Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance

Zhonghua Chen A , Meixue Zhou C , Ian A. Newman B , Neville J. Mendham A , Guoping Zhang D and Sergey Shabala A E
+ Author Affiliations
- Author Affiliations

A School of Agricultural Science, University of Tasmania, GPO Box 252-54, Hobart, Tas. 7001, Australia.

B School of Mathematics and Physics, University of Tasmania, GPO Box 252-54, Hobart, Tas. 7001, Australia.

C TIAR, University of Tasmania, Kings Meadows, Tas. 7249, Australia.

D Department of Agronomy, Huajiachi Campus, Zhejiang University, Hangzhou 310029, China.

E Corresponding author. Email: Sergey.Shabala@utas.edu.au

Functional Plant Biology 34(2) 150-162 https://doi.org/10.1071/FP06237
Submitted: 25 September 2006  Accepted: 18 January 2007   Published: 12 February 2007

Abstract

A large-scale glasshouse trial, including nearly 70 barley cultivars (5300 plants in total), was conducted over 2 consecutive years to investigate plant physiological responses to salinity. In a parallel set of experiments, plant salt tolerance was assessed by non-invasive microelectrode measurements of net K+ flux from roots of 3-day-old seedlings of each cultivar after 1 h treatment in 80 mm NaCl as described in our previous publication (Chen et al. 2005). K+ flux from the root in response to NaCl treatment was highly (P < 0.001) inversely correlated with relative grain yield, shoot biomass, plant height, net CO2 assimilation, survival rate and thousand-seed weight measured in glasshouse experiments after 4–5 months of salinity treatment. No significant correlation with relative germination rate or tillering was found. In general, 62 out of 69 cultivars followed an inverse relationship between K+ efflux and salt tolerance. In a few cultivars, however, high salt tolerance (measured as grain yield at harvest) was observed for plants showing only modest ability to retain K+ in the root cells. Tissue elemental analysis showed that these plants had a much better ability to prevent Na+ accumulation in plant leaves and, thus, to maintain a higher K+/Na+ ratio. Taken together, our results show that a plant’s ability to maintain high K+/Na+ ratio (either retention of K+ or preventing Na+ from accumulating in leaves) is a key feature for salt tolerance in barley.

Additional keywords: Hordeum vulgare, ion flux, leaf elemental content, potassium, salinity, screening, sodium.


Acknowledgements

This work was supported by GRDC (UT8) and DEST grant to MZ and NM, ARC Discovery (DP0449856) and DEST grants to SS, and ARC Discovery (A00105708) grant to IN. We thank Dr Sarah Tavassoli, Mr Phil Andrews, and Mr Bill Peterson for their technical assistance and helpful suggestions.


References


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

Ashraf M, Khanum A (1997) Relationship between ion accumulation and growth in two spring wheat lines differing in salt tolerance at different growth stages. Journal Agronomy and Crop Science 178, 39–51.

Ashraf M, McNeilly T (1988) Variability in salt tolerance of nine spring wheat cultivars. Journal Agronomy and Crop Science 160, 14–21.

Badr A, Müller K, Schäfer-Pregl R, El Rabey H, Effgen S, Ibrahim HH, Pozzi C, Rohde W, Salamini F (2000) On the origin and domestication history of barley (Hordeum vulgare L.). Molecular Biology and Evolution 17, 499–510.
PubMed |


Carden DE, Diamond D, Miller AJ (2001) An improved Na+-selective microelectrode for intracellular measurements in plant cells. Journal of Experimental Botany 52, 1353–1359.
CrossRef | PubMed |

Cattivelli L, Baldi P, Crosatti C, Di Fonzo N, Faccioli P, Grossi M, Mastrangelo AM, Pecchioni N, Stanca AM (2002) Chromosome regions and stress-related sequences involved in resistance to abiotic stress in Triticeae. Plant Molecular Biology 48, 649–665.
CrossRef | PubMed |

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.
CrossRef |

Chhipa BR, Lal P (1995) Na+/K+ ratios as the basis of salt tolerance in wheat. Australian Journal of Agricultural Research 46, 533–539.
CrossRef |

Cuartero J, Bolarín MC, Asíns MJ, Moreno V (2006) Increasing salt tolerance in the tomato. Journal of Experimental Botany 57, 1045–1058.
CrossRef | PubMed |

Cuin TA, Miller AJ, Laurie SA, Leigh R (2003) Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54, 657–661.
CrossRef | PubMed |


Davenport RJ, Reid RJ, Smith FA (1997) Sodium–calcium interactions in two wheat species differing in salinity tolerance. Physiologia Plantarum 99, 323–327.
CrossRef |

Dubcovsky J, Santa Maria G, Epstein E, Luo MC, Dvorak J (1996) Mapping of the K+/Na+ discrimination locus Kna1 in wheat. Theoretical and Applied Genetics 92, 448–454.
CrossRef |

Dvořák J, Gorham J (1992) Methodology of gene transfer by homoeologous recombination into Triticum turgidum L. transfer of K+/Na+ discrimination from Triticum aestivum L. Genome 35, 639–646.

Dvořák J, Noaman MM, Goyal S, Gorham J (1994) Enhancement of the salt tolerance of Triticum turgidum L. by the Kna1 locus transferred from the Triticum aestivum L. chromosome 4D by homoeologous recombination. Theoretical and Applied Genetics 87, 872–877.

El-Hendawy SE, Hu Y, Schmidhalter U (2005) Growth, ion content, gas exchange, and water relations of wheat genotypes differing in salt tolerances. Australian Journal of Agricultural Research 56, 123–134.
CrossRef |

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
CrossRef | PubMed |


Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22, 875–884.

Foolad MR, Lin GY (1997) Absence of a genetic relationship between salt tolerance during seed germination and vegetative growth in tomato. Plant Breeding 116, 363–367.
CrossRef |

Garcia A, Rizzo CA, Ud-Din J, Bartos SL, Senadhira D, Flowers TJ, Yeo AR (1997) Sodium and potassium transport to the xylem are inherited independently in rice, and the mechanism of sodium : potassium selectivity differs between rice and wheat. Plant, Cell & Environment 20, 1167–1174.
CrossRef |

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.
CrossRef | PubMed |

Gaxiola R, de Larrinoa IF, Villalba JM, Serrano R (1992) A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO Journal 11, 3157–3164.
PubMed |


Gorham J, Hardy C, Wyn Jones RG, Joppa LR, Law CN (1987) Chromosomal location of a K+/Na+ discrimination character in the D genome of wheat. Theoretical and Applied Genetics 74, 584–588.
CrossRef |

Gorham J, Bristol A, Young EM, Wyn Jones RG, Kashour G (1990) Salt tolerance in the Triticeae: K+/Na+ discrimination in barley. Journal of Experimental Botany 41, 1095–1101.
CrossRef |

Gorham J, Bristol A, Young EM, Wyn Jones RG (1991) The presence of the enhanced K+/Na+ discrimination trait in diploid Triticum species. Theoretical and Applied Genetics 82, 729–736.
CrossRef |

Greenway H (1962) Plant response to saline substrates. I. Growth and ion uptake of several varieties of Hordeum during and after sodium chloride treatment. Australian Journal of Biological Sciences 15, 16–38.

Greenway H (1965) Plant responses to saline substrates. IV. Chloride uptake by Hordeum vulgare as affected by inhibitors, transpiration and nutrients in the medium. Australian Journal of Biological Sciences 18, 249–268.

Heenan DP, Lewin LG, McCaffery DW (1988) Salinity tolerance in rice varieties at different growth stages. Australian Journal of Experimental Agriculture 28, 343–349.
CrossRef |

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.
CrossRef |

Koyama ML, Levesley A, Koebner RMD, Flowers TJ, Yeo AR (2001) Quantitative trait loci for competent physiological traits determining salt tolerance in rice. Plant Physiology 125, 406–422.
CrossRef | PubMed |

Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theoretical and Applied Genetics 108, 253–260.
CrossRef | PubMed |

Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Functional Plant Biology 31, 1105–1114.
CrossRef |

Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiology 114, 591–596.
CrossRef | PubMed |

Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945.
CrossRef | PubMed |

Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Annals of Botany 84, 123–133.
CrossRef |

Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94, 263–272.
CrossRef |

Munns R, Hare RA, James RA, Rebetzke GJ (2000) Genetic variation for improving the salt tolerance of durum wheat. Australian Journal of Agricultural Research 51, 69–74.
CrossRef |

Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant and Soil 253, 201–218.
CrossRef |

Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
CrossRef | PubMed |

Newman IA (2001) Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant, Cell & Environment 24, 1–14.
CrossRef | PubMed |

Richards RA, Dennett CW, Qualset CO, Epstein E, Norlyn JD, Winslow MD (1987) Variation in yield of grain and biomass in wheat, barley and triticale in a salt-affected field. Field Crops Research 15, 277–287.
CrossRef |

Rodriguez-Navarro A (2000) Potassium transport in fungi and plants. Biochimica et Biophysica Acta 1469, 1–30.
PubMed |


Royo A, Aragüés R (1999) Salinity-yield response functions of barley genotypes assessed with a triple line source sprinkler system. Plant and Soil 209, 9–20.
CrossRef |

Royo A, Aragüés R, Playán E, Ortiz R (2000) Salinity-grain yield response functions of barley cultivars assessed with a drip-injection irrigation system. Soil Science Society of America Journal 64, 359–365.

Rus A, Lee BH, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiology 136, 2500–2511.
CrossRef | PubMed |

Sayed HI (1985) Diversity of salt tolerance in a germplasm collection of wheat (Triticum spp.). Theoretical and Applied Genetics 69, 651–657.
CrossRef |

Shabala L, Cuin TA, Newman IA, Shabala SN (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222, 1041–1050.
CrossRef | PubMed |

Shabala SN, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiology 113, 111–118.
PubMed |


Shabala SN, Shabala L, van Volkenburgh E (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 30, 507–514.
CrossRef |

Shannon MC , Noble CL (1990) Genetic approaches for developing economic salt tolerant crops. In ‘Agricultural salinity assessment and management. ACSE Manuals and reports on engineering practice No. 71’. (Ed KK Tanji) pp. 161–185. (ASCE: New York)

Skoog DA , West DM , Holler FJ , Crouch SR (2000) ‘Analytical chemistry: an introduction.’ 7th edn. (Saunders College Publishing: Philadelphia)

Slavich PG, Read BJ, Cullis BR (1990) Yield response of barley germplasm to field variation in salinity quantified using the EM-38. Australian Journal of Experimental Agriculture 30, 551–556.
CrossRef |

Storey R, Wyn Jones RG (1978) Salt stress and comparative physiology in the Gramineae. I. Ion relations of two salt- and water-stressed barley cultivars, California Mariout and Arimar. Australian Journal of Plant Physiology 5, 801–816.

Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant, Cell & Environment 27, 1–14.
CrossRef |

Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19, 765–768.
CrossRef | PubMed |

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 USA 98, 12832–12836.
CrossRef |

Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence of a critical role for potassium nutrition. The Plant Cell 10, 1181–1192.
CrossRef | PubMed |








Rent Article (via Deepdyve) Export Citation Cited By (139)