Tissue tolerance: an essential but elusive trait for salt-tolerant crops
Rana Munns A B C G , Richard A. James B , Matthew Gilliham D , Timothy J. Flowers A E and Timothy D. Colmer A FA School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B CSIRO Agriculture, GPO Box 1600, Canberra, ACT 2601, Australia.
C ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
D ARC Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, Australia.
E School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK.
F Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
G Corresponding author. Email: rana.munns@uwa.edu.au
Functional Plant Biology 43(12) 1103-1113 https://doi.org/10.1071/FP16187
Submitted: 21 May 2016 Accepted: 20 August 2016 Published: 12 October 2016
Abstract
For a plant to persist in saline soil, osmotic adjustment of all plant cells is essential. The more salt-tolerant species accumulate Na+ and Cl– to concentrations in leaves and roots that are similar to the external solution, thus allowing energy-efficient osmotic adjustment. Adverse effects of Na+ and Cl– on metabolism must be avoided, resulting in a situation known as ‘tissue tolerance’. The strategy of sequestering Na+ and Cl– in vacuoles and keeping concentrations low in the cytoplasm is an important contributor to tissue tolerance. Although there are clear differences between species in the ability to accommodate these ions in their leaves, it remains unknown whether there is genetic variation in this ability within a species. This viewpoint considers the concept of tissue tolerance, and how to measure it. Four conclusions are drawn: (1) osmotic adjustment is inseparable from the trait of tissue tolerance; (2) energy-efficient osmotic adjustment should involve ions and only minimal organic solutes; (3) screening methods should focus on measuring tolerance, not injury; and (4) high-throughput protocols that avoid the need for control plants and multiple Na+ or Cl– measurements should be developed. We present guidelines to identify useful genetic variation in tissue tolerance that can be harnessed for plant breeding of salt tolerance.
Additional keywords: barley, chickpea, chloride, osmoregulation, rice, sodium, wheat.
References
Adem GD, Roy SJ, Plett DC, 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 |
Adem GD, Roy SJ, Plett DC, Zhou M, Bowman JP, Shabala S (2015) Expressing AtNHX1 in barley (Hordeum vulgare L.) does not improve plant performance under saline conditions. Plant Growth Regulation 77, 289–297.
| Expressing AtNHX1 in barley (Hordeum vulgare L.) does not improve plant performance under saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmt12itL0%3D&md5=b2043f16359a8d71d49cc16584c3db34CAS |
Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany 86, 1–20.
| The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlSntL8%3D&md5=98213a0b80a421904fb5cbead41685bfCAS |
Ashraf M, McNeilly T (1990) Responses of four Brassica species to sodium chloride. Environmental and Experimental Botany 30, 475–487.
| Responses of four Brassica species to sodium chloride.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpvVGlug%3D%3D&md5=94b4c39e9a27d0130f7b964075e2548cCAS |
Ayers AD, Brown JW, Wadleigh CH (1952) Salt tolerance of barley and wheat in soil plots receiving several salinization regimes. Agronomy Journal 44, 307–310.
| Salt tolerance of barley and wheat in soil plots receiving several salinization regimes.Crossref | GoogleScholarGoogle Scholar |
Barkla BJ, Zingarelli L, Blumwald E, Smith JAC (1995) Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiology 109, 549–556.
Barragan V, Leidi EO, Andres Z, Rubio L, De Luca A, Fernandez JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. The Plant Cell 24, 1127–1142.
| Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmsl2jtL4%3D&md5=0386eaab23396a0b8dd28e181caaeb7cCAS | 22438021PubMed |
Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. The Plant Cell 23, 224–239.
| The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCmsrw%3D&md5=2e0d7b958f204d2cbd717ead7cb87ab1CAS | 21278129PubMed |
Besford RT, Maw GA (1976) Effect of potassium nutrition on some enzymes from tomato plant. Annals of Botany 40, 461–471.
Bonales-Alatorre E, Shabala S, Chen ZH, Pottosin I (2013) Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, Quinoa. Plant Physiology 162, 940–952.
| Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, Quinoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Oqs7g%3D&md5=0b5144f02b96923d169e3d3c9d1a6647CAS | 23624857PubMed |
Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context salinity stress tolerance. Journal of Experimental Botany 65, 1241–1257.
| ROS homeostasis in halophytes in the context salinity stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htbY%3D&md5=75f259e49c111146271aa61a36df1a47CAS | 24368505PubMed |
Boyer JS, James RA, Munns R, Condon AG, Passioura JB (2008) Osmotic adjustment may lead to anomalously low estimates of relative water content in wheat and barley. Functional Plant Biology 35, 1172–1182.
| Osmotic adjustment may lead to anomalously low estimates of relative water content in wheat and barley.Crossref | GoogleScholarGoogle Scholar |
Cheeseman JM (2013) The integration of activity in saline environments: problems and perspectives. Functional Plant Biology 40, 759–774.
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=8de0795123844635e118c78e34e66cecCAS |
Chen ZC, Yamaji N, Fujii-Kashino M, Ma JF (2016) A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice. Plant Physiology 171, 494–507.
| A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice.Crossref | GoogleScholarGoogle Scholar | 26983995PubMed |
Colmer TD, Epstein E, Dvorak J (1995) Differential solute regulation in leaf blades of various ages in salt-sensitive wheat and a salt-tolerant wheat × Lophopyrum elongatum (Host) A. Love amphiploid. Plant Physiology 108, 1715–1724.
Conn S, Gilliham M (2010) Comparative physiology of elemental distribution in plants. Annals of Botany 105, 1081–1102.
| Comparative physiology of elemental distribution in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVOqt74%3D&md5=6b56342ced31d012bc508a5418234999CAS | 20410048PubMed |
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JL (2014) Plant salt-tolerance mechanisms. Trends in Plant Science 19, 371–379.
| Plant salt-tolerance mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksVWmsb8%3D&md5=0e72eb61fed69684d0e9b09a857d0643CAS | 24630845PubMed |
Flowers TJ (1972) Salt tolerance in Suaeda maritima (L.) Dum. The effect of sodium chloride on growth respiration and soluble enzymes in a comparative study with Pisum sativum L. Journal of Experimental Botany 23, 310–321.
| Salt tolerance in Suaeda maritima (L.) Dum. The effect of sodium chloride on growth respiration and soluble enzymes in a comparative study with Pisum sativum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XksVGmurY%3D&md5=3945b52846c484ecffbb23bb7c6a741bCAS |
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=ead9e0f52d5a777986f79fa03e42e1abCAS | 18565144PubMed |
Flowers TJ, Yeo AR (1981) Variability of sodium chloride resistance within rice (Oryza sativa L.) varieties. New Phytologist 88, 363–373.
| Variability of sodium chloride resistance within rice (Oryza sativa L.) varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt12ksL8%3D&md5=07f6f660ac61f4f12e7ba55373004434CAS |
Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Australian Journal of Plant Physiology 13, 75–91.
| Ion relations of plants under drought and salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XitVeku7g%3D&md5=9d8e84bf15f60ba6ae57adde2fe770a9CAS |
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology 28, 89–121.
| The mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXksFSisb8%3D&md5=ff9530ae4f1e1531c9e3b6fb259b818cCAS |
Flowers TJ, Colmer TD, Munns R (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of Botany 115, 419–431.
| Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 25466549PubMed |
Fricke W, Leigh RA, Tomos AD (1994) Epidermal solute concentrations and osmolality in barley leaves studied at the single-cell level – changes along the leaf blade, during leaf ageing and NaCl stress. Planta 192, 317–323.
| Epidermal solute concentrations and osmolality in barley leaves studied at the single-cell level – changes along the leaf blade, during leaf ageing and NaCl stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtVajt7Y%3D&md5=f581fac279422bdb83b0e5950383d0b6CAS |
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Critical Reviews in Plant Sciences 18, 227–255.
| Salt tolerance and crop potential of halophytes.Crossref | GoogleScholarGoogle Scholar |
Gorham J, Wyn Jones RG, Bristol A (1990) Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat. Planta 180, 590–597.
| Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXitFequr4%3D&md5=a0316c00d06fc03d6853d8ebf9f4f0c0CAS | 24202105PubMed |
Greenway H, Munns R (1983) Interactions between growth and uptake of Cl– and Na+, and water relations of plants in saline environments. Plant, Cell & Environment 6, 575–589.
| Interactions between growth and uptake of Cl– and Na+, and water relations of plants in saline environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVeltQ%3D%3D&md5=b4840be89b6cb894cd3b315876cb1806CAS |
Greenway H, Osmond CB (1972) Salt responses of enzymes from species differing in salt tolerance. Plant Physiology 49, 256–259.
| Salt responses of enzymes from species differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xps1amtg%3D%3D&md5=cef8be26b31d81dbfeff75bdc64bed68CAS | 16657936PubMed |
Hajibagheri MA, Hall JL, Flowers TJ (1984) Stereological analysis of leaf cells of the halophyte Suaeda maritima (L.) Dum. Journal of Experimental Botany 35, 1547–1557.
| Stereological analysis of leaf cells of the halophyte Suaeda maritima (L.) Dum.Crossref | GoogleScholarGoogle Scholar |
Hedrich R (2012) Ion channels in plants. Physiological Reviews 92, 1777–1811.
| Ion channels in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2lsbnF&md5=323dbe2187f22cff95fc90b8177b6c85CAS | 23073631PubMed |
Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR, Tyerman SD, Walker RR, Gilliham M (2015) Grapevine and Arabidopsis cation-chloride cotransporters localise to the Golgi and trans-Golgi network and indirectly influence long-distance ion homeostasis and plant salt tolerance. Plant Physiology 169, 2215–2229.
Husain S, von Caemmerer S, Munns R (2004) Control of salt transport from roots to shoots of wheat in saline soil. Functional Plant Biology 31, 1115–1126.
| Control of salt transport from roots to shoots of wheat in saline soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWjt7fJ&md5=ce9800c4f8e778e8ef08e7684edcb178CAS |
Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends in Plant Science 16, 614–623.
| The role of mitochondrial respiration in salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVaqtLnM&md5=43bb52b3e312ebbcf8d498cd6c5c5551CAS | 21903446PubMed |
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=885d4c0f8d5d4ec7c124bc9bce60fc4fCAS |
James RA, Davenport RJ, Munns R (2006a) Physiological characterisation of two genes for Na+ exclusion in durum wheat: Nax1 and Nax2. Plant Physiology 142, 1537–1547.
| Physiological characterisation of two genes for Na+ exclusion in durum wheat: Nax1 and Nax2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCns7vI&md5=24874c800e7fa59e5b8491eb9de532ebCAS | 17028150PubMed |
James RA, Munns R, von Caemmerer S, Trejo C, Miller C, Condon AG (2006b) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl− in salt-affected barley and durum wheat. Plant, Cell & Environment 29, 2185–2197.
| Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl− in salt-affected barley and durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaisA%3D%3D&md5=3f8359f2f3ee6ce9cf6301a981d3f7b8CAS |
James RA, von Caemmerer S, Condon AG, 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=59992d44908cac0c061aadb434fac6e3CAS |
James RA, Blake C, Zwart AB, Hare RA, Rathjen AJ, Munns R (2012) Impact of ancestral wheat sodium exclusion genes Nax1 and Nax2 on grain yield of durum wheat on saline soils. Functional Plant Biology 39, 609–618.
| Impact of ancestral wheat sodium exclusion genes Nax1 and Nax2 on grain yield of durum wheat on saline soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVCmtL7N&md5=7e0fab933147882418360922728a2c41CAS |
Kebrom TH, Chandler PM, Swain SM, King RW, Richards RA, Spielmeyer W (2012) Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious internode development. Plant Physiology 160, 308–318.
| Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious internode development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlOmtLzK&md5=39c12262848f922b57fe6ecaea2384bcCAS | 22791303PubMed |
Khan HA, Siddique KHM, Munir R, Colmer TD (2015) Salt sensitivity in chickpea: growth, photosynthesis, seed yield components and tissue ion regulation in contrasting genotypes. Journal of Plant Physiology 182, 1–12.
| Salt sensitivity in chickpea: growth, photosynthesis, seed yield components and tissue ion regulation in contrasting genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptVSmurk%3D&md5=9d3ae4874475a689be9bb4f5bfdf7b53CAS | 26037693PubMed |
Khan HA, Siddique KHM, Colmer TD (2016) Salt sensitivity in chickpea is determined by sodium toxicity. Planta 244, 623–637.
| Salt sensitivity in chickpea is determined by sodium toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmslOit7w%3D&md5=12aa5401285ed00f237da0220240dc01CAS | 27114264PubMed |
Krebs M, Beyhl D, Gorlich E, Al-Rasheid KAS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis VATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences of the United States of America 107, 3251–3256.
| Arabidopsis VATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1Cgurw%3D&md5=db46065ed63941e1c4310cdf015a0df8CAS | 20133698PubMed |
Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytologist 189, 54–81.
| Sodium transport in plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGhug%3D%3D&md5=a025ecb1a12065fcec42b5c5667cfc23CAS | 21118256PubMed |
Kurniasih B, Greenway H, Colmer TD (2013) Tolerance of submerged germinating rice to 50–200 mM NaCl in aerated solution. Physiologia Plantarum 149, 222–233.
| Tolerance of submerged germinating rice to 50–200 mM NaCl in aerated solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCqtLbK&md5=e93da53f64e04571ea2d9eabc8a24763CAS | 23379468PubMed |
Leach RP, Wheeler KP, Flowers TJ, Yeo AR (1990) Molecular markers for ion compartmentation in cells of higher plants. II Lipid composition of the tonoplast of the halophyte Suaeda maritima (L.) Dum. Journal of Experimental Botany 41, 1089–1094.
| Molecular markers for ion compartmentation in cells of higher plants. II Lipid composition of the tonoplast of the halophyte Suaeda maritima (L.) Dum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVyns7g%3D&md5=f13c1e3c1d27349b3eb5c30b5f39ff99CAS |
Ledesma F, Lopez C, Ortiz D, Chen P, Korth KL, Ishibashi T, Zeng A, Orazaly M, Florez-Palacios L (2016) Simple greenhouse method for screening salt tolerance in soybean. Crop Science 56, 585–594.
| Simple greenhouse method for screening salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |
Maksimovic JD, Zhang JY, Zeng FR, Živanović BD, Shabala L, Zhou MX, Shabala S (2013) Linking oxidative and salinity stress tolerance in barley: can root antioxidant enzyme activity be used as a measure of stress tolerance? Plant and Soil 365, 141–155.
| Linking oxidative and salinity stress tolerance in barley: can root antioxidant enzyme activity be used as a measure of stress tolerance?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkslantLs%3D&md5=d8618b2f2afff7a4a1b4748d21440febCAS |
Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences of the United States of America 111, 6092–6097.
| Sugar demand, not auxin, is the initial regulator of apical dominance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtlWksbY%3D&md5=ae13739e7a191ad7f64b74e3f58102c8CAS | 24711430PubMed |
McCubbin T, Bassil E, Zhang S, Blumwald E (2014) Vacuolar Na+/H+ NHX-type antiporters are required for cellular K+ homeostasis, microtubule organization and directional root growth. Plants-Basel 3, 409–426.
| Vacuolar Na+/H+ NHX-type antiporters are required for cellular K+ homeostasis, microtubule organization and directional root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFKnsLbN&md5=1b0164398b85a273dd016e2a54d48e76CAS | 27135511PubMed |
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
| Reactive oxygen species homeostasis and signalling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hur8%3D&md5=42f2cbcf2143d1c8e9db6fbe95dfa198CAS |
Munns R (1985) Na+, K+ and Cl– in xylem sap flowing to shoots of NaCl-treated barley. Journal of Experimental Botany 36, 1032–1042.
| Na+, K+ and Cl– in xylem sap flowing to shoots of NaCl-treated barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXkvVGisb4%3D&md5=1223fcfa9e5ec7e06dc2d91c63a4bc76CAS |
Munns R (1988) Why measure osmotic adjustment? Australian Journal of Plant Physiology 15, 717–726.
| Why measure osmotic adjustment?Crossref | GoogleScholarGoogle Scholar |
Munns R, Gilliham M (2015) Salinity tolerance of crops – what is the cost? New Phytologist 208, 668–673.
| Salinity tolerance of crops – what is the cost?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs12lsrzF&md5=2f335d2d51fd319d9cf3ddcd06668140CAS | 26108441PubMed |
Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant and Soil 253, 201–218.
| Screening methods for salinity tolerance: a case study with tetraploid wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsbc%3D&md5=7e726238b806bda9e38e996ba14ece64CAS |
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=dd68a82a6d2c6414e1266213f98edac3CAS | 18444910PubMed |
Munns R, Guo J, Passioura JB, Cramer GR (2000) Leaf water status controls day-time but not daily rates of leaf expansion in salt-treated barley. Australian Journal of Plant Physiology 27, 949–957.
| Leaf water status controls day-time but not daily rates of leaf expansion in salt-treated barley.Crossref | GoogleScholarGoogle Scholar |
Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology 30, 360–364.
| Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlOgu7w%3D&md5=37d8f5975a0ce922abb720ad8cf03d8fCAS | 22407351PubMed |
Oertli JJ (1968) Extracellular salt accumulation, a possible mechanism of salt injury in plants. Agrochimica 12, 461–469.
Osmond CB, Greenway H (1972) Salt responses of carboxylation enzymes from species differing in salt tolerance. Plant Physiology 49, 260–263.
| Salt responses of carboxylation enzymes from species differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xot1OntA%3D%3D&md5=6a8b625419b989aa4460c7841c257e1fCAS | 16657937PubMed |
Polle A, Chen S (2015) On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant, Cell & Environment 38, 1794–1816.
| On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1yqsLnO&md5=0981fedbbaa58d0782a7d2f2a4200599CAS |
Poorter H, Buehler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Functional Plant Biology 39, 839–850.
| Pot size matters: a meta-analysis of the effects of rooting volume on plant growth.Crossref | GoogleScholarGoogle Scholar |
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Frontiers in Plant Science 5, 154
| Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling.Crossref | GoogleScholarGoogle Scholar | 24795739PubMed |
Pottosin I, Bonales-Alatorre E, Shabala S (2014) Choline but not its derivative betaine blocks slow vacuolar channels in the halophyte Chenopodium quinoa: Implications for salinity stress responses. FEBS Letters 588, 3918–3923.
| Choline but not its derivative betaine blocks slow vacuolar channels in the halophyte Chenopodium quinoa: Implications for salinity stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsF2murvP&md5=63ed8c59ffc6f3bb6341f3739ec94becCAS | 25240200PubMed |
Qiu L, Wu D, Ali S, Cai S, Dai F, Jin X, Wu F, Zhang G (2011) Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theoretical and Applied Genetics 122, 695–703.
| Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVCmurs%3D&md5=fbe7a6fb7c6f1ec9688919f1f7a25c3bCAS | 20981400PubMed |
Raven JA (1985) Regulation of pH and generation of osmolarity in vascular plants – a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytologist 101, 25–77.
| Regulation of pH and generation of osmolarity in vascular plants – a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFWjt7g%3D&md5=149c3f276cef7adc596af8a92bf66928CAS |
Reguera M, Bassil E, Tajima H, Wimmer M, Chanoca A, Otegui MS, Paris N, Blumwald E (2015) pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. The Plant Cell 27, 1200–1217.
| pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosFSjtbc%3D&md5=be123f11e0d2d087a49e144f13350d08CAS | 25829439PubMed |
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115–124.
| Salt resistant crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1Cns7c%3D&md5=7f9cbeb695826e06a98f986e76327527CAS | 24679267PubMed |
Setter TL, Waters I, Stefanova K, Munns R, Barrett-Lennard EG (2016) Salt tolerance, date of flowering and rain affect the productivity of wheat and barley on rainfed saline land. Field Crops Research 194, 31–42.
| Salt tolerance, date of flowering and rain affect the productivity of wheat and barley on rainfed saline land.Crossref | GoogleScholarGoogle Scholar |
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, Cuin T (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=e3b7086a1c0639a11d71b2068d781bd9CAS | 18724408PubMed |
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=0be98b691971716a3ef0e5235d525e71CAS |
Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiologia Plantarum 151, 257–279.
| Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXps1OjtL0%3D&md5=a0acade96ec4a194c130a751673c8ed0CAS | 24506225PubMed |
Sirault XRR, James RA, Furbank RT (2009) A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Functional Plant Biology 36, 970–977.
| A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOgs7rI&md5=e1ddc0bd079fca8d9a056b6b41c68b74CAS |
Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115, 433–447.
| Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 25564467PubMed |
Storey R, Pitman MG, Stelzer R, Carter C (1983) X-ray microanalysis of cells and cell compartments of Atriplex spongiosa. Journal of Experimental Botany 34, 778–794.
| X-ray microanalysis of cells and cell compartments of Atriplex spongiosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlslart7c%3D&md5=e0557bd2ae8fea77625ef3d86837d98fCAS |
Termaat A, Passioura JB, Munns R (1985) Shoot turgor does not limit shoot growth of NaCl-affected wheat and barley. Plant Physiology 77, 869–872.
| Shoot turgor does not limit shoot growth of NaCl-affected wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitFymsrs%3D&md5=8db6b000c8e902a7d59877bd879a8a96CAS | 16664152PubMed |
Walker RR, Blackmore DH, Clingeleffer PR, Correll RL (2004) Rootstock effects on salt tolerance of irrigated field-grown grapevines (Vitis vinifera L. cv. Sultana) 2. Ion concentrations in leaves and juice. Australian Journal of Grape and Wine Research 10, 90–99.
| Rootstock effects on salt tolerance of irrigated field-grown grapevines (Vitis vinifera L. cv. Sultana) 2. Ion concentrations in leaves and juice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVyku7c%3D&md5=9765a40fe57b3981628002cd2ed9e19bCAS |
Walter A, Liebisch F, Hund A (2015) Plant phenotyping: from bean weighing to image analysis. Plant Methods 11, 14
| Plant phenotyping: from bean weighing to image analysis.Crossref | GoogleScholarGoogle Scholar | 25767559PubMed |
Wolf O, Munns R, Tonnet ML, Jeschke WD (1991) The role of the stem in the partitioning of Na+ and K+ in salt-treated barley. Journal of Experimental Botany 42, 697–704.
| The role of the stem in the partitioning of Na+ and K+ in salt-treated barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvV2gur8%3D&md5=f983a97b8cc0f511e570f53c551f03c8CAS |
Wu H, Shabala L, Barry K, Zhou M, Shabala S (2013) Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiologia Plantarum 149, 515–527.
| Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslyhtLnL&md5=1665f79029b20a93683151c26f65a4c2CAS | 23611560PubMed |
Wu H, Shabala L, Zhou M, Stefano G, Pandolfi C, Mancuso S, Shabala S (2015) Developing and validating a high-throughput assay for salinity tissue tolerance in wheat and barley. Planta 242, 847–857.
| Developing and validating a high-throughput assay for salinity tissue tolerance in wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVGls7%2FP&md5=efede3ebb7e196041bbb49f51b02a0fcCAS | 25991439PubMed |
Wyn Jones G, Gorham J (2002) Intra- and inter-cellular compartmentation of ions – a study in specificity and plasticity. In ‘Salinity: environment – plants – molecules’. (Ed. A Lauchli, U Luttge) pp. 159–180. (Springer: Dordrecht, The Netherlands)
Yeo AR (1983) Salinity resistance: physiologies and prices. Physiologia Plantarum 58, 214–222.
| Salinity resistance: physiologies and prices.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktlGqsLw%3D&md5=59d2b07bf963eb2738661517bdcd6d3aCAS |
Yeo AR, Flowers TJ (1983) Varietal differences in the toxicity of sodium ions in rice leaves. Physiologia Plantarum 59, 189–195.
| Varietal differences in the toxicity of sodium ions in rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXmtV2qtLg%3D&md5=7b3223acafd3694309fa3f0f2ef691c2CAS |
Yeo AR, Flowers TJ (1986) Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Australian Journal of Plant Physiology 13, 161–173.
| Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils.Crossref | GoogleScholarGoogle Scholar |
Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theoretical and Applied Genetics 79, 377–384.
| Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7mt1Whug%3D%3D&md5=b55fd772da32967952e08ec886c37ee9CAS | 24226357PubMed |