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barley (Widodo et al. 2009 ), and grapevine (Cramer et al. 2007 ) in addition to the
studies using the model organism A. thaliana (Kanani et al. 2010 ; Kim et al. 2007 ;
Gong et al. 2005 ). Major aspects of each study that need to be considered when at-
tempting to unify their results are the selected level of the salt stress and the duration
of the treatment. Treatment durations can be categorized into: (a) short term, i.e., up
to 24–30 h, (b) mid-term, i.e., from few days up to one week, and (c) long term, i.e.,
longer than one week up to few months.
Gavaghan et al. ( 2011 ) studied the mid-term responses of maize to high-salinity
(i.e., 50 and 150 mM NaCl) stress using NMR spectroscopy. They observed a
significantly increased concentration of sucrose, γ-aminobutyric acid (GABA),
glycine-betaine, and free amino acids, including alanine, in the roots of the salt-
stressed plants. The changes correlated with the salt concentration, suggesting thus
a response mechanism for the plants to maintain osmotic balance. The concentra-
tions of citrate, malate, succinate, and α-ketoglutarate declined in the shoot extracts
in response to the salinization. The depletion of these tricarboxylic acid (TCA)
cycle intermediates implies that the TCA cycle flux is reduced in the shoots as a
result of the salt stress, hence the plant growth and energy metabolism is slowed
down or arrested. Differences between the responses of salt tolerant and salt sensi-
tive cultivars to salinity stress were observed in rice plants after long-term treatment
with 100 mM NaCl (Zuther et al. 2007 ). Even the tolerant cultivars did not have
common responses to salinity stress, but formed physiological response subgroups.
One common response to salinity stress for most cultivars was the depletion of TCA
cycle intermediates, in agreement with the results of the previously described maize
study. Hence, both studies suggest that the acclimation to high salt concentrations
has a high demand for energy, competing thus with the plant growth.
Lu et al. studied the mid-term response to the salinity (i.e., 100 mM NaCl) stress
of two varieties of soybean using GC–MS and LC–MS metabolomics (Lu et al.
2013 ). In leaf samples from salt-stressed plants of both varieties, they observed a
significant reduction in the concentration of alanine, sucrose, and TCA cycle in-
termediates and a significant increase in the concentration of abscisic acid (ABA),
glycine, serine, and sugar alcohols, such as lactitol and maltitol, compared to the
control conditions. ABA is a plant hormone that accumulates under drought stress
and causes stomata closure. The ABA-induced stomata closure reduces transpira-
tion, thus preventing further water loss from the leaves in times of low water avail-
ability (Steuer et al. 1988 ). Sugar alcohols and amino acids can act as osmolytes and
their increase under salt stress is a response mechanism for the plants to maintain
osmotic balance, balancing the decreased water potential associated with the sodi-
um ion accumulation in the vacuoles and the extracellular volume, as stated above.
The reduction in the concentration of sucrose and TCA cycle intermediates suggests
the high energy cost for the acclimation to salinity stress that was observed in all rel-
evant studies discussed so far. The accumulation of osmolytes under salinity stress
has also been observed in grapevines after mid- and long-term treatment (Cramer
et al. 2007 ). The shoot concentrations of fructose, glucose, proline, glycine, and
malate increased in the salinized compared to the control plants. The observed in-
crease in the malate concentration was consistent with the significant increase in the
M.-E. P. Papadimitropoulos and M. I. Klapa