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Potassium homeostasis and salinity tolerance in barley : physiological and genetic aspects

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Chen, Z (2008) Potassium homeostasis and salinity tolerance in barley : physiological and genetic aspects. PhD thesis, University of Tasmania.

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Abstract

Developing salt-tolerant crops is central to remediation of salinity affected land and to meet increasing global food demand. Salt tolerance is a polygenic trait involving multiple mechanisms, with contributions from genetic, developmental, physiological and environmental interactions. The molecular and physiological mechanisms of plant salt tolerance have been intensively investigated with most of the studies focused on detrimental effects of `Na^+`. Accordingly, most of the plant breeding for salt tolerance has been focused almost exclusively on excluding `Na^+` from uptake and/or transport to shoot. Salt-induced perturbations in `K^+` homeostasis are often recognised as being of secondary importance or even ignored by many researchers. This work argues that surmounting those constraints may open new avenues for breeding for salt-tolerant crops. Various plant physiological and genetic techniques were employed to test the hypothesis that the `K^+` retention in barley under saline conditions is central to maintain the cytosolic \(K^+/Na^+\) ratio and hence that salt-induced loss of `K^+` from seedling roots can be used for effective selection and breeding of salt-tolerant barley.
A comprehensive study was undertaken comparing whole-plant and cellular responses to salinity. Using seven barley cultivars contrasting in salt tolerance, a strong negative correlation was observed between the magnitude of `K^+` release from the roots of young seedlings and salt tolerance of mature plants judged by various physiological indices under saline conditions in glasshouse experiments. This suggested that `K^+` loss from the mature zone of intact 3-d old roots following 1 h pre-treatment with 80 mM NaCl can be used as a reliable screening indicator for salt tolerance in barley. A faster and more cost-effective procedure, based on the amount of `K^+` lost from plant roots during exposure to NaCl, was developed for rapid screening of large numbers of seedlings.
To confirm the suitability of `K^+` efflux trait as a screening method for breeding programmes, nearly 70 randomly selected barley cultivars were employed in glasshouse trials over two consecutive years to evaluate their responses to salinity. `K^+` loss under salt stress was measured from roots according to the above method. NaCl-induced `K^+` loss was found highly inversely correlated with relative grain yield, shoot biomass, plant height, net `CO_2` assimilation, survival rate, and thousand seed weight measured in the glasshouse experiments. Altogether, 60 out of 69 genotypes showed strong negative correlation (`r^2 > 0.6`) between the magnitude of `K^+` loss from roots of young seedlings and plant salt tolerance. Further analysis showed that a few remaining cultivars that did not follow the above trend, showed a superior ability to prevent `Na^+` accumulation in plant leaves and, thus, to maintain a higher cytosolic \(K^+/Na^+\) ratio despite the `K^+` loss.
A half diallel cross was made among six barley cultivars contrasting in salt tolerance for further understanding of the genetic behaviour of this trait. The variance (Vr) and covariance (Wr) analysis showed the existence of epistatic effects, which was confirmed by further tests using six different populations (parents, `F_1, F_2, BC_1 and BC_2`) from two different crosses. However, the tolerance was mainly controlled by additive effects with relatively smaller contributions from dominant and epistatic effects. A high heritability for salt tolerance based on salt-induced root `K^+` loss in barley was found, thereby supporting the use of this technique in breeding programmes. Given the fact that root `K^+` flux might be affected by a large number of other factors, the most reliable results are likely to be obtained while screening for salt tolerance of different genotypes or a doubled haploid population instead of segregating populations (e.g. when net ion fluxes are averaged between several samples).
Electrophysiological and biochemical techniques were also employed to investigate specific cellular mechanisms contributing to barley salt tolerance. It was found that, in salt-tolerant genotypes, multiple mechanisms are combined effectively in order to withstand saline conditions. These mechanisms include better control of membrane voltage, intrinsically higher `H^+` pump activity, greater ability of root cells to pump `Na^+` from the cytosol to the external medium or into the vacuoles, and higher sensitivity to supplemental `Ca^(2+)`. Meanwhile, no significant difference was found between salt-tolerant and -sensitive cultivars in their unidirectional \(^{22}Na^+\) influx or in the density and voltage dependence of depolarisation-activated outward-rectifying `K^+` channels (KORCs).
The impact of hydrogen peroxide (`H_2``0_2`) (one of components of salt stress) on `K^+` flux and the mitigating effects of glycine betaine and proline on NaCl-induced le loss were found to be significantly higher in salt-sensitive barley genotypes. Higher accumulation of leaf glycine betaine, proline, and total amino acid concentration was found in salt-sensitive cultivars under salinity stress. Significant negative correlations were observed between NaCl-induced `K^+` loss and leaf glycine betaine and proline concentration. Potassium was the main contributor to cytoplasmic osmolality in salt-tolerant genotypes, while in salt-sensitive ones glycine betaine and proline contributed substantially to cell osmolality, compensating for reduced cytoplasmic `K^+`.
In conclusion, I propose that (1) the ability to maintain high cytosolic \(K^+/Na^+\) ratio is the key feature for salt tolerance in barley; (2) multiple mechanisms and pathways control the high cytosolic \(IC/Na^+\) ratio in salt-tolerant barley, `K^+` retention appears to be central to this process; (3) hyperaccumulation of known compatible solutes in barley does not appear to play a major role in barley salt tolerance; (4) `K^+` efflux trait is highly inheritable; and (5) NaCl-induced `K^+` efflux can be used as a reliable and cost-effective early screening indicator for salt tolerance in addition to other known indices. Breeding for salt tolerance should therefore be achieved by targeting `K^+` homeostasis.

Item Type: Thesis (PhD)
Keywords: Barley
Copyright Information:

Copyright 2008 the author - The University is continuing to endeavour to trace the copyright owner(s) and in the meantime this item has been reproduced here in good faith. We would be pleased to hear from the copyright owner(s).

Additional Information:

Chapter 4 appears to be the equivalent of a peer reviewed version of the following article: Chen, Z., Newman, I.A., Zhou, M., Mendham, N.J., Zhang, G., Shabala, S.N., (2005) Screening plants for salt tolerance by measuring `K^+` flux: a case study for barley, Plant cell & environment, 28(10) 1230-1246, which has been published in final form at http://dx.doi.org/10.1111/j.1365-3040.2005.01364.x. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

Chapter 5 appears to be the equivalent of a post print version of an article published as: Chen, Z., Zhou, M., Newman, I.A., Mendham, N.J., Zhang, G., Shabala, S.N., (2007), Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance, Functional plant biology, 34(2) 150-162

Chapter 7 appears to be the equivalent of a post print version of an article published as: Chen, Z., Pottosin, I.I., Cuin, T.A., Fuglsang, A.T., Tester, M., Jha, D., Zepeda-Jazo, I., Zhou, M., Palmgren, M.G., Newman, I.A., Shabala, S. 2007, Root plasma membrane transporters controlling \(K^+/Na^+\) homeostasis in salt stressed barley, Plant physiology, 145(4) 1714-1725

Chapter 8 appears to be the equivalent of a a pre-copyedited, author-produced PDF of an article accepted for publication in Journal of experimental botany following peer review. The version of record (Chen, Z., Cuin, T.A., Zhou, M., Towmey, A., Naidu, B.P., Shabala, S. (2007), Compatible solute accumulation and stress mitigating effects in barley genotypes contrasting in their salt tolerance, Journal of experimental botany, 28(15-16) 4245-4255) is available at http://dx.doi.org/10.1093/jxb/erm284

Date Deposited: 25 Nov 2014 00:56
Last Modified: 23 Oct 2017 00:50
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