Halophytes are plants that can tolerate saline soils, and can complete their life cycle in soils with salinity concentrations above 200 mm NaCl (Flowers & Colmer, this issue, pp. 945–963). Some species require salt concentrations of this order for optimal growth, and grow poorly without it. The mechanisms that allow this remarkable adaptation are largely unknown, so the review by Flowers & Colmer is timely.
Halophytes constitute 1% of the world's flora, and are found in diverse taxonomic groups, and in a wide range of environments from arid land to coastal marshes. Many halophytes grow in waterlogged or flooded soils, and seagrasses are totally immersed in seawater. When salinity and waterlogging occur in combination, the effects on most plants can be severe (Barrett-Lennard, 2003), yet many halophytes can tolerate this combination. The mechanisms associated with flooding tolerance are the subject of the companion review by Colmer & Flowers, also in this issue (pp. 964–974).
‘It is curious that no monocotyledonous species is able to benefit from the presence of salinity to the same extent as dicotyledonous species.’
The species that are most tolerant of salinity, and show a marked growth improvement when the salinity increases, are all dicotyledonous species. It is curious that no monocotyledonous species is able to benefit from the presence of salinity to the same extent. This phenomenon has not been explained. Do dicotyledonous and monocotyledonous species use very different mechanisms? In their review, Flowers & Colmer stress the importance of choosing several contrasting ‘model’ species for further research into mechanisms of salinity tolerance, to cover the mechanistic diversity that exists across a spectrum of halophytes. However, we suggest that fastest progress can be made by initially focusing on comparisons between species that are genetically closely related but where one is tolerant of salinity and the other is not.
Differences between halophytes and glycophytes are illustrated in Fig. 1, using a pair of closely related monocotyledonous species and a pair of closely related dicotyledenous species. The examples chosen are wheat and its halophytic relative, and Arabidopsis and its halophytic relative. The typical monocotyledonous response is shown by the salt-sensitive wheat (Triticum aestivum) and the salt-tolerant tall wheatgrass (Thinopyrum ponticum). Moderate salinity reduces growth of both species, but higher salinities (over 150 mm NaCl) reveal differences (Fig. 1a). In contrast, a large difference between the salt-tolerant Thellungiella halophila and salt-sensitive Arabidopis thaliana is evident in low salinity, around 50 mm NaCl (Fig. 1b).
Thellungiella, although it is not especially salt-tolerant, appears to us to be the halophyte of choice as a model plant, owing to its fast generation time, ease of transformation, publicly available genetic information, and because, compared with most other halophytes, it is easy to grow in laboratory conditions. The growth of Thellungiella is illustrated as dropping markedly with increasing salinity in the comparative salinity tolerance diagram presented by Flowers & Colmer, particularly in comparison with other much more salt-tolerant species. However, a recent comparison between Thellungiella and Arabidopsis (Fig. 1b) shows a maintenance or slight increase in growth of Thellungiella when exposed to salinities of 50–100 mm NaCl, whereas the growth of Arabidopsis decreased significantly (Ghars et al., 2008). In the work of Ghars et al. (2008), plants were grown in sand under moderately high light intensities (400 µmol m−2 s−1), the salinity treatments were imposed when plants were 2 wk old, and lasted for 3 wk. These growth conditions are quite stringent, pointing to a clearly higher tolerance in Thellungiella over Arabidopsis at low to moderate salinity.
For a relatively mild treatment (50 or 75 mm NaCl), it is more likely that the difference in growth rate between these two species is the result of differing tolerance to the osmotic stress imposed by the salt outside the roots, rather than to a differing toxic effect of the salt within the plant. This could be tested by measuring daily the rate at which new leaves grow. Osmotic stress impacts on leaf growth immediately after the salt concentration around the roots increases above a threshold (approximately 40 mm NaCl for most species; Munns & Tester, 2008). By contrast, the impact of Na+ toxicity on leaf growth is delayed; Na+ accumulates to higher concentrations in fully expanded leaves than in expanding leaves, leads slowly to increased senescence of older leaves, and to the reduction in supply of photosynthate to the growing regions of the plant. The effects of this toxicity would have an impact on leaf growth only after injury occurs in older leaves (Munns & Tester, 2008). It would therefore be of interest to study the osmotic adjustment of Thellungiella in saline conditions, compared with Arabidopsis, looking at differences in maintenance of photosynthesis and stomatal conductance at these low concentrations of salinity (50 mm NaCl), and to investigate the expression in photosynthetic tissues of genes likely to be involved in the uptake of Na+ and Cl− into cells and in compartmentation of these ions in vacuoles (Munns, 2005).
Other than for comparisons with Thellungiella, the use of Arabidopsis to discover mechanisms and genes for salt tolerance seems questionable. Arabidopsis is sensitive to moderate concentrations of NaCl; and mechanisms of Na+ tolerance and Na+ accumulation in Arabidopsis are different to those in many crop species (Moller & Tester, 2007). It is more likely that novel and useful mechanisms for salt tolerance will be found by studying the mechanisms that already exist in plants that are tolerant to salinity, rather than studying what happens to a salt-sensitive plant when it is exposed to salt. Along a similar line, it is more likely that mechanisms for flooding tolerance will be found by studying a flooding-tolerant plant than a flooding-sensitive one.
Thellungiella may be the first halophyte of choice as a model for salt tolerance. However, studies of salt-tolerance mechanisms in Thellungiella may provide limited information to understand why plants such as Suaeda maritima require a saline solution to grow quickly, and reach their optimum growth rate in solutions of 150 mm NaCl or higher. Possible explanations for the high growth rate observed in many dicotyledonous halophytes in moderately, or even highly, saline conditions may include changes in biomass allocation between leaf, stem and root, maintenance of turgor (perhaps consequential on regulation of apoplastic ion concentrations), ability to accumulate sufficient nutrients or synthesize sufficient organic solutes, and minimization of energetic demands of ion transport.
Understanding how halophytes use Na+ to their advantage will undoubtedly be helpful in understanding the sensitivity of glycophytes, and in improving the salinity tolerance of crop plants.