Plant responses to heterogeneous salinity: agronomic relevance and research priorities.

BACKGROUND: Soil salinity, in both natural and managed environments, is highly heterogeneous, and understanding how plants respond to this spatiotemporal heterogeneity is increasingly important for sustainable agriculture in the era of global climate change. While the vast majority of research on crop response to salinity utilizes homogeneous saline conditions, a much smaller, but important, effort has been made in the past decade to understand plant molecular and physiological responses to heterogeneous salinity mainly by using split-root studies. These studies have begun to unravel how plants compensate for water/nutrient deprivation and limit salt stress by optimizing root-foraging in the most favourable parts of the soil. SCOPE: This paper provides an overview of the patterns of salinity heterogeneity in rain-fed and irrigated systems. We then discuss results from split-root studies and the recent progress in understanding the physiological and molecular mechanisms regulating plant responses to heterogeneous root-zone salinity and nutrient conditions. We focus on mechanisms by which plants (salt/nutrient sensing, root-shoot signalling and water uptake) could optimize the use of less-saline patches within the root-zone, thereby enhancing growth under heterogeneous soil salinity conditions. Finally, we place these findings in the context of defining future research priorities, possible irrigation management and crop breeding opportunities to improve productivity from salt-affected lands.

Mapping of novel salt tolerance QTL in an Excalibur × Kukri doubled haploid wheat population.

KEY MESSAGE: Novel QTL for salinity tolerance traits have been detected using non-destructive and destructive phenotyping in bread wheat and were shown to be linked to improvements in yield in saline fields. Soil salinity is a major limitation to cereal production. Breeding new salt-tolerant cultivars has the potential to improve cereal crop yields. In this study, a doubled haploid bread wheat mapping population, derived from the bi-parental cross of Excalibur × Kukri, was grown in a glasshouse under control and salinity treatments and evaluated using high-throughput non-destructive imaging technology. Quantitative trait locus (QTL) analysis of this population detected multiple QTL under salt and control treatments. Of these, six QTL were detected in the salt treatment including one for maintenance of shoot growth under salinity (QG(1-5).asl-7A), one for leaf Na+ exclusion (QNa.asl-7A) and four for leaf K+ accumulation (QK.asl-2B.1, QK.asl-2B.2, QK.asl-5A and QK:Na.asl-6A). The beneficial allele for QG(1-5).asl-7A (the maintenance of shoot growth under salinity) was present in six out of 44 mainly Australian bread and durum wheat cultivars. The effect of each QTL allele on grain yield was tested in a range of salinity concentrations at three field sites across 2 years. In six out of nine field trials with different levels of salinity stress, lines with alleles for Na+ exclusion and/or K+ maintenance at three QTL (QNa.asl-7A, QK.asl-2B.2 and QK:Na.asl-6A) excluded more Na+ or accumulated more K+ compared to lines without these alleles. Importantly, the QK.asl-2B.2 allele for higher K+ accumulation was found to be associated with higher grain yield at all field sites. Several alleles at other QTL were associated with higher grain yields at selected field sites.

Salinization of the soil solution decreases the further accumulation of salt in the root zone of the halophyte Atriplex nummularia Lindl. growing above shallow saline groundwater.

Water use by plants in landscapes with shallow saline groundwater may lead to the accumulation of salt in the root zone. We examined the accumulation of Na+ and Cl- around the roots of the halophyte Atriplex nummularia Lindl. and the impacts of this increasing salinity for stomatal conductance, water use and growth. Plants were grown in columns filled with a sand-clay mixture and connected at the bottom to reservoirs containing 20, 200 or 400 mM NaCl. At 21 d, Na+ and Cl- concentrations in the soil solution were affected by the salinity of the groundwater, height above the water table and the root fresh mass density at various soil depths (P < 0.001). However, by day 35, the groundwater salinity and height above the water table remained significant factors, but the root fresh mass density was no longer significant. Regression of data from the 200 and 400 mM NaCl treatments showed that the rate of Na+ accumulation in the soil increased until the Na+ concentration reached ~250 mM within the root zone; subsequent decreases in accumulation were associated with decreases in stomatal conductance. Salinization of the soil solution therefore had a feedback effect on further salinization within the root zone.

Hydraulic redistribution: limitations for plants in saline soils.

Hydraulic redistribution (HR), the movement of water from wet to dry patches in the soil via roots, occurs in different ecosystems and plant species. By extension of the principle that HR is driven by gradients in soil water potential, HR has been proposed to occur for plants in saline soils. Despite the inherent spatial patchiness and salinity gradients in these soils, the lack of direct evidence of HR in response to osmotic gradients prompted us to ask the question: are there physical or physiological constraints to HR for plants in saline environments? We propose that build-up of ions in the root xylem sap and in the leaf apoplast, with the latter resulting in a large predawn disequilibrium of water potential in shoots compared with roots and soil, would both impede HR. We present a conceptual model that illustrates how processes in root systems in heterogeneous salinity with water potential gradients, even if equal to those in non-saline soils, will experience a dampened magnitude of water potential gradients in the soil-plant continuum, minimizing or preventing HR. Finally, we provide an outlook for understanding the relevance of HR for plants in saline environments by addressing key research questions on plant salinity tolerance.

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

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.

The source of nitrogen (NH4+ or NO3-) affects the concentration of oxalate in the shoots and the growth of Atriplex nummularia (oldman saltbush).

Atriplex nummularia Lindl. (oldman saltbush) is a halophytic shrub used widely as a forage for ruminant production in saline farming systems. However, it can contain high concentrations of oxalate in the leaves, which may cause calcium deficiency in grazing animals. We hypothesised that supplying NH4+ instead of NO3- to a clone of this species would decrease oxalate concentrations in the shoots, and also decrease plant growth. Oxalate concentrations were measured in plants in the field, and a glasshouse experiment was conducted in which plants were grown with 10mM NO3- or NH4+, with 50, 200 or 500mM NaCl. The field survey showed effects of site (P<0.001), with average oxalate concentrations in shoots varying between 2.4 and 6.4% dry mass (DM). In the glasshouse, oxalate concentrations and plant growth were both affected by N-source and salinity (P<0.001). Averaged across salinities, plants grown with NH4+ for 24 days had only 43% of the shoot DM but 25% of the oxalate concentration of plants grown with NO3-. We discuss the effects of N-source on oxalate concentrations, the implications of this for halophyte growth, and the opportunity to select halophytes with lower oxalate and higher nutritive value for livestock.

Improvement of salt and waterlogging tolerance in wheat: comparative physiology of Hordeum marinum-Triticum aestivum amphiploids with their H. marinum and wheat parents.

Hordeum marinum Huds. is a waterlogging-tolerant halophyte that has been hybridised with bread wheat (Triticum aestivum L.) to produce an amphiploid containing both genomes. This study tested the hypothesis that traits associated with waterlogging and salinity tolerances would be expressed in H. marinum-wheat amphiploids. Four H. marinum accessions were used as parents to produce amphiploids with Chinese Spring wheat, and their responses to hypoxic and 200mM NaCl were evaluated. Relative growth rate (RGR) in the hypoxic-saline treatment was better maintained in the amphiploids (58-71% of controls) than in wheat (56% of control), but the amphiploids were more affected than H. marinum (68-97% of controls). In hypoxic-saline conditions, leaf Na+ concentrations in the amphiploids were lower than in wheat (30-41% lower) but were 39-47% higher than in the H. marinum parents. A strong barrier to radial oxygen loss formed in basal root zones under hypoxic conditions in two H. marinum accessions; this barrier was moderate in the amphiploids, absent in wheat, and was weaker for the hypoxic-saline treatment. Porosity of adventitious roots increased with the hypoxic treatments; values were 24-38% in H. marinum, 16-27% in the amphiploids and 16% in wheat. Overall, the amphiploids showed greater salt and waterlogging tolerances than wheat, demonstrating the expression of relevant traits from H. marinum in the amphiploids.

Plant responses to heterogeneous salinity: growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root zone.

Soil salinity is generally spatially heterogeneous, but our understanding of halophyte physiology under such conditions is limited. The growth and physiology of the dicotyledonous halophyte Atriplex nummularia was evaluated in split-root experiments to test whether growth is determined by: (i) the lowest; (ii) the highest; or (iii) the mean salinity of the root zone. In two experiments, plants were grown with uniform salinities or horizontally heterogeneous salinities (10-450 mM NaCl in the low-salt side and 670 mM in the high-salt side, or 10 mM NaCl in the low-salt side and 500-1500 mM in the high-salt side). The combined data showed that growth and gas exchange parameters responded most closely to the root-weighted mean salinity rather than to the lowest, mean, or highest salinity in the root zone. In contrast, midday shoot water potentials were determined by the lowest salinity in the root zone, consistent with most water being taken from the least negative water potential source. With uniform salinity, maximum shoot growth was at 120-230 mM NaCl; ~90% of maximum growth occurred at 10 mM and 450 mM NaCl. Exposure of part of the roots to 1500 mM NaCl resulted in an enhanced (+40%) root growth on the low-salt side, which lowered root-weighted mean salinity and enabled the maintenance of shoot growth. Atriplex nummularia grew even with extreme salinity in part of the roots, as long as the root-weighted mean salinity of the root zone was within the 10-450 mM range.

Aerenchymatous phellem in hypocotyl and roots enables O2 transport in Melilotus siculus.

• Aerenchymatous phellem (secondary aerenchyma) has rarely been studied in roots. Its formation and role in internal aeration were evaluated for Melilotus siculus, an annual legume of wet saline land. • Plants were grown for 21 d in aerated or stagnant (deoxygenated) agar solutions. Root porosity and maximum diameters were measured after 0, 7, 14 and 21 d of treatment. Phellem anatomy was studied and oxygen (O(2)) transport properties examined using methylene blue dye and root-sleeving O(2) electrodes. • Interconnecting aerenchymatous phellem developed in hypocotyl, tap root and older laterals (but not in aerial shoots), with radial intercellular connections to steles. Porosity of main roots containing phellem was c. 25%; cross-sectional areas of this phellem were threefold greater for stagnant than for aerated treatments. Root radial O(2) loss was significantly reduced by complete hypocotyl submergence; values approached zero after disruption of hypocotyl phellem below the waterline or, after shoot excision, by covering hypocotyl phellem in nontoxic cream. • Aerenchymatous phellem enables hypocotyl-to-root O(2) transport in M. siculus. Phellem increases radially under stagnant conditions, and will contribute to waterlogging tolerance by enhancing root aeration. It seems likely that with hypocotyl submerged, O(2) will diffuse via surface gas-films and internally from the shoot system.

Response to non-uniform salinity in the root zone of the halophyte Atriplex nummularia: growth, photosynthesis, water relations and tissue ion concentrations.

BACKGROUND AND AIMS: Soil salinity is often heterogeneous, yet the physiology of halophytes has typically been studied with uniform salinity treatments. An evaluation was made of the growth, net photosynthesis, water use, water relations and tissue ions in the halophytic shrub Atriplex nummularia in response to non-uniform NaCl concentrations in a split-root system. METHODS: Atriplex nummularia was grown in a split-root system for 21 d, with either the same or two different NaCl concentrations (ranging from 10 to 670 mm), in aerated nutrient solution bathing each root half. KEY RESULTS: Non-uniform salinity, with high NaCl in one root half (up to 670 mm) and 10 mm in the other half, had no effect on shoot ethanol-insoluble dry mass, net photosynthesis or shoot pre-dawn water potential. In contrast, a modest effect occurred for leaf osmotic potential (up to 30 % more solutes compared with uniform 10 mm NaCl treatment). With non-uniform NaCl concentrations (10/670 mm), 90 % of water was absorbed from the low salinity side, and the reduction in water use from the high salinity side caused whole-plant water use to decrease by about 30 %; there was no compensatory water uptake from the low salinity side. Leaf Na(+) and Cl(-) concentrations were 1.9- to 2.3-fold higher in the uniform 670 mm treatment than in the 10/670 mm treatment, whereas leaf K(+) concentrations were 1.2- to 2.0-fold higher in the non-uniform treatment. CONCLUSIONS: Atriplex nummularia with one root half in 10 mm NaCl maintained net photosynthesis, shoot growth and shoot water potential even when the other root half was exposed to 670 mm NaCl, a concentration that inhibits growth by 65 % when uniform in the root zone. Given the likelihood of non-uniform salinity in many field situations, this situation would presumably benefit halophyte growth and physiology in saline environments.