Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture
Halophytes of the lower coastal salt marsh show increased salt tolerance, and under high salinity they grow faster than upper marsh species. We could not show reduced growth rate of halophytes compared with glycophytes when grown under non-saline conditions. This indicates limited energy costs associated with high-salt tolerance in plants of genera such as Salicornia, providing a good perspective of saline agriculture cultivating Salicornia as a vegetable crop.We show that halophytes do not occur on non-saline or inland sites because of a reduced growth rate at low soil salinity, but probably due to other ecological traits of glycophytic upper marsh species. These traits provide competitive advantage over lower salt marsh halophytes, such as earlier germination and increased growing season length.Some halophytic Amaranthaceae (Salicornioideae, Chenopodioideae and Suaedoideae) are not just highly salt tolerant, their growth rate is stimulated at a salinity range of 150–300 mM NaCl. Alternatively this may be described as depressed growth at low salinity.Selective pressure for such high-salt tolerance and salt stimulated growth likely occurred with prevailing arid climate and saline soil conditions. Under such conditions highly-salt tolerant succulent Salicornioideae, Chenopodioidea and Suaedoideae may have evolved about 65 Mya. In the context of evolution and diversication of land plants this origin of highly-salt tolerant succulent plants is relatively recent.Such high-salt tolerance might be characterized as constitutive in comparison with inducible (lower) salt tolerance of other dicotyledonae and monocotyledonae (Poaceae) species. Levels of salt tolerance of the latter type span a large range of low, intermediate to high-salt tolerance, but do not include salt stimulated growth. Salt tolerant traits of the latter inducible type appear to have evolved repeatedly and independently.Early highly-salt tolerant succulent Salicornioideae, Chenopodioidea and Suaedoideae were perennial and frost sensitive and occurred in warm temperate and Mediterranean regions. A shift from the perennial Sarcocornia to an annual life form has been phylogenetically dated circa 9.4–4.2 Mya and enabled evolution of annual hygrohalophytes in more northern coastal locations up to boreal and subarctic coastal sites avoiding damage of winter frost. Diversification of such hygrohalophytes was facilitated by polyploidization (e.g. occurrence of tetraploid and diploid Salicornia species), and a high degree of inbreeding allowing sympatric occurrence of Salicornia species in coastal salt marshes.High-level salt tolerance is probably a very complex polygenic trait. It is unlikely that glycophytes would accommodate the appropriate allelic variants at all the loci involved in halophyte salt tolerance. This might explain why attempts to improve crop salt tolerance through conventional breeding and selection have been unsuccessful to date.Genetic engineering provides a viable alternative, but the choice for the appropriate transgenes is hampered by a fundamental lack of knowledge of the mechanisms of salt tolerance in halophytes. The chances to identify the determinant genes through QTL analyses, or comparisons among near isogenic lines (NILS) are limited. Salt-tolerance is usually a species-wide trait in halophytes, and intra-specific divergence in salt tolerance in facultative halophytes seems to be often associated with chromosomal incompatibility.A variety of candidate salt tolerance genes been identified in Arabidopsis thaliana, among which genes encoding Na+ and K+ transporters, and genes involved in the general stress or anti-oxidant response, or in compatible solute metabolism. Many of these genes have been over-expressed in different glycophytic hosts, which usually appeared to alleviate, to some degree, the response to high salinity levels. However, with few exceptions, there are no indications that the same genes would be responsible for the superior salt tolerance in (eu)halophytes. Comparisons of gene expression and gene promoter activity patterns between halophytes and glycophytes are, with few exceptions, virtually lacking, which is a major omission in current day salt tolerance research.Full-genome transcriptomic comparisons between halophytes and related glycophytes through deep sequencing seem to be the most promising strategy to identify candidate genetic determinants of the difference in salt tolerance between halophytes and glycophytes.The most reliable validation of any candidate gene is through silencing the gene in the halophytic genetic background, preferably down to the level at which it is expressed in the glycophyte reference species. This requires genetically accessible halophyte models, which are not available to date, with the exception of Thellungiella halophila. However, more models are required, particularly because T. halophila is not a typical halophyte. Eventually, the pyramiding of validated salt tolerance genes under suitable promoters may be expected to be a viable strategy for crop salt tolerance improvement.