Harnessing salt for woody biomass production

In medieval times, salt (sodium chloride, NaCl) was called ‘white gold’ because it was a costly commodity that was balanced with gold. Although salt has many positive usages and applications, it is currently considered more a threat than an asset. Soil salinization has endangered ancient as well as modern agriculture and forestry (Owens 2001). Inappropriate soil management practices have led to and continue to cause soil salinization. Reasons for salt accumulation include changes in the hydrological balance of soils caused by clearing of perennials and replacement by annual plants, as well as irrigation with salt-contaminated water and insufficient drainage in dry hot areas. Salt-affected soils can be found in almost all climatic regions, but the majority occur in arid and semiarid climatic regions (FAO 2009). Therefore, from a plant's perspective, water limitations due to lack of water or the unavailability of water from salty solutions and the accumulation of salt in the plant body with internal changes in the water balance are often co-occurring stresses. Consequences of these constraints are severe limitations on food and biomass production. Notably, even in very hot, dry and saline deserts some woody species exist, and these have obviously acquired specific measures to adapt to these hostile conditions. In this issue, Ma et al. (2011) report on an interesting example of stress adaptation, the succulent xerophyte Zygophyllum xanthoxylum. Zygophyllum xanthoxylum is a fodder shrub that colonizes arid areas in China and Mongolia (Flora of China Editorial Committee 1988–2013). Ma et al. (2011) show that this species responds to salt with increased growth, a feature typical for halophytes (Flowers et al. 1977) and moreover becomes more tolerant to drought in the presence of moderate salinity. They conducted detailed ecophysiological analyses to dissect the contribution of salt to the adjustment of the plant water balance in response to changes in the external conditions. The analyses of the different components of the forces acting within the plant and at the cellular level can be integrated into a growth model that sets a physiological framework for the observed responses (Figure 1). Scheme of different water and pressure regimes in a plant as a whole and in a single cell. Arrows indicate vectors for the direction and amount of osmotic potential (blue, negative values) and hydrostatic and mechanical pressure (red, positive values). Dots indicate osmotically active substances, (red, sodium ions; blue, compatible solutes, e.g., proline and sugars). C, control; D, drought; S, mild salt; D + S, drought and mild salt; ML, middle lamella; CW, cell wall; V, vacuole; CP, cytoplasm; ΨL, leaf water potential (≈ apoplastic water potential); ΨSC, osmotic potential, cytoplasm, ΨSV, osmotic potential, vacuole; ΠT, turgor pressure; PCW, cell wall pressure. Under unstressed conditions, cells adjust the osmotic potential of their cytoplasm (Ψsc) below that of the apoplast (≈ leaf water potential ΨL), thus maintaining a moderate positive turgor pressure (ΠT, Figure 1, C). In non-growing tissues, ΠT is almost completely compensated for by the mechanical cell wall pressure (PCW, Figure 1, C). Major osmo-regulators in this situation are usually potassium, other ions and organic solutes. Plants pre-adapted to saline soils such as Populus euphratica, Thellungiella halophila and sugar beet (Beta vulgaris) maintain high concentrations of sugars or other compatible solutes in leaves, even in the absence of stress (Zhao et al. 2009, Hoffmann 2010, Janz et al. 2010) and therefore have only a small requirement for the adjustment of osmotic pressure and stress signalling in response to salt (Amtmann 2009, Brinker et al. 2010, Ding et al. 2010, Qiu et al. 2011). Salt-adapted species such as Z. xanthoxylum and P. euphratica accumulate Na preferentially in the vacuole and not the cytosol (Ottow et al. 2005, Wu et al. 2011). Ma et al. (2011) showed elegantly that cellular ion uptake resulted in a strong increase in turgor pressure under mild salt stress compared with non-salt-exposed Z. xanthoxylum plants, because under these conditions, the decrease in cytosolic osmotic potential was stronger than the decrease in leaf water potential (Figure 1, S). We can suppose that the generation of this increased pressure is relatively ‘cheap’, since the cell can concentrate costly compatible solutes like sugars or proline in the cytoplasm counter-balancing Na in the vacuole (Figure 1, S). In fact, decreased organic solute concentrations were found in Z. xanthoxylum grown with mild salt stress (Cai et al. 2011), supporting the idea that Na can at least partly compensate for organic solutes. The increased turgor pressure due to Na may result in cell enlargement, a typical trait of succulents (Ogburn and Edwards 2010), if the mechanical pressure of the cell wall (PCW) is not correspondingly re-enforced. Indeed, long-term salt acclimation goes along with cell wall remodelling (Luo et al. 2009, Janz et al. 2011). Cell wall properties are important determinants of growth rate and shape (Winship et al. 2010). Naturally, in Z. xanthoxylum cytosolic osmotic potential (ΨSC) decreased more strongly under high than under mild salt stress but at the same time the leaf water potential (ΨL) also showed a much stronger decrease than that under mild salt stress (Ma et al. 2011). The resulting turgor (ΠT) was therefore similar to or even less than that under control conditions. Consequently, the cell cannot expand or may shrink, resulting in negative salt effects observed by Ma et al. (2011). Under drought conditions, the soil water potential is decreased, and the plant is forced to produce compatible solutes to maintain water uptake, both in the apoplast and in the cytoplasm. As a consequence, the turgor pressure in Z. xanthoxylum becomes lower than that under unstressed conditions, since the plant needs a low apoplastic water potential (ΨL) to minimize water loss by transpiration (Figure 1, D). The situation is similar to that under high salt stress, where the cells lack turgor-induced growth stimulus. While excessive salt accumulation may have negative effects on protein folding and thus disturb the cellular homeostasis, water loss due to drought with increased concentrations of ionic solutes in the cytoplasm may have similar consequences (Vinocur and Altman 2005). Besides, solute production for drought adaptation is an energy-intensive process that diverts carbon from biomass production. When drought stress is combined with weak saline conditions, it becomes easier and probably less costly for the plant to maintain positive turgor pressure. Just as without drought stress, sodium ions can be used as osmolytes in the vacuole, while compatible solutes can be efficiently concentrated in the cytoplasm (Figure 1, D + S). As a result, the plant is able to keep a lower leaf water potential than that under drought alone. This more negative water potential effects a lower vapour pressure in the spongy mesophyll, thus decreasing the transpiration rate and consequently increasing the amount of CO2 fixed per unit of water lost. Therefore, the plant is now able to maintain a higher turgor pressure than under water stress by itself, without excessive trade-off for solute production (Figure 1, D + S). This elegantly demonstrates the physiological background of a classic ecological model for plants like Z. xanthoxylum or P. euphratica that are adapted to saline conditions. The finding that Z. xanthoxylum can harness Na to rescue its performance under drought stress is exciting and opens new perspectives for the improvement of plants for biomass production in arid areas. Some molecular and mechanistic details required for Na translocation across different cellular membranes have already been unravelled for the woody species P. euphratica (Sun et al. 2009, Chen and Polle 2010). Salt-exposed trees like P. euphratica and mangroves, but also other crops such as soybean and cucumber, exhibited higher accumulation of Na together with other ions in the vacuole than in the cytosol (Ottow et al. 2005, Dabuxilatu and Ikeda 2005, Li et al. 2008). Since neither Z. xanthophyllum nor P. euphratica showed pronounced increases in organic osmolytes in response to salt (Li et al. 2005, Brinker et al. 2010), we must postulate redistribution and concentration of existing solutes in the cytosol for intracellular pressure balance. The identification of involved transporters and molecular cross-talk with Na uptake and allocation is expected to disclose novel pathways towards biotechnologically improved plants for arid areas that withstand drought by exploiting Na as an abundant and cheap osmolyte. The authors' laboratory is supported by the German Science Foundation (DFG), the European Communities (FP5, FP7) and the Federal State of Lower Saxony (Cluster of Excellence, Functional Biodiversity Research).