Life presumably arose in the primeval oceans (with similar or even greater salinity
than present ocean—Knauth, 1998), so the ancient cells were designed to withstand
salinity. However, for the plants to “land,” their immediate ancestors most likely
lived in fresh, or slightly brackish, water. These algae already developed roots/rhizoids
to obtain nutrients from the substrate and did not face hyper-salinity, as well as
air exposure, in a drying pond (Raven and Edwards, 2001; Flowers et al., 2010). The
fresh/brackish water origins might explain why many land plants, including some cereals,
can withstand moderate salinity, but only 1–2% of all the higher plant species survive
at salinities close to that of seawater (Santos et al., 2016). Salt tolerance does
not have a firm dividing line: 80 mM NaCl is usually taken as a stress threshold and
200 mM NaCl as the halophyte territory (compare to ~470 mM NaCl content of the modern
seawater). However, plants have re-discovered their saline origins in more than 70
independent halophytic lines (Bennett et al., 2013).
Salinity is among the major threats to agriculture, having been one of the reasons
for the demise of the ancient Mesopotamian Sumer civilization (Jacobsen and Adams,
1958) and in the present time causing huge annual economic losses of over 10 billion
USD (this figure exceeds the gross domestic product of more than 50 less-developed
countries of the modern world—Qadir et al., 2014). The effects of salinity on plants
include osmotic stress, disruption of membrane ion transport, direct toxicity of high
cytoplasmic concentrations of sodium and chloride on cellular processes and induced
oxidative stress. Ion transport is the crucial starting point that determines salinity
tolerance in plants: this includes the cation and anion transport across the plasma
membranes of the root cells, the transport through the vacuolar membranes, the long-distance
ion transport via xylem and phloem and the salt excretion and accumulation by the
specialized cells.
Transport via membranes is mediated mostly by the ion channels and transporters, which
ensure selective passage of specific ions. In the model salt-sensitive plant, Arabidopsis
thaliana, over a thousand genes are predicted to encode membrane proteins: over one
hundred of these determine the cation channels and transporters (Mäser et al., 2001).
The molecular and structural diversity of these ion channels and transporters is amazing.
They differ in the number of protein transmembrane domains, in the selectivity filters
for allowing passage of specific ions, in the molecular structures for gating (opening
and closing) by the change of trans-membrane potential difference or by chemical compounds
and also in regulation by the interacting proteins or the chemical modifications (e.g.,
by phosphorylation and dephosphorylation, SUMOylation, S-nitrosylation, potentially
carbamylation etc.).
Naturally occurring salt-tolerant plants, halophytes, which survive at high salt concentrations,
provide a unique source of traits for the tolerance and of genes for membrane proteins
involved in ion transport and their regulators: the genes that are functioning under
salinity and could be transferred to agriculturally important crops to increase their
tolerance. The older lineage of Chlorophyta contains many marine algae with ion transporters,
channels and pumps, potentially unknown in land plants. Fungi can also provide useful
transporters, not found in Kingdom Plantae. An alternative approach, drawn from synthetic
biology, is to modify the existing membrane transport proteins or to create new ones,
with the desired properties, for transforming of the agricultural crops. Obtaining
the detailed descriptions of distinct ion channels and transporters present in halophytes,
and then progressing to the cellular and the whole plant mechanisms, is the logical
way to understand salinity tolerance. The theoretical scientific approaches involve
protein chemistry, structure-function relations of membrane proteins, systems biology
and physiology of stress and ion homeostasis.
At the time of compiling this Research Topic many aspects of ion transport under salinity
stress are not yet well understood. The structure-function relationships of ion channels
and transporters are slowly being deciphered, but essentially remain terra incognita.
The multiple links between the ion fluxes, electrophysiology and other physiological
processes, leading to salinity tolerance, are often not described in any detail. Completely
unexpected features of ion transport under salinity stress may be waiting to be discovered.
The Research Topic has attracted researchers in ion transport and salinity tolerance
of plants (and fungi) and we have combined our efforts to achieve a wider, more detailed
understanding of salt tolerance in plants mediated by ion transport.
The papers in the Research Topic address the aspects of ion transport under salinity
stress mentioned above: they analyse precise details of the molecular structure of
ion transporters linked to the selectivity of ion transport and compare ion fluxes
in different organisms. The results suggest a diversity of adaptations to salt stress
and ion transport in yeast and other fungi, in algae, in agriculturally important
plants and crops and further in halophytes from mangroves to recretohalophytes, which
excrete salt via specialized salt glands. The topic contributions explore numerous
aspects of salinity tolerance, including osmotic adjustment, oxidative stress, changes
in photosynthesis and morphology of cells. The wide and comprehensive picture of the
processes related to salinity tolerance is united under the heading of ion transport
at the time of saline stress. The following short introduction, describing the contributing
papers, provides a brief guide to the topics that have been addressed.
The reviews in this topic lay out a logical pathway for understanding the ion transport
and physiology of plants affected by salinity: from characterization of Na+ fluxes
and their regulation at the level of the whole plant to fluxes at the cellular and
vacuolar membranes with specific ion channels and transporters. Maathuis et al. provide
a solid description of the morphological structures and the molecular mechanisms important
for Na+ transport. Volkov applies a quantitative approach to ion transport, initially
in yeast and other small cells and then to entire plants (Volkov; Volkov). The current
advanced methods allow us to estimate the exact number of the individual ion channels
and transporters in a single yeast cell. Further, we can determine their uneven distribution
in specific lipid domains with a size around hundreds of nanometers. The ion fluxes
via cellular membranes are also influenced by the cell walls and by the hydrostatic
pressure inside cells, adding more complexity (Volkov). A similar quantitative approach
is useful for the whole plants, although much less is known about the larger organisms.
In a second review, Volkov applies a systems biology approach, describing the progress
in genetic and protein engineering to manipulate ion fluxes in plants (Volkov).
The Characeae are one of the three charophyte branches of the phylogenetic tree that
gave rise to land plants. Beilby provides a comprehensive review of salinity tolerance
in giant-celled algae of the Characeae, introducing this classical system and its
response to salinity, measurement of ion fluxes and study of fast electric action
potentials. The narrative compares the salt-tolerant Chara longifolia and Lamprothamnium
species with the salt-sensitive Chara australis and discusses several electrically
active states of the plasma membrane, when different sets of ion transporters determine
the membrane electrophysiology. The review ponders both hyper and hypo-osmotic regulation
in these unusually large cells (Beilby).
Moving to more saline environments in a brief perspective paper on halophytes, Duarte
et al. focus on morphological features of halophytes, particularly photosynthesis,
accumulation of osmotically active substances and antioxidants protecting the plant
exposed to high salinity. Yuan et al. and Dassanayake and Larkin present reviews that
discuss novel advances in research on the ion transport via salt glands of excreting
salt recretohalophytes. The former review focuses on the morphological structure of
salt glands, methods of collection of salt gland liquid, mechanisms of ion transport
including the specific ion channels and transporters involved (Yuan et al.). The latter
review discusses morphology and evolution of salt glands, suggesting that the salt
glands emerged independently at least 12 times in recretohalophytes. Further narrative
briefly describes the present genetic resources available for genetic engineering
of salt glands and ponders the strategies and complications on the way (Dassanayake
and Larkin).
Research papers within the Topic feature two reports analysing macroscopic results
of single amino acid substitutions within specific regions of potassium HAK5 (Alemán
et al.) and cation HKT (Almeida et al.) transporters. The plant transporter HAK5 is
important for K+ uptake at low K+ concentrations in the soil. The mutation F130S in
HAK5 from A. thaliana substituted phenylalanine to serine in a presumed pore for K+
binding of the transporter. The mutated HAK5 increased the survival of yeast cells
of strain 9.3 under salinity. These yeast cells lacked their own K+ and Na+ transport
systems, but expressed the mutated HAK5 from Arabidopsis (Alemán et al.). The kinetic
transport properties of mutated HAK5 were also characterized in the yeast 9.3 cells.
The F130S mutation surprisingly increased affinity for Rb+ (Rb+ mimicked K+ uptake)
over 100 times, while reducing the inhibitory constants Ki of the Rb+ transport by
Na+ or by Cs+ over 10 times. Several other HAK5 mutants also demonstrated altered
kinetic properties of transport (Alemán et al.). The HKT cation transporters play
a role in Na+ and K+ transport to xylem and in uptake of the ions by roots. A single
amino acid change from serine to glycine (S70G) in the first pore domain of tomato
HKT1;2 (SlHKT1;2) transporter altered the ion selectivity of transport. The mutated
form of SlHKT1;2 transported K+ and Na+, instead of only Na+, but at lower rates.
The selectivity of ion transport was characterized when SlHKT1;2 was expressed in
oocytes of African clawed toad Xenopus laevis. The ion currents were measured by the
electrophysiological method of two-electrode voltage clamp. The heterologous expression
of tomato HKT1;2 in the mutant Arabidopsis athkt1;1 plants without native HKT transporter
restored the K+ accumulation in the shoots. Thus the combined methods of molecular
biology and electrophysiology characterized the functioning of SlHKT1;2 transporter
in tomato (Almeida et al.).
Two more experimental papers link expression of the individual genes with salinity
tolerance and ion transport (Liu et al.; Jing et al.). In barley under salinity treatment
the expression of slow anion channel genes, HvSLAH1 and HvSLAC1, was up-regulated
in the leaves of salt-tolerant cultivars and positively correlated with the grain
yield under field conditions. Compared to sensitive varieties, the aperture of stomatal
cells under salinity remained larger in the salt tolerant barley plants, although
significantly decreased in comparison to control conditions (Liu et al.). The trees
of the mangrove Kandelia candel grow at the sea coast with roots in seawater and the
expression of its superoxide dismutase gene KcSOD in tobacco plants increased their
salt tolerance (Jing et al.). Further, the Na+ fluxes in roots, the accumulation of
ions, the activity and intracellular location of superoxide dismutase, the kinetics
of reactive oxygen species and the parameters of photosynthesis or growth were characterized
for the mangrove, the transgenic tobacco and the Arabidopsis plants (Jing et al.).
Three experimental papers report important physiological aspects of ion transport
and salinity tolerance for different plant species. The sodium accumulation in vacuoles
and in the cytoplasm of distinct root zones was explored in detail for six salt-tolerant
and sensitive wheat cultivars by using a sodium-sensitive fluorescent dye. Unexpectedly,
the cells of root meristem in the salt-tolerant cultivars had a higher Na+ in their
cytoplasm than those of the salt-sensitive cultivars (Wu et al.). The responses to
salinity of salt-tolerant and salt-sensitive varieties of habanero pepper plants (Capsicum
chinense) also differed greatly (Bojórquez-Quintal et al.). The salt tolerant variety
accumulated fifty times more osmolyte proline in roots, retained more K+ in the roots
under salinity, sequestered Na+ in the cytoplasm in vacuole-like structures and not
in the apoplast, compared to the salt sensitive pepper plants (Bojórquez-Quintal et
al.). The halophyte Atriplex canescens (fourwing saltbush) increased the net photosynthetic
rate, accumulated more proline and betaine, kept relatively stable K+ concentrations
in its tissues and had higher Na+ in the salt glands under salinity than under non-saline
conditions (Pan et al.).
Finally, three other experimental papers elucidate several novel areas, usually not
associated with salt stress. Selected strain BG03 of the soil bacterium Bacillus subtilis
improved salinity tolerance of the white clover by decreasing the osmotic potential
of the leaves and preserving better K+/Na+ ratio under salinity (Han et al.). The
examination of potato plantlets, using electron microscopy, revealed unusual features
of the ultrastructure of leaf mesophyll cells and their chloroplasts, which were recorded
under a gradient of salinity treatments (Gao et al.). The associated biochemical tests
and X-ray microanalysis of plant tissues added more details to understanding the survival
of these plantlets under saline conditions (Gao et al.). The salt avoidance bending
of growing roots, known as halotropism, was documented for Arabidopsis plants (Yokawa
et al.). Halotropism was influenced by the illumination stress for these roots. The
illumination stress increased their growth rate, stimulated oxidative stress and influenced
F-actin-dependent processes. The UVR8 light receptor relocated to nuclei in apical
root cells after UV-B treatment, while the halotropism was inhibited by light (Yokawa
et al.).
We believe that our simultaneous efforts will inspire further research and wider understanding
of the ion transport in general and at the time of salinity stress. We also hope that
the Research Topic lays one more foundation stone in understanding the biophysics
of ion transport via ion channels and transporters en route to deciphering salinity
tolerance, creation of salt-tolerant crops, and of growing crops in the fields irrigated
with salt water.
Author contributions
All authors listed have made a substantial, direct and intellectual contribution to
the work, and approved it for publication.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.