The integration of activity in saline environments: problems and perspectives

Abstract

Abstract. The successful integration of activity in saline environments requires flexibility of responses at all levels, from genes to life cycles. Because plants are complex systems, there is no 'best' or 'optimal' solution and with respect to salt, glycophytes and halophytes are only the ends of a continuum of responses and possibilities. In this review, I briefly examine seven major aspects of plant function and their responses to salinity including transporters, secondary stresses, carbon acquisition and allocation, water and transpiration, growth and development, reproduction, and cytosolic function and 'integrity'. I conclude that new approaches are needed to move towards understanding either organismal integration or 'salt tolerance', especially cessation of protocols dependent on sudden, often lethal, shock treatments and the embracing of systems level resources. Some of the tools needed to understand the integration of activity and even 'salt stress' are already in hand, such as those for whole-transcriptome analysis. Others, ranging from discovery studies of the nature of the cytosol to expanded tool kits for proteomic, metabolomic and epigenomic studies, still need to be further developed. After resurrecting the distinction between applied stress and the resultant strain and noting that with respect to salinity, the strain is manifest in changes at all -omic levels, I conclude that it should be possible to model and quantify stress responses.

Sodium as nutrient and toxicant

“…Indeed, on account of its physico-chemical similarity to K + , a role for Na + as a generic, "benign" osmoticum in plant vacuoles is especially plausible and reasonable. However, differences in chaotropic and lyotropic properties of the two ions in terms of their effects on water and molecular structure, while controversial (Mancinelli et al 2007;Galamba 2012), may yet emerge as important to toxicity manifestations in intracellular compartments (Cheeseman 2013), and as a foundation for the maintenance of a high cytosolic K + /Na + ratio, although this has not yet been investigated stringently. A good number of the studies listed in Tables 1, 2, and 3 supports this notion.…”

“…Interestingly, despite considerable effort, entry paths for Na + into roots have not as yet been successfully identified at the molecular level across taxonomic groups (Munns and Tester 2008;Zhang et al 2010;Kronzucker and Britto 2011;Cheeseman 2013), while a strong body of evidence has shown, at least in grasses, that one family of genes, HKT2 (formerly referred to as HKT1, but the latter designation is now reserved for a group of Na + transporters believed to be predominantly involved in intra-plant Na + transfer from root to shoot; Sunarpi et al 2005;Møller et al 2009), encodes transporters that can transport Na + at substantial rates across root plasma membranes, especially when K + is limiting (Horie et al 2001(Horie et al , 2011Laurie et al 2002;Munns and Tester 2008;Hauser and Horie 2010). This is instructive, given that Na + benefits tend to be at their most pronounced when K + is in short supply, and, indeed, Na + can assume some of the functions of K + .…”

“…From beet to chocolate: the classic literature-Na + benefits are common It has long been known that Na + can be of benefit to the growth of algae and cyanobacteria (Allen and Arnon 1955;Simonis and Urbach 1963;Brownell and Nicholas 1968), but, for higher plants, the reputation of the ion as a toxic one has held sway (Maathuis 2007;Munns and Tester 2008;Kronzucker and Britto 2011;Cheeseman 2013), and the vast majority of higher-plant literature on the ion has focused on this aspect, even though studies in a wide variety of species, including such important cultivated ones as tomato, potato, carrot, cacao, and cereals, have demonstrated the potential benefit of the ion for higher-plant growth as well (Wheeler and Adams 1905;Lehr 1941;Lehr and Wybenga 1955;Woolley 1957;Williams 1960;Brownell 1965;Brownell and Jackman 1966;Montasir et al 1966;El-Sheikh et al 1967;Hylton et al 1967;Draycott and Durrant 1976;Galeev 1990;Takahashi and Maejima 1998;Gattward et al 2012). It is important to emphasize that every substance has a threshold below which it is not toxic, in accordance with the "sola dosis facit venemum" (only the dose makes the poison) principle, famously attributed to Theophrastus Bombastus von Hohenheim (Paracelsus), but, for Na + , beneficial effects are seen well into the range of concentrations that would be considered high for ordinary nutrient ions, such as NO 3 − , NH 4 + , or K + , and, in the cases of halophytes, go far beyond that (Flowers and Colmer 2008).…”

“…It is common in complex toxicological syndromes to invoke a large number of causes, or confound causes and their effects. Manifold as the effects of Na + on critical processes such as photosynthesis, transpiration, production of reactive oxygen species and, ultimately, growth and yield, are (Bazihizina et al 2012;Cheeseman 2013), many, if not most, of these must be considered as downstream effects rather than primary causes of toxicity. There is no doubt that Na + , when appearing suddenly at high concentrations, in "shock" scenarios (see discussion in Cheeseman 2013), carries osmotic consequences that disrupt, typically temporarily, the membrane integrity of roots (Britto et al 2010;Coskun et al 2013), or also those of shoots, such as shown in rice (Flowers et al 1991), preceding, or perhaps coinciding with, more "ion-specific" effects (see later discussions).…”

“…For other, nonosmotic functions of K + , replacement by Na + may, however, not be as easily achieved. From the perspective of biochemical functions, such as in the cytoplasm, poorly characterized as it remains (Cheeseman 2013), there is believed to be a rather strict requirement for K + , and a strong maintenance of its concentration ; indeed, K + is considered essential for protein synthesis (Hall and Flowers 1973;Wyn Jones et al 1979) and oxidative phosphorylation (Flowers 1974), both of which are equally inhibited by Na + in glycophytes and halophytes (Greenway and Osmond 1972). More generally, K + is considered essential for the functioning of 50-60 enzymes (Leigh and Wyn-Jones 1986).…”