Biology 35, 111–123.
Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVKktbY%3D&md5=4bd5bdf82d298e166e73f695b2520f13CAS |

Jiang Q, Roche D, Monaco TA, Hole D (2006) Stomatal conductance is a key parameter to assess limitations to photosynthesis and growth potential in barley genotypes. Plant Biology 8, 515–521.
Stomatal conductance is a key parameter to assess limitations to photosynthesis and growth potential in barley genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1ygsL4%3D&md5=d9adad08b1c9f22be1b2575db64571ecCAS | 16906488PubMed |

Leigh RA, Tomos AD (1993) Ion distribution in cereal leaves – pathways and mechanisms. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 341, 75–86.
Ion distribution in cereal leaves – pathways and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht12nurw%3D&md5=b674d77f3952b53d1587fe65e2ceb574CAS |

Li JY, Jiang AL, Chen HY, Wang Y, Zhang W (2007a) Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. Journal of Integrative Plant Biology 49, 1024–1031.
Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1Gqurw%3D&md5=e96cfd299ba9d608d57f0a76d5029bccCAS |

Li JY, Jiang AL, Zhang W (2007b) Salt stress-induced programmed cell death in rice root tip cells. Journal of Integrative Plant Biology 49, 481–486.
Salt stress-induced programmed cell death in rice root tip cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFOhtrw%3D&md5=a94b35640261e85f40e4ec0362539b9cCAS |

Liu JP, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiology 114, 591–596.
Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktVSks78%3D&md5=c2f9c81904f234530abcf030bddaaf13CAS |

Mian A, Oomen R, Isayenkov S, Sentenac H, Maathuis FJM, Very AA (2011) Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. The Plant Journal 68, 468–479.
Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCksrbK&md5=aba588dff9aa50027592971ca6979855CAS | 21749504PubMed |

Miedema H, Assmann SM (1996) A membrane-delimited effect of internal pH on the K+ outward rectifier of Vicia faba guard cells. The Journal of Membrane Biology 154, 227–237.
A membrane-delimited effect of internal pH on the K+ outward rectifier of Vicia faba guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXosFCq&md5=b8330545c4272557ac8900d733cb3921CAS | 8952952PubMed |

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=b0cf2c24ed0afbb17d466344b5ea8b75CAS |

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=7779a409bb17e45fbc90b71689d168ecCAS | 18444910PubMed |

Munns R, Schachtman DP, Condon AG (1995) The significance of a 2-phase growth-response to salinity in wheat and barley. Australian Journal of Plant Physiology 22, 561–569.
The significance of a 2-phase growth-response to salinity in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1erur0%3D&md5=9b0c08f7d063acd7ce4ab1de2700cb1dCAS |

Munns R, James RA, Sirault RR, Furbank RT, Jones HG (2010) New phenotyping methods for screening wheat and barley for beneficial response to water deficit. Journal of Experimental Botany 61, 3499–3507.
New phenotyping methods for screening wheat and barley for beneficial response to water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7jJ&md5=6f9e6930e1dbace6ecedad7099ab6ea6CAS | 20605897PubMed |

Nevo E, Chen G (2010) Drought and salt tolerance in wild relatives for wheat and barley improvement. Plant, Cell & Environment 33, 670–685.
Drought and salt tolerance in wild relatives for wheat and barley improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hu7g%3D&md5=08e8a3a4fe8a5c9e7d920b42ba71c21eCAS |

Oren A (1999) Bioenergetic aspects of halophilism. Microbiology and Molecular Biology Reviews 63, 334–348.

Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Carrasco KBR, 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. Functional Plant Biology 38, 818–831.
Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFymsL7M&md5=db26bc24397e0dbd8ae97dfa82da6149CAS |

Quintero JM, Fournier JM, Benlloch M, Rodriguez-Navarro A (2008) Na+ accumulation in root symplast of sunflower plants exposed to moderate salinity is transpiration-dependent. Journal of Plant Physiology 165, 1248–1254.
Na+ accumulation in root symplast of sunflower plants exposed to moderate salinity is transpiration-dependent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFeiu7nN&md5=350e594955750b811ce66f6b5a34f2c4CAS | 18166246PubMed |

Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment 32, 237–249.
Quantifying the three main components of salinity tolerance in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKlsL4%3D&md5=be7fa8c7201184ae233f7f55596b90a6CAS |

Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Australian Journal of Experimental Agriculture 42, 351–361.
Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview.Crossref | GoogleScholarGoogle Scholar |

Rengasamy P (2006) World salinization with emphasis on Australia. Journal of Experimental Botany 57, 1017–1023.
World salinization with emphasis on Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls74%3D&md5=04b0c44119d7537a2307e19a91731beeCAS | 16510516PubMed |

Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164, 151–162.
Effects of salt stress on the growth, ion content, stomatal behavior and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlGjs7o%3D&md5=a1ac57d7d8ac6d2575e2d32e83741a71CAS | 24249556PubMed |

Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell & Environment 25, 333–341.
Osmolyte accumulation: can it really help increase crop yield under drought conditions?Crossref | GoogleScholarGoogle Scholar |

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=b8c99fc5782436fc037f3537d096808bCAS | 14500326PubMed |

Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112, 1209–1221.
Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops.Crossref | GoogleScholarGoogle Scholar | 24085482PubMed |

Shabala S, Pottosin I (2014) Regulation potassium transport in plants under hostile condition: Implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257–279.
Regulation potassium transport in plants under hostile condition: Implications for abiotic and biotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXps1OjtL0%3D&md5=2a4b1212e8119b259f44513b5e2d6969CAS | 24506225PubMed |

Shabala S, Shabala L (2011) Ion transport and osmotic adjustment in plants and bacteria. Biomolecular Concepts 2, 407–419.
Ion transport and osmotic adjustment in plants and bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFejtrrP&md5=6040d31fa84d7a5f88b86872cf6c7930CAS |

Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou DW, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiologia Plantarum 146, 26–38.
Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWltb3E&md5=0b9b26cdcdd63a9c41cefc4e602e0230CAS | 22324972PubMed |

Shabala S, Hariadi Y, Jacobsen SE (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomata density. Journal of Plant Physiology 170, 906–914.
Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomata density.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFSrurk%3D&md5=56fc3088898743b2d2cd431381225d63CAS | 23485259PubMed |

Tavakkoli E, Fatehi F, Rengasamy P, McDonald GK (2012) A comparison of hydroponic and soil-based screening methods to identify salt tolerance in the field in barley. Journal of Experimental Botany 63, 3853–3867.
A comparison of hydroponic and soil-based screening methods to identify salt tolerance in the field in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSht7nO&md5=56a9e82c31a1e72e2bc22f2bb8375d81CAS | 22442423PubMed |

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyisbk%3D&md5=63bbf4f7ed27a81807b9f364ac50ba03CAS | 12646496PubMed |

Véry AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology 54, 575–603.
Molecular mechanisms and regulation of K+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 14503004PubMed |

Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G (2013) Tissue metabolic response to salt stress in wild and cultivated barley. PLoS ONE 8, e55431
Tissue metabolic response to salt stress in wild and cultivated barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1ylsb8%3D&md5=4ef85ee5ee025284654e380c06438435CAS | 23383190PubMed |

Wu H, Zhu M, Shabala L, Zhou M, Shabala S (2014) K+ retention in leaf mesophyll, an overlooked component of salinity tolerance mechanism: a case study for barley. Journal of Integrative Plant Biology
K+ retention in leaf mesophyll, an overlooked component of salinity tolerance mechanism: a case study for barley.Crossref | GoogleScholarGoogle Scholar | 25040138PubMed |

Yeo AR, Lee KS, Izard P, Boursier PJ, Flowers TJ (1991) Short-term and long-term effects of salinity on leaf growth in rice (Oryza sativa L). Journal of Experimental Botany 42, 881–889.
Short-term and long-term effects of salinity on leaf growth in rice (Oryza sativa L).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsl2msr0%3D&md5=0bcd46c359b1250fb8a220de52b1b6d0CAS |

Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19, 765–768.
Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslektLw%3D&md5=814706ae4d0099cfe4bdc9f13e49f9d0CAS | 11479571PubMed |

Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proceedings of the National Academy of Sciences of the United States of America 98, 12 832–12 836.
Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFahsLs%3D&md5=2e589816c4cf8c64f9e5b2f0f38ac3aeCAS |

Zhu JK, Liu JP, Xiong LM (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. The Plant Cell 10, 1181–1191.
Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFejt7g%3D&md5=f6835171164904d9d60cf4f8632b5cf3CAS | 9668136PubMed |