A Reassessment of the Function of the So-Called Compatible Solutes in the Halophytic Plumbaginaceae Limonium latifolium  

Abstract

The compatible solute hypothesis posits that maintaining osmotic equilibrium under conditions of high salinity requires synthesis of organic compounds, uptake of potassium ions, and partial exclusion of NaCl. To assess whether osmotic adaptation in Limonium latifolium proceeds according to this hypothesis, a comprehensive analysis of solute accumulation during NaCl treatments was conducted. Determination of prevailing inorganic ions and establishment of the metabolic profiles for low M r organic substances revealed that contrary to the mentioned hypothesis the major contributors to osmolarity were constituted by inorganic solutes. Independent of salinity, only 25% of this osmolarity resulted from organic solutes such as Suc and hexoses. Proline (Pro), b-alanine betaine, and choline-O-sulfate were minor contributors to osmolarity. Compatible inositols also occurred, especially chiro-inositol, characterized for the first time in this species, to our knowledge. Principal component analysis showed that only a limited number of metabolic reconfigurations occurred in response to dynamic changes in salinity. Under such conditions only sugars, chiro-inositol, and Pro behave as active osmobalancers. Analysis of metabolic profiles during acclimatization to either mild salinity or nonsaline conditions showed that organic solute accumulation is predominantly controlled by constitutive developmental programs, some of which might be slightly modulated by salinity. Osmolarity provided under such conditions can be sufficient to maintain turgor in salinized seedlings. Compartmental analysis of Pro and b-alanine betaine in leaf tissues demonstrated that these solutes, mainly located in vacuoles under nonsaline conditions, could be partly directed to the cytosol in response to salinization. Thus they did not conform with the predictions of the compatible solute hypothesis.Due to either water loss or induced processes responsible for enhancement of the total number of osmotically active particles, higher plants are able to increase their osmolarity in response to hyperosmotic conditions. Accumulation of such particles, collectively termed osmolytes, contributes to osmotic adjustment (OA), which is needed for survival and resuming of growth at after-stress recovery. Active OA has been recognized as one of the key determinants of tolerance to salinity and other osmotic stresses encountered by higher plants (Jamaux et al., 1997). Inorganic and/or organic solutes could be involved in such function and depending on their origin, their production is associated with different energetic requirements partly responsible for inhibitory effects on growth rate. It is widely believed that osmolytes do not exert, per se, damaging effects on cell compartments where they are located.Primarily OA could be achieved with ions such as K 1 , Na 1 , NO 3 2 , or Cl 2 when available in the root environment (Shabala and Lew, 2002) through stressinduced activation of uptake and translocation of these substances. At the cellular level further accumulation of ...

Growth, sodium uptake and antioxidant responses of coastal plants differing in their ecological status under increasing salinity

“…Conversely, NaCl-treated L. latifolium plants accumulated less Na in their shoots at equivalent salinity levels. This result suggested that this plant possesses a better capacity to control the absorption of sodium ions and/or the excretion of such ions through its leaves, probably in relation to its high capacity to accumulate osmoregulatory solutes (Gagneul et al 2007). In addition, we observed the presence of salt crystals on both sides of L. latifolium leaves, proportionally to the salinity concentrations in the medium (data not shown).…”

Effects of Drought and Salinity on European Larch (Larix decidua Mill.) Seedlings

“…Also, field studies revealed only small fluctuations in GB contents in response to drastic changes in environmental conditions (i.e., in soil humidity and salinity) in some halophytes that use GB as the functional osmolyte [36]. These data suggest the existence of constitutive mechanisms of tolerance in plants adapted to stressful environments, based on changes in the intracellular location of specific osmolytes rather than on their de novo synthesis [79], and similar mechanisms could also operate in L. decidua.…”

Whole-Genome Mapping of Agronomic and Metabolic Traits to Identify Novel Quantitative Trait Loci in Bread Wheat Grown in a Water-Limited Environment

“…Similarly, the accumulation and maintenance of a high sugar pool containing nonreducing sugars and oligosaccharides has been reported to act as a replacement for water by providing a hydration shell around proteins. Although there is evidence from some previous studies that enhanced accumulation of Pro (Hong et al, 2000) and sugars (Hoekstra et al, 2001;Bogdan and Zagdanska, 2006;Urano et al, 2009) improves the osmotic stress tolerance of plants, there have also been reports that the accumulation of organic compatible solutes makes only minor contributions to osmotic stress tolerance (Gagneul et al, 2007;Hill et al, 2013). Here, metabolites of Glu and Pro metabolism (including Gln, Orn, Arg, and 5-oxo-Pro) and sugar metabolism (raffinose, Fru, and Glc) were highly genetically correlated with grain yield and other yield-related agronomic traits.…”