10 1016@j Xinn 2020 100017

The Innovation Review
Mechanisms of Plant Responses

and Adaptation to Soil Salinity
Chunzhao Zhao,1,2,* Heng Zhang,3 Chunpeng Song,2 Jian-Kang Zhu,1,4,* and Sergey Shabala5,6,*
DOI:https://doi.org/10.1016/
Soil salinity is a major environmental stress that restricts the growth and yield of
j.xinn.2020.100017
crops. Understanding the physiological, metabolic, and biochemical responses of
http://www.cell.com/the-innovation
plants to salt stress and mining the salt tolerance-associated genetic resource in
nature will be extremely important for us to cultivate salt-tolerant crops. In this ª 2020 This is an open access article
review, we provide a comprehensive summary of the mechanisms of salt stress under the CC BY-NC-ND license
responses in plants, including salt stress-triggered physiological responses, (http://creativecommons.org/
oxidative stress, salt stress sensing and signaling pathways, organellar stress, ion licenses/by-nc-nd/4.0/).
homeostasis, hormonal and gene expression regulation, metabolic changes, as

*Corresponding author:
well as salt tolerance mechanisms in halophytes. Important questions regarding
Email: czzhao@psc.ac.cn (C.Z.),
salt tolerance that need to be addressed in the future are discussed.
jkzhu@sibs.ac.cn (J.-K.Z.),
sergey.shabala@utas.edu.au (S.S.)
Introduction
Soil salinity is a worldwide problem that threatens the growth and yield of crops 1
Shanghai Center for Plant Stress
and prevents the sustainable development of modern agriculture. More than one- Biology and CAS Center for
third of irrigated lands in the world are affected by salinization.1 The major causes Excellence in Molecular Plant
of soil salinity are rising levels of groundwater with high salt content and poor- Sciences, Chinese Academy of
Sciences, Shanghai 200032, China;
quality drainage and irrigation systems.2 All the major staple crops responsible
2
State Key Laboratory of Crop
for the bulk of calorie uptake by humans (e.g., rice, wheat, and corn) are glyco-
Stress Adaptation and
phytes, which are unable to complete their life cycle when soil NaCl concentra- Improvement, School of Life
tions exceed 200 mM.3,4 Thus, improving salinity stress tolerance in crops is of Sciences, Henan University, Kaifeng
paramount importance for global food security. To achieve this goal, it is neces- 475004, China;
3
sary to understand how high salinity affects the morphological, physiological, State Key Laboratory of Plant
biochemical, metabolic, and gene expression properties of plants. Molecular Genetics, Shanghai
Center for Plant Stress Biology,
4 Center of Excellence in Molecular
The ability of plants to tolerate high salinity varies between and within species,
Plant Sciences, Chinese Academy of
which enables us to identify gene loci and natural variations that are critical for
Sciences, Shanghai 200032, China;
salt stress tolerance in plants. Fundamental studies in the model plant Arabidopsis 4
Department of Horticulture and
have revealed many genes that are required for salt stress tolerance, and applica- Landscape Architecture, Purdue
tions of some of these genes to crops increase their salt stress tolerance. The dis- University, West Lafayette, IN
covery of the salt overly sensitive (SOS) signaling pathway,5,6 a major mechanism 47907, USA;
5
behind the exclusion of Na+ from the cytosol to the outside of cells, was a mile- International Research Centre for
Environmental Membrane Biology,
stone in our understanding of how plants deal with salt load. Recent work
Foshan University, Foshan 528000,
showed that glycosyl inositol phosphorylceramide (GIPC) sphingolipids may
China;
function as salt stress sensors in plants.7 Research on halophytic plants, which 6
Tasmanian Institute of Agriculture,
usually reside in high salinity environments, have also been important for us University of Tasmania, Hobart, TAS
to understand salt tolerance mechanisms in plants. Some halophytes have 7001, Australia
1
developed special structures, such as epidermal bladder potentially transduce a change in the xylem pressure
cells that accumulate excessive Na+ in their vacuoles, caused by salinity into altered stomatal apertures.
which enable them to adapt to high salinity. Recent
progress in understanding the mechanisms underlying The second constraint imposed by salinity is ionic
the salt stress tolerance of halophytes will facilitate the imbalance (often called “ionic stress” or “ion toxicity”
breeding of salt-tolerant crops. This review provides a in the literature). In most cases, this constraint is associ-
synopsis of salt stress responses and adaptation in plants ated with an excessive accumulation of Na+ and Cl in
and considers the newest developments in the field. metabolically active intracellular compartments. Sur-
These developments include adaptative physiological prisingly, the mechanistic basis of such toxicity is poorly
responses, sensing and signaling pathways, salinity- understood. Although it is well known that Na+ can
induced stress on specific organelles, hormonal regula- harm plant metabolism and can potentially kill the
tion, ion homeostasis, metabolic changes, and salt toler- plant,17 the target(s) of Na+ in the plant is unknown.
ance mechanisms of halophytes. The most common explanation for Na+ toxicity is that
it has an inhibitory effect on the activities of enzymes.
The cytosolic compartment, for example, contains
Physiological Responses to Salt Stress many enzymes involved in primary metabolism, the Cal-
Salinity stress inhibits plant growth and development vin cycle, the phenylpropanoid pathway, glycolysis, and
by imposing several major constraints. The first polyamine and starch synthesis. Many of these enzymes
constraint is an osmotic stress (the lowering of the are controlled by K+.18 Given the close similarity between
external water potential) that compromises a plant's Na+ and K+,19 it is usually accepted that the Na+ tends to
ability to take up water. This process triggers several replace K+ in those enzymatic reactions, but with much
major events in plant tissues. At the macroscopic level, less efficiency.14,18,20 In addition Cheeseman,17 noted that
expansion of both root8 and shoot9 cells is immediately biomacromolecules occupy 20%–30% of the cytoplasmic
arrested as a result of a decreased turgor pressure. To volume. Because biomacromolecules are complexed and
deal with this issue, plants must adjust osmotically. charged 3D structures, their operation is strongly
Most of the cell turgor in the root is regained within affected by electrostatic interactions and the ionic
40–60 min10 by an increase in the uptake of inorganic strength of the solution, as well as by the presence of
ions, and growth is resumed, although at a reduced both screened and unscreened electrostatic forces.21 As
rate. The latter fact is most likely explained by modifi- a result, small hydrated Na+ ions tend to accumulate in
cation of the composition of the cell wall resulting the regions of greater density, while larger K+ ions tend
from the binding of Na+ to cell wall components.11 Os- to be found in the less dense regions. This differential
motic stress also results in rapid closure of stomata, intracellular ion distribution will have an impact on
which reduces the plant's ability to assimilate CO2. cell operation, as the fixed charge and ionic conditions
Rapid closure of stomata can be explained by the rapid of the cytosol will inevitably determine the local water
drop in xylem pressure (e.g., by 0.05 MPa in maize roots relations relevant to the cytoskeleton and proteins.17
exposed to 100 mM NaCl)12 that accompanies salinity
stress. This drop in xylem pressure occurs within mi- A related issue is chloride (Cl) toxicity. The current
nutes upon stress onset, and the hydraulic signals notion is that Cl exclusion from the shoot is crucial
sensed by roots move at the speed of sound13 and are for salt tolerance.22 This inference is supported by the
transduced almost instantaneously to the shoot, where findings in certain salt-sensitive species that high shoot
they are decoded and alter shoot metabolism.14 Because Cl levels are positively correlated with severe physiolog-
stomatal guard cells possess a range of mechano-sensi- ical dysfunctions.23,24 However, the negative correlation
tive (stretch-activated) ion channels,15,16 they could between shoot Cl concentration and plant biomass
2
recorded for some salt-grown non-halophytes does not mental stresses, including pathogen infection, high
hold for halophytes,23 some of which are capable of accu- salinity, drought, and heat stress.37 The major ROS in
mulating Cl at a concentration >1 M without experi- plants include hydrogen peroxide (H2O2), superoxide
encing a major negative effect on plant performance.25 anion (O2$), singlet oxygen (1O2), and hydroxyl radical
Researchers have argued that the detrimental effects of (OH$). These ROS are mainly produced in the apoplast,
Cl on plant performance may be not a result of toxicity chloroplasts, mitochondria, and peroxisomes.37 Produc-
per se but rather from a Cl-induced deficiency of key tion of ROS in the apoplast is mediated by plasma mem-
macro-nutrients (e.g., N and S), as uptake of NO3 and brane-localized respiratory burst oxidase homologs
SO42 are mediated by the same (non-selective) anion (such as AtRbohD and AtRbohF), apoplastic diamine
transporters as Cl.23 It therefore appears that the nega- oxidase, peroxidase, and polyamine oxidases.37 AtRbohD
tive effect caused by either Na+ or Cl is not a nutrient and AtRbohF genes are both upregulated under salt
toxicity per se but instead results from interference with stress, and simultaneous mutations of these two genes
the uptake or metabolism of other essential ions. For result in hypersensitivity to salt stress.38 The mecha-
this reason, the use of the term ionic imbalance is more nisms underlying the positive roles of AtRbohD/AtR-
suitable and should be used instead of the more popular bohF in salt stress tolerance have been revealed by
specific ion toxicity. several studies. Salt-induced production of ROS by AtR-
bohD/AtRbohF promotes the movement of K+ into the
Another widely held misconception is related to the cytosol and thus reduces Na+/K+ ratios.38 AtRbohF is
timescale imposed by these two constraints. The tradi- able to restrict the distribution of Na+ in xylem sap,
tional view is that ionic stress has a slower speed of onset and thereby reduces the delivery of Na+ from roots to
than osmotic stress and operates at a timescale of days if shoots via transpiration.39 AtRbohD mediates the prop-
not weeks.26,27 Although this view does apply to shoot tis- agation of long-distance signals triggered by a variety of
sues, it does not apply to the plant as a whole. In response environmental stimuli, including high salinity, wound-
to ionic stress, various PCD (programmed cell death) ing, heat, cold, and high-intensity light,40 suggesting
events are observed in roots at a much more rapid time- that ROS are required for systemic signaling in plants.
scale. Apoptotic events, such as DNA laddering or cyto- AtRbohD/F-mediated production of H2O2 at the early
chrome c release, are observed in plant roots within stage of salt stress could be a signal that triggers an anti-
hours of salinity exposure.28–30 In Arabidopsis roots, the oxidative response that reduces the oxidative damage to
level of autophagy (another form of PCD) peaks within cells.41 ROS production in the apoplast contributes to
30 min of salt stress.31 Importantly, these salinity-induced lignin formation under a saline environment.42
PCD events are Na+ specific and not related to the os-
motic component of salt stress.32,33 The salinity-induced In shoots, both osmotic stress-induced stomatal closure
PCD events in plant roots are significantly reduced or and accumulation of high levels of Na+ in the cytosol
prevented in Arabidopsis mutants lacking a gated impair the photosynthetic machinery. As a result, the
outwardly rectifying K+ channel (GORK),34 suggesting a amount of absorbed light exceeds the demand for
causal link between Na+ entry into the cytosol, resulting photosynthesis, which leads to the formation of ROS
in membrane depolarization and accompanied by K+ in green tissues.43 There are three major sites of ROS
efflux, and activation of caspase-like proteases and endo- production in chloroplasts: (1) the Mehler reaction in
nucleases that execute PCD.35,36 the PSI; (2) 1O2 production by photosystem II (PSII) in
the thylakoid membrane resulting from limitation of
Salinity and Oxidative Stress the electron transport chain between photosystems;
Reactive oxygen species (ROS), which function as versa- and (3) H2O2 production at the electron donor side of
tile signals, are rapidly induced by a variety of environ- PSII via incomplete oxidation of water due to the
3
inhibition of the water-splitting manganese com- To reduce the oxidative stress caused by the accumula-
plex.44,45 Another major source of ROS production in tion of ROS under high salinity, plants rely on activation
salt-affected plants is mitochondrial respiration. Over- of ROS-scavenging machineries. The enhanced toler-
reduction of the ubiquinone pool during salt stress al- ance of halophytes to high salinity is to some extent
lows electrons to leak from complexes I and III of the due to an enhanced capacity to maintain ROS homeo-
mitochondrial electron transport chain to molecular ox- stasis.59 The scavenging of excessive ROS under high
ygen, which results in O2$ production.37 The peroxi- salinity may be attributed to non-enzymatic antioxidant
some is a major site for the production of intracellular metabolites, including ascorbate, glutathione, and to-
H2O2.46 The reduced CO2/O2 ratio in plant cells under copherols, and to enzymatic agents, such as catalases
salt stress promotes H2O2 production in peroxisomes (CAT), superoxide dismutase (SOD), ascorbate peroxi-
through enhanced photorespiration.47 dase (APX), and glutathione reductase (GR).60 Enhance-
ment of these antioxidant systems increases salt stress
At low concentrations, ROS act as signal molecules to tolerance in plants. For example, the increased accumu-
regulate many biological processes, including plant lation of total glutathione in peroxisomes, chloroplasts,
growth and responses to a variety of biotic and abiotic and mitochondria conferred increased tolerance to salt
stresses. An excessive accumulation of ROS under saline stress,59,61 and a reduction in the ascorbate content in
conditions, however, has detrimental effects on plant tis- the vtc2-1 mutant is correlated with a reduction in salt
sues. The detrimental effects of ROS are traditionally stress tolerance.62 In chloroplasts, SOD catalyzes the
attributed to their ability to damage key cellular transfer of O2$ to H2O2, and APX is required for the
structures, including lipid peroxidation in cellular conversion of H2O2 to H2O.43 Plants that overexpress
membranes, DNA damage, protein denaturation, carbo- the APX gene show enhanced tolerance to salt and
hydrate oxidation, pigment breakdown, and an impair- drought stresses.63 NCA1, a chaperone protein that is
ment of enzymatic activities.48 Before this damage to required for the maintenance of the functional state of
key cellular structures occurs, however, stress-induced CAT, positively regulates salt stress tolerance.64 In mito-
accumulation of ROS disturbs ionic homeostasis in the chondria, alternative oxidase (AOX) and manganese
cells by activating many different types of ROS-sensitive SOD (Mn-SOD) are the major enzymes involved in the
ion channels. H2O2-sensitive Ca2+-permeable ion chan- detoxification of ROS. Plants with higher activities of
nels have been found in both root epidermal cells49 mitochondrial AOX1 and Mn-SOD exhibit increased
and stomatal guard cells.50 Constitutively expressed in- tolerance to salt and drought stress.65,66
ward-rectifying K+ channels in stomata are also inhibited
by H2O.51 OH$, which is generated upon H2O2 reduction
in cell walls, has a much wider action spectrum and can Salt Stress Sensors
activate a broad range of non-selective (thus, Na+-perme- To avoid the damage caused by the high concentrations
able) cation channels52,53 as well as GORK-like K+ efflux of salts in soil, plants must have evolved the ability to
channels,34,54 annexin-mediated conductance,55 and a sense salt stress, to transduce signals to cell interiors,
Ca2+-pump.54 ROS-regulated ion channels are also pre- and to adjust cellular traits. Identification of salt stress
sent at organellar membranes (e.g., chloroplasts,56 vacu- sensor(s) has been challenging, perhaps because of the
oles57) and alter the operation of these organelles. For functional redundancy of sensors, technical difficulties,
example, the salt stress-induced decrease in the photo- or lethality when salt stress sensors are knocked out.
synthetic performance of chloroplasts is associated Many abiotic stresses, including high salinity, drought,
with the swelling of thylakoids58 that results from and cold, trigger increases in the cytosolic Ca2+ concen-
increased ion fluxes across the thylakoid membrane via tration within seconds to minutes.67,68 For this reason,
H2O2-activated ion channels.56 identification of proteins or other components that are
4
required for the rapid influx of Ca2+ under stress condi- induced transcriptional and growth adaptation.71 The
tions is considered to be a good way to discover stress KEA1/2 and KEA3 transporters are required for osmotic
sensors. Based on this possibility, researchers have con- stress-induced Ca2+ response, suggesting that KEA1/2
ducted genetic screens for mutants that are defective in and KEA3 may function as sensors of osmotic stress.72
the activation of Ca2+ signaling under a variety of envi-
ronmental stresses. In addition to sensing salt stress via Ca2+ signaling,
plants may also sense salt stress by recognizing
Reduced hyperosmolality-induced [Ca2+]i increase1 (OSCA1), salinity-induced changes in cellular structures. High
which encodes a hyperosmolality-gated calcium- salinity rapidly reduces turgor pressure, which is the
permeable channel, was identified as an osmotic stress consequence of osmotic stress-mediated water loss.
sensor.69 Mutation in the OSCA1 gene impairs osmotic The reduced turgor pressure can be perceived by me-
stress-induced Ca2+ signaling in guard cells and root chanosensitive sensors, such as MscS-like (MSL),
cells, which results in reduced stomatal closure and Mid1-complementing activity (MCA), and two-pore po-
root growth in response to osmotic stress. The osca1 tassium (TPK) family proteins.73 MSL8 is required for
mutant does not show altered phenotypes under high the survival of pollens subjected to the hyperosmotic
salinity, which raises a question about the role of shock of rehydration,74 and MSL2 and MSL3 are
OSCA1 in the sense of high salinity-triggered osmotic required for the adaptation of plastids to hyperosmotic
stress. Using a similar screening strategy, researchers stress.75 It is well known that excessive accumulation
recently identified monocation-induced [Ca2+]i increases 1 of ions in the apoplast affects the properties of cell
(MOCA1), which encodes a glucuronosyltransferase wall components, which are perceived by cell wall-local-
that is involved in the biosynthesis of glycosyl inositol ized glycoproteins or plasma membrane-localized re-
phosphorylceramide (GIPC) sphingolipids and that is ceptor-like kinases.76 Proteins potentially involved in
specifically required for spikes in cytosolic Ca2+ in sensing cell wall changes include hydroxyproline-
response to ionic stress but not in response to osmotic rich glycoproteins (HRGPs), wall-associated kinases
stress.7 Mutation in the MOCA1 gene leads to reduced (WAKs), and CrRLK1L family proteins.76–79 WAKs are
weight and reduced survival under salt stress. GIPCs able to bind to pectin and Ca2+, and excessive Na+ may
were shown to directly bind to Na+ and regulate the affect these interactions and thus trigger stress
entry of Ca2+ into the cytosol.7 However, which Ca2+ signaling.80 Recent studies indicate that the cell wall-
channels are involved in this process and how binding localized leucine-rich repeat extensins LRX3, LRX4,
of Na+ to GIPCs activates Ca2+ channels remain and LRX5, together with secretory peptides RALFs and
unknown. the receptor-like kinase FER, are involved in sensing
and relaying salt stress signals by monitoring the status
Other proteins that mediate salt-induced Ca2+ signaling of cell wall integrity, although the initial sensing of
have also been reported. These proteins include FERO- salinity-triggered cell wall changes by the LRXs is still
NIA (FER), annexin1 (ANN1), and plastid K+ exchange not understood.79 FER inhibits the proton transport ac-
antiporters (KEAs).70–72 FER, a member of the Catharan- tivity of plasma membrane H+-ATPase (AHA2) and thus
thus roseus receptor-like kinase 1-like (CrRLK1L) protein regulates pH in the apoplast.81 FER is also required for
family, directly binds to pectin. Loss of function of FER the activation of cell wall repair pathways to maintain
results in reduced salt-induced Ca2+ signaling and cell wall integrity under high salinity.70 FEI1 and FEI2,
increased sensitivity to high salinity.70 ANN1 mediates two leucine-rich repeat receptor kinases (LRR-RKs),
ROS-activated Ca2+ influx in response to increased accu- are also associated with cell wall integrity sensing.
mulation of extracellular Na+. Mutation in the ANN1 Loss of function of FEI1 and FEI2 results in hypersensi-
gene leads to increased Na+ influx and impaired salt- tivity to high sucrose and high salt.82,83
5
Ionic Stress Signaling modulating the activity of the K+ channel AKT1, a pro-
The environmental stimuli-triggered Ca2+ influx signal cess that requires SOS2-mediated phosphorylation of
into the cytoplasm can be decoded by diverse Ca2+- SCaBP8.92,93
dependent proteins, such as calcium-dependent protein
kinases (CDPKs), calcineurin B-like proteins (CBLs)/ MAPK cascades94–96 and phosphatidic acid (PA)97 are
SOS3-like calcium-binding proteins (SCaBPs), CBL-in- also involved in the regulation of the salt stress signaling
teracting protein kinases (CIPKs)/protein kinases of pathway. Salt stress activates MPK3, MPK4, and MPK6,
the SOS2 family (PKS).67 In Arabidopsis, the SOS which contribute to salt stress tolerance in Arabidop-
signaling pathway, which consists of SOS3 and SCaBP8, sis.94,95,97 The activities of MPK4 and MPK6 under salt
SOS2, and SOS1, plays a critical role in the regulation of stress are induced by MKK2. Phenotypic analysis re-
Na+/K+ ion homeostasis5,6,84 (Figure 1). SOS3 and vealed that plants overexpressing MKK2 exhibit
SCaBP8 relay salt-induced Ca2+ signals to SOS2 ki- increased salt stress tolerance, while mkk2 null mutants
nase.84–86 SOS3 activates and recruits SOS2 to the are hypersensitive to salt stress.94 In rice, the osmkk1-
plasma membrane via its interaction with the regulatory knockout mutant is hypersensitive to salt stress, which
domain of SOS2.5 SOS2 is a serine/threonine protein ki- is caused by the impaired activation of OsMPK4.95
nase belonging to the sucrose non-fermenting 1 (SNF1)/ Conversely, activation of MKK9 increases sensitivity to
AMPK family.5 Under normal conditions, the kinase ac- salt stress in Arabidopsis,96 suggesting a complex regula-
tivity of SOS2 is inhibited by 14-3-3 and GIGANTEA (GI) tory network among distinct MAP cascades in response
proteins. Salt stress promotes the degradation of 14-3-3 to salt stress. Salt stress triggers phospholipase D
and GI, resulting in the release of SOS2 from SOS2- (PLDa)-mediated production of PA, which in turn regu-
GI/14-3-3 complexes and consequently the activation of lates the salt stress response by activating MPK6. Acti-
SOS2 by SOS3.87,88 A recent report indicated that PKS5 vated MPK6 phosphorylates the C-terminal fragment
inhibits the activity of SOS2 by promoting interaction of SOS1 and promotes salt stress tolerance.97 Mutations
between SOS2 and 14-3-3 proteins; the salt stress- in PLDa1, PLDd, or PLDa3 lead to hypersensitivity to salt
induced Ca2+ signal induces the interaction between stress.98–100 PLD-mediated production of PA is also
PKS5 and 14-3-3 and thus releases the inhibition of required for the activation of H+-ATPase101 and root
SOS2.89 The kinase activity of SOS2 is also regulated hair formation under high salinity.102
by the protein phosphatase 2C ABI2.90 SOS1 is a plasma
membrane Na+/H+ antiporter that is required for the Osmotic Stress Signaling
extrusion of the excess of Na+ out of the cells (i.e., into Whether cellular responses are induced by salinity-
the rhizosphere via root epidermal cells, or into the xy- induced ion stress or osmotic stress can be determined
lem via xylem parenchyma cells) and therefore for the by comparing plants exposed to high salinity with those
alleviation of ionic stress. SOS1 is autoinhibited under exposed to isotonic non-ionic solutions, such as
normal conditions, and the inhibition is released by mannitol and PEG. Osmotic stress triggers signaling
the phosphorylation of Ser1044 at the C-terminal pathways that promote the biosynthesis and accumula-
domain of SOS1 by SOS2 under salt stress.91 Notably, tion of compatible osmolytes, which is important for
sos mutants only show a hypersensitive phenotype un- both short-term and long-term osmotic stress tolerance
der high salinity but grow normally under osmotic stress in plants. The increased levels of compatible osmolytes
imposed by mannitol or PEG (polyethylene glycol), indi- in the cytosol reduce water loss and enhance turgor
cating that the SOS signaling pathway is specifically pressure and cell expansion.103 Both salt stress and os-
involved in the response to ionic stress. SCaBP8 also me- motic stress can activate SNF1-related protein kinase 2s
diates the regulation of Na+/K+ ion homeostasis by (SnRK2s).104,105 Osmotic stress triggers the activation of
6
Figure 1 Salt Stress Signaling Pathways

The SOS signaling pathway, consisting of SOS3/SOS3-like calcium-binding protein 8 (SCaBP8), SOS2, and SOS1, is important
for sensing salt-induced Ca2+ signals and in the regulation of ion homeostasis by extruding excessive Na+ out of cells. 14-3-3, GI,
and ABI2 negatively regulate the kinase activity of SOS2. Ca2+-mediated binding of PKS5 with 14-3-3 releases the inhibition on
SOS2. GIPCs act as putative salt stress sensors that directly bind to Na+ and trigger Ca2+ influx via an unknown Ca2+ channel.
GIPCs-mediated Ca2+ influx is required for the activation of the SOS signaling pathway. RbohD/F are involved in the pro-
duction of ROS at the plasma membrane, and ROS can activate the ANN1-mediated Ca2+ signaling pathway. AKT1, which is
regulated by SCaBP8, mediates the influx of K+ to the cytosol under salt stress. MAP kinase cascades, including MAPKKK20,
MKK2, MKK4, MPK3, MPK4, and MPK6, are involved in the relay of salt stress signals. Salt stress-induced accumulation of ABA
activates subclass III SNF1-related protein kinase 2s (SnRK2s) via the PYR/PYLs-PP2Cs-mediated regulatory module. Subclass I
SnRK2s are activated via an ABA-independent pathway under osmotic stress. Activated MPKs and SnRK2s transduce signals to
downstream transcription factors, including ABFs, zips, MYBs, NACs, WRKYs, and AP2/ERFs, in the nucleus to induce the
expression of stress-responsive genes. In the apoplast, cell wall-localized leucine-rich repeat extensins LRX3, LRX4, and LRX5,
together with secreted peptides RALF22/23 and receptor-like kinase FER, function as a module to sense salt stress-induced cell
wall changes. FER, RALFs, and LLG1 form a complex at the plasma membrane to trigger Ca2+ signaling and consequently
activate the cell wall repair pathway. FER also inhibits the activity of AHA2 to regulate apoplastic pH. In the vacuole, NHXs,
CAX1, TPK1, and H+-ATPase are involved in the regulation of ion homeostasis under high salinity. The dashed lines indicate
that the negative regulatory roles are released under salt stress.
SnRK2s in both ABA-dependent and -independent important role in the transduction of ABA signals and
manners. SnRK2 kinases are divided into three groups: in the regulation of downstream gene expression re-
subclasses I, II, and III.104,105 Subclass III SnRK2 kinases, sponses by activating AREB/ABF (ABA-responsive
including SnRK2.2, SnRK2.3, and SnRK2.6, play an element binding factor) transcription factors.106–108
7
Subclass I SnRK2s, including SnRK2.1, SnRK2.4, Cell Wall Stress

SnRK2.5, SnRK2.9, and SnRK2.10, are specifically The plant cell wall consists of cellulose, hemicellulose,
responsive to osmotic stress, but not to ABA.104,109,110 pectins, and many glycoproteins. Cell wall integrity is
The molecular mechanisms underlying the specificity an important factor that determines plant growth and
of subclass I SnRK2s to osmotic stress are still unclear. salt stress tolerance.70,79 Several mutants that are defec-
It is likely that some early signaling components, such tive in cell wall integrity are hypersensitive to salt stress.
as kinases, can be activated by osmotic stress to trigger For example, CESA6, which is a core component of the
the activation of subclass I SnRK2s. Abiotic stress- cellulose synthase complex, is required for normal root
responsive Raf-like kinases mediate the activation of elongation under salt stress.116 SOS5, encoding a fasci-
SnRK2s under osmotic stress in the moss Physcomitrella clin-like arabinogalactan protein (AGP),117 and SOS6, en-
patens,110 and whether this is also the case in higher coding a cellulose synthase-like protein, are required for
plants, such as Arabidopsis, needs to be investigated. root elongation under high salinity.118 CC1 and CC2 were
Phenotypic analysis indicates that the simultaneous discovered as companions of CESAs, and both are
disruption of ten SnRK2s increases growth inhibition required for hypocotyl growth under high salinity.119
and leaf chlorosis under osmotic stress.111 Among these MUR4 is a Golgi-localized enzyme involved in the
SnRK2s, SnRK2.4 and SnRK2.10 are important in biosynthesis of UDP-arabinose (UDP-Ara). UDP-Ara is
the maintenance of root growth and architecture involved in the modification of diverse polysaccharides
under saline conditions.105,112 The MKK4-MPK3 and and glycoproteins, which are exported to the apoplast
MAPKKK20-MPK6 cascades are required for osmotic to maintain cell wall integrity. Mutation in MUR4 leads
stress responses in Arabidopsis.113,114 Loss of function of to reduced root elongation and defective cell-cell adhe-
MKK4 increases water loss and ROS accumulation un- sion under high salinity,120 indicating that arabinose
der dehydration conditions, and salt-induced activation modifications are important for the regulation of cell
of MKK4 regulates the activity of MPK3 and increases wall integrity in roots under salt stress.
the expression of abiotic stress-responsive genes
NCED3 and RD29A.114 MAPKKK20 is required for the Na+ accumulated in the apoplast may directly bind to
activation of MPK6 under various abiotic stresses. The cell wall components and affect their chemical proper-
plants overexpressing MAPKKK20 exhibit enhanced ties.121 Because detecting the changes in cell wall compo-
tolerance to salt stress.113 sition is challenging, our understanding of the mecha-
nisms underlying the modifications of cell walls upon
exposure to high salinity is limited. Cell wall polymers
Salt-Induced Organellar Stresses are negatively charged and are therefore able to revers-
Proper functioning of cells requires coordination among ibly bind to cations.121,122 Pectin, a major component of
different organelles and cellular compartments. The the cell wall, is composed of homogalacturonan, rham-
cellular damage caused by abiotic stresses, including nogalacturonan I and II (RGI and RGII), and xylogalac-
high salinity, drought, cold, and heat, can cause stress turonan.123 Boron is required for the cross-linking of
on various organelles.115 Endoplasmic reticulum (ER) RGII,124 and the cross-linking is coordinated by Ca2+.125
stress has been widely considered as an important When present at high levels in the apoplast, Na+ may
cellular response to stress conditions, and significant ad- replace Ca2+ in binding to pectins and may thereby
vances have recently been made to understand the role interfere with pectin cross-linking,11 leading to reduced
of cell wall stress in salt stress tolerance. To attenuate cell expansion.126 Pectins are synthesized and secreted
stress-induced organellar stresses, each affected organ- into the cell wall in a methylesterified form. Pectin
elle must be able to perceive the stress signals and also methyl esterase (PME)-mediated demethylesterification
to relay the signals to the nucleus. is an important form of pectin modification.126 Binding
8
of Na+ to the substrate sites of PMEs affects the deme- genes encode chloroplast-localized proteins, many of
thylesterification of pectins and thus inhibits cell which are important for salt stress tolerance.133 Most
growth.11,127 AGPs function as a reservoir of extracellular steps of ABA biosynthesis occur in the chloroplast,
Ca2+. Excessive Na+ may free the Ca2+ bound in the AGPs and ABA biosynthesis-associated proteins, such as
and initiate influx of Ca2+ into the cytosol.128 Plants that ABA1, ABA4, and NCED3, are localized in chloroplasts
are defective in the production of AGPs are hypersensi- and are required for salt stress-induced accumulation
tive to high salinity.129,130 of ABA.137,138 MsK4, a novel Medicago sativa GSK-3-like ki-
nase localized in plastid, positively regulates the salt
Apoplastic acidification promotes cell expansion. High stress response by modulating sugar metabolism.139
salinity causes the alkalinization of the apoplast131 and Fad6 and GPAT, two plastid-localized enzymes, facilitate
thus inhibits cell growth. RALF peptides were identified thylakoid membrane fluidity and thereby increase salt
that can cause alkalinization of the apoplast by regu- stress tolerance by modulating fatty acid meta-
lating H+-ATPases at the plasma membrane.81 High bolism.140,141 Some genes encoded in chloroplasts, such
salinity can induce the production of mature RALF pep- as RUB and RCI, are associated with the maintenance
tides,79 suggesting that salt stress-induced alkalinization of PSII activity under high salinity.142,143
of the apoplast is probably mediated by RALFs. The ef-
fect of apoplastic pH on cell growth is mainly mediated The signals caused by chloroplast stress can be trans-
by the regulation of expansin activities.11 Expansins duced to the nucleus via retrograde signaling path-
facilitate cell expansion by loosening cell walls under a ways.132 High salinity-induced production of 1O2, which
variety of environmental stresses, including high salinity causes photo-oxidative damage of PSII, acts as one of
and drought stress.124 the retrograde signals.144 1O2 can be sensed by EXE-
CUTER (EX1), a nuclear-encoded protein localized in
Chloroplast Stress the thylakoid membrane of chloroplasts.145 The stress-
In addition to functioning in photosynthesis, chloro- induced release of 1O2 promotes the degradation of
plasts also contribute to the biosynthesis of amino acids, EX1, the process of which depends on oxidative post-
vitamins, isoprenoids, fatty acids, and lipids.132 Dysfunc- translational modification at the Trp643 residue in the
tion of chloroplasts caused by environmental stresses DUF3506 domain of EX1.144 Besides the EX1-mediated
can have harmful effects on the physiological, biochem- pathway, 1O2 can trigger chloroplast-to-nucleus retro-
ical, and metabolic properties of plant cells. High grade signaling via oxidative products of beta caro-
salinity has multiple effects on chloroplasts, including tene.146 Methylerythritol cyclodiphosphate (MEcPP), a
reduced CO2 uptake due to stomatal closure, reduced precursor of isoprenoids produced by the plastidial
photosynthetic efficiency, thylakoid membrane damage, methylerythritol phosphate (MEP) pathway,147 and
oxidative stress, impaired osmotic and ionic homeosta- phosphonucleotide (30 -phosphoadenosine 50 -phosphate
sis, and disrupted protein synthesis and turnover.133 [PAP]),148 are another two retrograde signaling metabo-
The reduced efficiency of photosynthesis is a major lites involved in the transduction of signals from chloro-
reason for the growth inhibition that occurs under plast to the nucleus to regulate stress-responsive gene
high salinity.134,135 K+, as an essential nutrient for plants, expression.
is required for the regulation of pH, volume, and elec-
tron transport in chloroplast.56,136 Excessive accumula- ER Stress
tion of Na+ and Cl results in reduced K+ influx in chlo- Biotic and abiotic stresses can cause the accumulation of
roplasts and thus causes ionic, osmotic, and oxidative unfolded or misfolded proteins in the ER, resulting in
stresses (see more details in other sections). Transcrip- ER stress. The misfolded proteins can be recognized
tomic profiling has indicated that 53 salt-responsive by a protein quality control system in the ER, which
9
induces the expression of chaperone genes that are (ABI4) acts as a negative regulator of AOX1a gene expres-
important for protein folding and triggers ER-associated sion. Cyclin-dependent kinase E1 (CDKE1), a component
protein degradation (ERAD) and autophagy.149 Upon of the mediator complex, regulates AOX1a gene expres-
exposure to salt stress, the ubiquitinated proteins in- sion by interacting with SNF1-related kinase 1 (SnRK1/
crease in the ER, and this accumulation activates an KIN10).157
ER stress response. The positive role of the ER stress
response in salt stress tolerance is supported by the
finding that a defect in the HRD3A of the HRD1/HRD3 Hormonal Regulation during Salt
complex, which is required for the unfolded protein Stress
response in the ERAD pathway, confers hypersensitivity Response and adaptation to salt stress require the inte-
to salt stress, and Ca2+ and ROS are required for the gration and coordination of multiple phytohormones,
ERAD-mediated response to salt stress.150 UBC32, which including ABA, jasmonic acid (JA), gibberellic acid
encodes an E2 ubiquitin-conjugating enzyme, is an (GA), ethylene, and salicylic acid (SA) (Figure 2). Among
active component of the plant ERAD compartment. these hormones, ABA is the most involved in the
UBC32 gene expression is highly induced by drought response to diverse abiotic stresses. Osmotic stress
and salt stress, and loss of function of UBC32 enhances imposed on roots results in a very rapid (within several
salt stress tolerance via a BR-dependent pathway.151 ER minutes) and massive increase in ABA concentration
stress can trigger regulated intramembrane proteolysis in both root and leaf tissues.9,158 ABA is one of the key
under stress conditions. For example, salt stress induces signaling molecules known to cause stomatal closure.159
subtilisin-like serine protease (AtS1P)-mediated cleavage This process involves binding of ABA to PYR/PYL/RCAR
of a membrane-localized bZIP transcription factor, Atb- receptors.160,161 Once the receptors bind to ABA, they
ZIP17, in the ER. The activated AtbZIP17 translocates to interact with PP2C phosphatases and inhibit their activ-
the nucleus where it upregulates the expression of ity, thus releasing SnRK2s from repression.160,161 The
many salt stress responsive genes.152 S2P stimulates the SnRK2s then activate a range of anion efflux chan-
nuclear localization of bZIP17 and bZIP28 via a process nels162,163 resulting in a loss of turgor pressure and sto-
of cleavage. In the nucleus, these two transcription fac- matal closure. Although the role of ABA in salinity-
tors induce the expression of chaperone genes and the induced stomatal closure is beyond any doubt, the origin
activation of BR signaling, and finally confer salt stress of the ABA signal is still debated. For many years, it was
tolerance.153 thought that ABA is generated in osmotically stressed
roots and is then rapidly transported to the shoot with
Mitochondrial Stress the transpiration stream.164,165 More recent studies, how-
The mitochondrion is an energy-producing organelle ever, showed that root-to-shoot ABA delivery may be not
that is important for the survival of plants under stress be required for stress-induced stomatal closure.166,167
conditions.154 Abiotic stress-induced perturbation of The NCED3 gene, which encodes the first step of ABA
mitochondrial functions can activate the expression of biosynthesis, is expressed predominantly in the vascular
stress-responsive genes via a mitochondrial retrograde parenchyma of leaves168 and is rapidly upregulated by
regulation (MRR) or retrograde signaling pathway.154,155 osmotic stress, and many experiments using reciprocal
AOX is a well-studied mitochondrion-localized protein grafting of ABA-deficient mutants suggest that drought
that is responsive to environmental stresses, and AOX in- resistance was conferred by the genotype of the scion
duction has been used as a marker for MRR in response and not of the rootstock (reviewed in Buckley166). In
to stress.154 In Arabidopsis, influx of Ca2+ into mitochon- addition, ABA synthesis in roots may require precursors
drial is required for the induction of AOX1a gene expres- transported from leaves.169 On the other hand, the stress-
sion under salt stress,156 and ABA INSENSITIVE 4 induced increase in ABA concentration is several fold
10
Figure 2 The Biological Functions of Phytohormones in

the Regulation of Salt Stress Response in Plants
ABA is a major hormone involved in the
regulation of salt stress response, including
the regulation of stomatal closure, ion ho-
meostasis, salt stress-responsive gene
expression, and metabolic changes. JA is
required for the inhibition of root elonga-
tion and activation of antioxidative en-
zymes upon exposure to high salinity. Salt
stress reduces the accumulation of endog-
enous bioactive GAs, leading to inhibition of plant growth and root elongation, delay of flowering, and promotion of survival
under high salinity. The effect of ethylene on salt stress tolerance acts in a species- or gene-specific manner. The components
involved in ethylene biosynthesis or signaling transduction either positively or negatively regulate ion homeostasis and seed
germination, but ethylene induces detoxifying machineries and promotes survival under salt stress. SA participates in the
accumulation of osmoprotectants, induction of antioxidative enzymes, and improvement of ion homeostasis under salt stress.
higher in roots than in leaves,158 but the role of ABA pro- with class C basic-helix-loop-helix (bHLH) transcription
duction in roots in the plant response to salt stress re- factors and JASMONATE ZIM-DOMAIN (JAZ) proteins,
mains unclear. the latter being the negative regulators of the JA
pathway. Loss of function of RSS3 results in the upregu-
A clue to how ABA production in roots may contribute to lation of JA-responsive genes.179 These results support
the salt stress response is provided by the fact that ABA the notion that the JA pathway is required for root
interacts with H2O2 in plant systemic responses to growth inhibition under high salinity. Overexpression
stresses.170 Salinity stress results in a significant accumu- of the OsCYP94C2b gene, which encodes an enzyme
lation of ROS in plant roots.171,172 A major source of these that catalyzes the conversion of bioactive JA-Ile to an
ROS is NADPH oxidase, a plasma-membrane-bound inactive form, enhances the survival rate of rice under
enzyme complex from the NOX family.173 Osmotic high salinity, demonstrating the negative role of JA in
stress-induced increase in H2O2 production requires salt stress tolerance. However, opposite phenotypes
NADPH oxidase stimulation by ABA.174 Also, inhibition have also been observed in studies showing that overex-
of the NADPH oxidase-mediated H2O2 production in pression of the JA biosynthesis gene TaORP1 or applica-
the root abolishes rapid stomatal closure, resulting in a tion of exogenous JA enhances salt stress tolerance in
salt-sensitive phenotype.172 Thus, salinity-induced in- wheat, rice, and soybean.180–182 Together, these results
crease in root ABA content may be critical for generating suggest that JA may act as a positive or negative regulator
an “ROS wave” that triggers stomatal closure. of salt stress response in a spatially and temporally
dependent manner.
Increasing evidence has linked the JA pathway to salt
stress responses in plants.175 Transcriptomic studies Coordination of growth and stress tolerance is critical
have revealed that many JA biosynthesis genes are upre- for the survival of plants under unfavorable conditions.
gulated under salt stress and that the JA signaling GA, as an important hormone that regulates plant
pathway is involved in the regulation of salt stress- growth, has been linked to the regulation of growth un-
responsive genes.176,177 In Arabidopsis, the JA signaling der abiotic stress.183 Treatment of Arabidopsis seedlings
pathway is required for the inhibition of root elongation with salt reduces endogenous bioactive GAs and in-
under high salinity.178 In rice, RICE SALT SENSITIVE3 creases the accumulation of DELLA protein.184,185 In
(RSS3), a nuclear-localized protein, promotes root cell the quadruple-della mutant, salt stress-triggered growth
elongation under salt stress by physically interacting inhibition and delayed flowering are attenuated, and salt
11
stress-induced death is enhanced,184 suggesting that unlike cold acclimation, for which CBF (C-repeat bind-
DELLA proteins promote the survival of plants by re- ing factor)/DREB (dehydration responsive element
stricting growth under high salinity. Ethylene is also binding protein) TFs function as master regulators, mas-
involved in salt stress tolerance in plants. Application ter transcriptional regulators for salt stress have not
of the ethylene precursor 1-aminocyclopropane-1-car- been identified. CBF1/2/3, belonging to the AP2/ERF
boxylic acid (ACC) increases salt stress tolerance,186 (APETALA2/Ethylene-Responsive Factor) family, were
while mutations in ethylene signaling pathway-associ- first identified for their involvement in low-temperature
ated genes, such as ETR1, EIN4, EIN2, and EIN3, lead responses.197,198 Overexpression of CBF3/DREB1A en-
to hypersensitivity to high salinity.186–189 The positive ef- hances plant tolerance to salinity,199 and mutation of
fect of ethylene on salt stress tolerance is largely medi- all three CBF genes results in hypersensitivity to salt
ated via the modulation of ROS-generating and ROS- stress,200 indicating a positive role of CBFs in plant salt
scavenging machineries.187,190 The role of SA in salt response. ABA mediates transcriptional regulation
stress tolerance is represented by its ability to improve mainly through the AREB/ABF subfamily of bZIP
the accumulation of osmoprotectants, such as glycine TFs.201,202 For example, overexpression of ABF2 in-
betaine, proline, and polyamines,191 and to enhance anti- creases plant resistance to multiple stresses, including
oxidant enzyme activities under high salinity.192 Pretreat- salt stress.203 A new class of ABA-responsive TFs named
ment of plants with SA also reduces NaCl-induced K+ DIG (dynamic influencer of gene expression)/DIL (DIG-
efflux and H+ influx and thus promotes the adaptation like) was also identified, and overexpression of these TFs
of plants to high salinity.193 results in hypersensitivity to high salt or ABA.204 TFs
involved in other hormone signaling pathways also
function in the salt stress response. MYC2, a master
Salt-Responsive Gene Expression and TF of jasmonate signaling, is a positive regulator of
Epigenetic Regulation of Salt Stress salt tolerance.181,205 EIN3, a TF that mediates core
Tolerance ethylene signaling, is stabilized by salt treatment and in-
Transcription is the first and the most critical step in the creases plant salt tolerance through the DELLA pro-
regulation of gene expression. Early transcriptome ana- teins.184,187 EIN3 increases salt tolerance partly through
lyses in Arabidopsis indicated that salt stress causes dif- two downstream TFs, ERF1 (Ethylene Response Factor
ferential expression in hundreds to thousands of genes 1) and ESE1 (Ethylene and Salt Inducible 1), which
depending on the strength or duration of the treat- directly bind to salt-responsive genes and activate their
ment.194,195 Salt stress, osmotic stress, and ABA treatment expression.189,206 Many other TFs from non-model plant
induce common sets of differentially expressed genes, species have also been identified mainly through tran-
especially during the early stages of stress treat- scriptome analyses. Although the specific mechanisms
ment.194,195 The transcriptome is significantly different by which most of these TFs operate are not clear, their
when salt stress is combined with other types of environ- roles in salt tolerance have usually been validated using
mental stresses compared with when salt stress is transgenic approaches in Arabidopsis or the original spe-
applied alone, indicating extensive crosstalk between cies.207 It is also important to keep in mind that TFs are
the salt stress signaling pathway and other stress highly dynamic and that the transcriptional network
signaling pathways.196 To date, hundreds if not thou- functions in a spatially and temporally specific manner.
sands of salt stress-related transcriptomes have been A recent study constructed an ABA-responsive network
conducted in many plant species. Members from all of and defined the hierarchy among 21 ABA-related TFs by
the major transcription factor (TF) families (such as associating the in vivo binding dynamics of these TFs
NAC, ERF/AP2, bZIP, MYB, and WRKY) have been with time-series transcriptome data.204 The results re-
found to be involved in the salt stress response. However, vealed that dynamic binding of multiple TFs, compared
12
with static binding, better predicts changes in gene and class II enzymes (HDA5/14/15/18) of the RPD3 his-
expression over time.204 In summary, many TFs are tone deacetylase family play negative and positive roles
involved in the regulation of salt-induced changes in in plant salinity tolerance, respectively.209–211 Further-
gene expression. High-throughput sequencing technol- more, HUB2, a ubiquitin E3 ligase responsible for
ogy facilitates the identification of TFs involved in the mono-ubiquitination of histone H2B, increases plant re-
salt stress response. Additional research on the dy- sponses to drought and salt.212,213 In Arabidopsis, the NAP1
namics of transcriptional networks is needed, however, (Nucleosome Assembly Protein 1) protein, which func-
to increase systematic understanding and identify key tions as a histone chaperone for histone H2A and H2B,
players in transcriptional regulation of the salt stress is a positive regulator of ABA signaling.214 In addition
response. to factors that modify chromatin composition and/or
conformation, various types of noncoding RNAs,
Genomic DNA in the eukaryotic nucleus is packed into including siRNAs (small interfering RNA), miRNAs (mi-
the highly ordered structure of chromatin. Transcrip- croRNA), or lncRNAs (long noncoding RNAs), also
tional regulation inevitably requires dynamic changes contribute to salt stress response. Additional details
in chromatin conformation. Many chromatin modifiers are provided in other reviews.215–217
have been identified as regulators of the salt stress
response in plants. The nucleosome is the basic unit of Certain chromatin modifications such as DNA methyl-
chromatin and is typically composed of 147 bp of ation and histone H3 lysine 27 trimethylation
genomic DNA wrapped around a histone octamer con- (H3K27me3) can be faithfully transmitted through
taining two copies of histone H2A, H2B, H3, and H4. meiosis or mitosis and are therefore considered epige-
The structure of chromatin can be remodeled by ATP- netics.218–220 Epigenetic regulatory mechanisms of salt
dependent remodelers or covalent modifications. His- stress tolerance or abiotic stress tolerance, in general,
tones contain flexible N-terminal tails, many residues have drawn substantial attention in the past two decades
of which are post-translationally modified by methyl- because they represent attractive mechanisms for plant
ation, acetylation, phosphorylation, ubiquitination, etc. stress memory, which enables plants to enhance their
In addition, genomic DNA can be methylated. Specific stress response by remembering previous stresses. This
modifications or a combination of modifications can effect is also termed “stress priming.” Priming of seeds
directly change the chromatin conformation or can re- using sodium chloride, hyperosmotic reagents, or
cruit specific binding proteins that promote changes. BABA (b-aminobutyric acid) enhances the drought or
For example, acetylation of the histone lysine residue salinity tolerance of the plants.221–223 In Arabidopsis,
neutralizes the positive charge of the lysine side chain mild salt priming of seeds results in genome-wide alter-
and reduces the interaction between the histones and ation of H3K27me3, a repressive histone mark typically
the negatively charged DNA backbone, resulting in a associated with developmental genes.223 In addition,
less-compact chromatin conformation. As a conse- multiple studies have reported salt stress-induced
quence, histone acetylation is usually associated with changes in DNA methylation across the genome.224–226
transcriptional activation. Histone acetylation is cata- Natural epigenetic variations or DNA methylation de-
lyzed by histone acetyltransferases (HATs) and is fects resulting from mutations in the DNA methylation
removed by histone deacetylases (HDACs). Multiple machinery have been linked to gene expression differ-
HATs and HDACs are involved in the salt stress ences involved in salt tolerance.227–229 Despite these ob-
response. The plant-specific histone deacetylase HD2C servations, convincing examples showing salt-induced
interacts with HDA6 and reduces salt tolerance by re- epigenetic (i.e., heritable) changes that are important
pressing the expression of ABA-responsive genes such for salt stress response have yet to be reported. The sta-
as ABI1 and ABI2.208 The class I (HDA6/HDA9/HDA19) bility of the epigenetic mark and the functional
13
Figure 3 Major Transporters Mediating Na+ Homeostasis

in Salinized Root Tissues
The major pathways for Na+ uptake in the
root epidermis are glutamate receptor-like
(GLRs) channels or cyclic nucleotide-gated
(CNGCs) non-selective cation channels and
HKT2 high-affinity K+ transporters. Other
possible pathways for Na+ uptake may
involve AKT1 Shaker-type K+ channels,
HAK5 high-affinity K+ transporters, the
low-affinity cation transporter LCT1, and
PIP2;1 aquaporins. The uptake of Na+ is
counterbalanced by active Na+ extrusion via
SOS1 Na+/H+ exchangers. Vacuolar Na+
sequestration is conferred by tonoplast-
based Na+/H+ exchangers from the NHX
family fueled by either H+-ATPase or H+-
PPase pumps. Another component of
vacuolar Na+ sequestration is efficient
control over tonoplast slow- (SV) and fast-
(FV) activating ion channels that may allow
Na+ to leak back to the cytosol. Passive Na+ loading into the xylem is mediated by non-selective cation channels (NSCCs), and its
active loading requires operation of cotransporters such as SOS1, CCC (cation-chloride cotransporters), and HKT2 (K+/Na+
symporter). Na+ withdrawal from the xylem is achieved by HKT1 high-affinity K+ transporters. Salinity-induced K+ loss from the
root epidermis is mediated by NSCCs and depolarization-activated outward-rectifying GORK K+ channels.
consequences of stress-induced epigenomic reprogram- in the almost paranoiac avoidance of cytoplasmic Na+”.
ing remain unclear. A recent study of DNA methylome Even though that paper was published more than 30
changes in response to phosphate starvation in Arabidop- years ago, Cheeseman's statement still describes the cur-
sis found that most DNA methylation changes occur af- rent view.
ter transcriptional changes and are usually transient.230
Many studies on stress-induced epigenetic changes have Plants can use two major ways to prevent accumulation
been performed in Arabidopsis, which has an unusual of high levels of Na+ in the cytosol of root cells: (1) Na+
plant genome with a very low amount of transposable el- exclusion from root uptake and (2) vacuolar Na+ seques-
ements. Salt-induced epigenetic changes in other plant tration. For photosynthetically active mesophyll cells,
species remain to be determined. there are three additional ways: (3) control of xylem
Na+ loading; (4) Na+ retrieval from the xylem; and (5)
Na+ recirculation from the shoot via the phloem.
Ion Homeostasis under Salinity
Salinity stress is usually associated with too much NaCl. Na+ Exclusion from Uptake
Because Na+ is considered to be toxic (see the section on Symplastic root uptake of Na+ is potentially mediated by
physiological responses to salt stress for details), it is several types of ion transporters (Figure 3). Two major
hardly surprising that most research concerning salinity types are non-selective cation channels,52 either gluta-
stress has been aimed at revealing the mechanisms of mate receptor-like (GLRs) or cyclic nucleotide-gated
Na+ transport and sequestration in plants. This was (CNGCs) channels; and HKT2 high-affinity K+ trans-
nicely summarized by Cheeseman,231 who stated “phys- porters.232 Other possible pathways for Na+ uptake
iological folklore has elevated sodium toxicity to a belief may involve AKT1 Shaker-type K+ channels, HAK5
14
high-affinity K+ transporters,232,233 and the low-affinity H+ exchangers.246,247 This prompted the suggestion
cation transporter LCT1,234,235 although arguments that some other mechanisms and, specifically, enhanced
against their involvement have been presented.233 vacuolar trafficking, may also deliver Na+ to the
PIP2;1 aquaporins (initially identified as plant water vacuole.248
channels) were recently added to the list of candidates
for root Na+ uptake.236 The uptake of Na+ is counterbal- Control of Xylem Na+ Loading
anced by active Na+ extrusion (Figure 3). The most prom- Despite its critical importance for salinity tolerance,
inent component in this process is the SOS1 Na+/H+ whether Na+ loading into the xylem is an active or pas-
exchanger,237 although the involvement of vesicle-medi- sive process is still debated. Both active and passive
ated Na+ transport cannot be ruled out.238 It is generally transport systems are probably involved, but their
assumed that 95% of all Na+ taken up by the root is respective roles may differ depending on the length of
then exported back to the rhizosphere.26 The reasons time since salinity onset.249,250 Passive Na+ loading is
for and the consequences of such a futile cycle are dis- likely to be mediated by non-selective cation channels
cussed in detail elsewhere.239,240 (NSCC).251 Consideration of thermodynamics suggests,
however, that under most physiologically relevant sce-
Vacuolar Na+ Sequestration narios, xylem Na+ loading should be an active process
Another way of avoiding excessive Na+ accumulation in (see Shabala250 for supporting arguments). One of the
the cytosol is to deposit it in the vacuole. The traditional most likely candidates for such active loading is the
view is that such vacuolar sequestration is conferred by Na+/H+ antiporter encoded by the SOS1 gene. Highly
operation of the tonoplast-based Na+/H+ exchangers in abundant in the xylem parenchyma,237 SOS1 belongs
the NHX family.241 Both NHX activity and transcript to the cation proton antiporter (CPA) subfamily of pro-
levels are inducible by salt in glycophytes, and such teins. The SOS1 protein is a homodimer and consists
tonoplast antiporters are constitutive in halo- of 10–12 transmembrane domains. Class 2 HKT trans-
phytes.238,242,243 More recent studies have suggested porters represent another pathway for active xylem
that NHX exchangers represent only part of the vacuolar Na+ loading. Functionally, HKT2 operates as a K+/Na+
Na+ sequestration mechanism. Another equally impor- symporter. HKT2 transporters are highly expressed in
tant sequestration mechanism involves the efficient con- the stellar root tissues.252 The depolarization of paren-
trol of tonoplast leak channels, which enables vacuolar chyma cells under saline conditions12 favors a passive
Na+ retention in the tonoplast.244 Two types of Na+- outward movement of K+ into the xylem, thus creating
permeable channels, namely slow- (SV) and fast- (FV) a driving force for the loading of Na+ into the xylem.249
activating ion channels, are present at the tonoplast, Finally, cation-chloride cotransporters (CCC) were
and model calculations show that if each cell opened found to be preferentially expressed at the xylem/sym-
only one SV channel at a specific time, the back-leak plast boundary in Arabidopsis.253 These transporters
fraction would range from 30% to 100%.244 Thus, to mediate symport of Cl, Na+, and K+, and given that
avoid the futile movement of Na+ into and out of the Cl transport into the xylem is thermodynamically
tonoplast, plants can afford to open only a very small passive, they may provide a driving force for Na+ (sec-
percentage (about 0.1%) of all tonoplast channels; this ondary) active loading into the xylem.249 Supporting
is consistent with experimental observations in salt- evidence for that view was provided by the pharmaco-
tolerant species.245 Recent studies have reported addi- logical studies conducted by Zhu et al.,254 who
tional complexity in the relationship between Na+/H+ demonstrated a significant reduction in the magnitude
antiporters and vacuolar Na+ sequestration; the studies of Na+ efflux from barley root stellar tissue in the pres-
showed that NHX antiporters have higher affinity to ence of bumetanide, a known inhibitor of mamma-
K+ than to Na+ and thus operate predominantly as K+/ lian CCC.
15
Retrieval of Na+ from the Xylem compromise root functions. The export of Na+ in the
Class I high-affinity K+ transporters have been firmly es- phloem could also cause damage to growing leaves
tablished to operate in the withdrawal of Na+ from the and meristematic regions of the shoot, assuming that
xylem sap in various species.255–259 HKT proteins belong they are connected to the phloem via sieve tubes.270
to the HKT/Trk/Ktr-type superfamily of K+ transporters, This may explain why salt-tolerant species have much
which consists of four repeats of transmembrane/pore- lower rates of Na+ export in the phloem than salt-sensi-
loop/transmembrane motifs, similar to the ion-con- tive species; for example, the percentage of Na+ that is
ducting pore-forming units of K+ channels. Members exported in the phloem is only 10% in salt-tolerant
of class I (HKT1) contain a Ser residue at the first pore- barley species271 but is 50% in salt-sensitive white
loop domain and are highly selective for Na+ over lupin.272
K+.260 The Arabidopsis genome contains only a single
copy of the AtHKT1;1 gene, but its halophytic relative Potassium Retention in the Cytosol
Thellungiella salsuginea contains three copies of HKT1- Over the last decade, researchers have found that cyto-
type genes.261 When expressed in Xenopus laevis oocytes solic K+ homeostasis and the ability of various plant tis-
and yeast, HKT1 transporters show a highly specific Na+ sues to retain K+ under stress conditions are essential for
influx.259,262 Arabidopsis hkt1;1 mutants were salt-sensitive salinity tolerance (reviewed by Shabala et al.14 and Sha-
compared with the wild type and hyperaccumulate Na+ bala and Pottosin273). Reported initially for barley
in the shoot, but accumulate less Na+ in the root,263 and roots,274 a positive correlation between the overall
targeted overexpression of the Arabidopsis HKT1;5 homo- salinity tolerance and the ability of a root tissue to retain
log in Arabidopsis and rice increases Na+ exclusion from K+ was later expanded to at least a dozen other plant spe-
the shoot.264,265 In rice, the OsHKT1;5 locus has been nar- cies (reviewed in Wu et al.18). Efficient cytosolic K+ reten-
rowed down as a salt tolerance determinant by QTL tion is also considered to be a hallmark of halophytes.275–
277
(quantitative trait locus) analysis.257 In wheat, the There are at least four physiological reasons why K+
TmHKT1; 5-A locus derived from a wild wheat relative retention is important under saline conditions. First, a
T. monococcum corresponds to the Na+ exclusion 2 high level of K+ retention allows the plant to accumulate
(Nax2) QTL that contributes to the lowering of the Na+ high amounts of Na+ in the cytosol without compro-
level in leaves.266,267 mising the cytosolic K+/Na+ ratio, the ratio that deter-
mines cell metabolic competence and, ultimately, the
Na+ Recirculation via the Phloem ability of a plant to survive in saline environments. Sec-
The Na+ load in the shoot may also be reduced by its ond, depletion of the cytosolic K+ pool may activate cas-
recirculation back to the roots via the phloem.268 The pase-like proteases and endonucleases, thus triggering
molecular mechanisms of this process remain elusive, PCD.34–36 While the physiological role of PCD under sa-
although the HKT1 class of transporters is thought to line conditions is still debated,33,36 the causal relation-
play a major role.263,269 The fate of the Na+ remobilized ship between K+ efflux and stress-induced PCD is
in the phloem is also unclear. The anatomical structure beyond any doubt.18 Third, to maintain normal meta-
of the root favors a unidirectional, radial transport of bolic activity in the cytosol, plants rely on the vacuolar
Na+. Once it passes through the Casparian strip and K+ pool to replenish the K+ lost from the cytosol. The
is loaded into the stele, Na+ has very little chance of be- vacuolar K+ buffering capacity in a typical plant cell is
ing transported back to the cortex. Hence, if a substan- estimated to be between 1 and 7 h.18,244 Thus, unless
tial quantity of Na+ is returned to the root, it presum- the cell is able to activate high-affinity K+-uptake sys-
ably must remain in the rather limited number of tems within this time frame, depletion of the vacuolar
parenchyma cells in the stele. Unless sequestered prop- K+ pool may result in a loss of turgor and collapse of
erly in vacuoles, this could cause phytotoxicity and the cell.
16
Two major pathways mediate salinity-induced K+ loss Salt Stress-Induced Metabolite

from the cell.14,18 One pathway involves the GORK chan- Changes
nel, which belongs to the Shaker family of K+ channels A major strategy used by plants to maintain a low intra-
and consists of six transmembrane domains (TMDs), a cellular osmotic potential under high salinity is the
pore helix, and a selectivity filter between the last two accumulation of compatible osmolytes,26,103 including
TMDs.278 The GORK channel is highly sensitive to proline, hydroxyproline, glycine betaine, sugars, poly-
changes in membrane potential (as occur under stress amines, and proteins from the late embryogenesis abun-
conditions) and is activated upon depolarization.279 To dant (LEA) superfamily.289–291 Among these metabolites,
prevent depolarization-induced K+ leakage, plants proline plays a dominant role in osmotic adjustment un-
must restore (otherwise depolarized) the membrane po- der salt stress.292 The accumulation of proline under os-
tential by more active H+ pumping.280 This comes at a motic stress can be achieved both by activation of the
significant ATP cost281 and may compromise the plant's proline biosynthesis pathway and by inactivation of
ability to adapt and grow. The second pathway for the proline catabolic pathway.293 Proline is bio-
salinity stress-induced K+ loss from the cell is via K+- synthesized mainly via reductions of glutamic acid by
permeable ROS-activated NSCCs.18 Differential sensi- two successive enzymes: P5C synthase (P5CS) and P5C
tivity of K+-permeable NSCC to various ROS (e.g., reductase (P5CR).294,295 P5CS is a rate-limiting enzyme
H2O2 and ,OH) explains the intraspecific,275,282 geno- in proline biosynthesis, and its activity is mainly
typic,283,284 and tissue-specific14,49 differences in salinity controlled at the transcriptional level.295 Both P5CS
stress tolerance. and P5CR genes are upregulated under high salinity,
which enables the accumulation of proline and subse-
Potassium as a Second Messenger
quent salt stress tolerance.295 In the catabolic pathway,
In addition to being an essential nutrient, K+ functions
proline can be converted to glutamate via the reactions
in signaling.285,286 When plants deal with energy crises
catalyzed by proline dehydrogenase (PDH) and P5C de-
(as they do under saline conditions240), they must use
hydrogenase (P5CDH).296 The negative role of PDH in
a large fraction of available ATP for defense, at the
salt stress tolerance is supported by the fact that plants
expense of “business as usual” metabolism. Given that
with lower transcript levels of PDH have higher salt
many metabolic enzymes require K+,18,287 transient cyto-
stress tolerance.297,298 Apart from its role in osmotic
solic K+ efflux is thought to operate as a “metabolic
adjustment, proline acts to stabilize proteins and mem-
switch” that inhibits energy-consuming anabolic reac-
brane structures, as well as an ROS scavenger that atten-
tions and saves energy for adaptation and repair, which
uates oxidative stress under high salinity.299–301
may give species a competitive advantage under the en-
ergy-limiting conditions imposed by salinity.35,286 At the
same time, the amount of K+ lost for signaling purposes GB is another major metabolite that is increased under
should not compromise the plant's nutritional demand salt stress and is associated with adjustment of osmotic
for this element. This dilemma is resolved by the tran- potential under dehydrating conditions.302,303 Choline
sient nature and high tissue specificity of stress-induced monooxygenase (CMO) and NAD+-dependent betaine
K+ efflux.14 In addition, different plant species may aldehyde dehydrogenase (BADH) are required for the
display distinct salt stress-induced K+ flux “signa- biosynthesis of glycine betaine from choline via two
tures,”281 prompting analogies with cytosolic Ca2+ oxidation reactions. Glycine betaine is also important
signaling.67 In the latter case, an array of protein kinases for protecting enzymes, stabilizing membranes, and
and calcium-binding proteins decode transient Ca2+ reducing oxidative stress under stress conditions.304
spikes.288 It remains to be determined whether a similar Trehalose is a non-reducing disaccharide of glucose
mechanism characterizes K+ signaling. that helps protect plants against abiotic stress.305
17
Application of trehalose reduces ROS accumulation, Succulence

which in turn alleviates oxidative stress under high Succulence is an important adaptive strategy that accu-
salinity.305,306 Transgenic rice plants that overexpress mulates excessive salt and conserves water in saline-
OsTRE1 have enhanced salt stress tolerance.307 Other grown plants. This trait is not unique to halophytes,
sugars, such as glucose, fructose, and fructans, are also because increased leaf succulence also occurs in glyco-
involved in the osmotic adjustment under drought and phytes,315 although to a much lesser extent than in halo-
salt stress.193 Polyamines are organic amines, which phytes. In halophytes, a specialized parenchymatous tis-
include putrescine, spermidine, and spermine.308,309 sue beneath the photosynthetically active
Application of exogenous polyamines or the engineer- chlorechymatous tissue functions in both salt storage316
ing of plants with increased levels of polyamines in- and water storage.317 Succulence is mostly characteristic
creases tolerance to salinity and to other abiotic of dicot species belonging to the Chenopodioideae and
stresses.310 Salicornioideae.318 The mechanistic basis of develop-
ment of succulent structures in plants is linked to endo-
Myo-inositol metabolism is important for the relay polyploidy or endoreduplication,319 although specific
of specific signals to the cell. Several myo-inositol- details are still emerging. An increase in the activity of
derived inositol phosphates have been shown that are aquaporins increases succulence in some halophyte spe-
required for the response to environmental stresses. cies,320 suggesting that a turgor-driven mechanism may
Inositol trisphosphate (IP3) is rapidly induced upon also be involved. The molecular mechanisms mediating
salt stress and ABA treatment.311,312 In plants, IP3 is salt deposition in succulent storage tissues remain
associated with the release of Ca2+ from vacuolar vesicles elusive. A recent study found that storage parenchyma
and thus relay of environmental stress signals. cells in the succulent halophyte Carpobrotus rosii act as
Inositol 1,3,4-trisphosphate 5/6-kinase (ITPK) catalyzes Na+ sinks and have both a higher Na+ sequestration abil-
the conversion of IP3 to inositol tetrakisphopsphate ity and a higher K+ retention ability than mesophyll
(IP4). In rice, disruption and overexpression of the cells;316 the latter trait was indicated by a higher rate of
OsITPK2 gene both lead to increased sensitivity to H+-ATPase operation and higher non-enzymatic antiox-
salt and drought stress,313 which implies that the homeo- idant activity in this tissue. Also, storage parenchyma
stasis between IP3 and IP4 is important for stress cells have a constitutively lower number of open SV
tolerance. vacuolar channels and the ability to downregulate activ-
ity of FV vacuolar channels. Because both SV and FV
channels represent major pathways for Na+ leakage
Salinity Tolerance in Halophytes into the cytosol, the efficiency of salt load sequestration
According to the Dictionary of Botany, halophytes are in parenchymatous tissues depends on the ability of the
“plants that are adapted to live in soil containing a plant to control this process.
high concentration of salt;” many other definitions of
halophytes are available in the literature. Despite these Salt Glands and Bladders
differences in definition, all authors agree that the phys- Salt glands are present in more than 50 halophyte spe-
iological, anatomical, or genetic traits do not fundamen- cies from 14 families321 and are believed to have evolved
tally differ between halophytic species and domesticated independently at least 12 times. At the functional level,
(non-halophytic) crop species.314 The major difference is two types of salt glands can be distinguished: those
that halophytes are simply much more efficient in im- that directly secrete salts to the surface of the leaf
plementing these traits.238 Some traits, however, can be (exo-recretohalophytes), and those that collect salt in
considered as hallmarks of halophytic species, and these the vacuole of a specialized bladder cell (endo-recreto-
are briefly summarized in the following sections. halophytes).321,322 Structurally, salt glands are divided
18
SC
EC
Figure 4 A Proposed Model for the Mechanism of Salt Sequestration in Epidermal Bladder Cells
Left part of figure shows the morphology of an epidermal cell (EC), stalk cell (SC), and epidermal bladder cell (EBC). Right part
of the figure presents ion transport systems in the EC, SC, and EBC. SOS1 (Na+/H+ plasma membrane exchanger) and HKT1
(high-affinity potassium transporter) transport Na+, while SLAH (Cl permeable anion channel) and NRT (Cl/H+ co-trans-
porter) transport Cl from EC to EBC. In the EBC, NHX1 (tonoplast-based Na+/H+ exchanger) and CLC (anion channel) are
required for the sequestration of excessive Na+ and Cl in the vacuole. Plasma membrane-localized H+-ATPase and vacuolar
ATPase (V-ATPase) are essential for the generation of proton gradients and membrane potential that drive the transport of Na+
and Cl from the EC to the vacuole of the EBC.
into four groups: (1) highly vacuolated unicellular secre- has been characterized at the molecular and func-
tary cells (e.g., those in Porteracia species); (2) two-celled tional level.
excretory structures (those in graminoids); (3) multi-
cellular (up to 40 cells) glands found in some graminoids Salt glands in the fourth group, which are characteristic
and several dicot families; and (4) a structure consisting of endo-recretohalophytes, deposit the salt load in a
of a stalk cell and an epidermal bladder cell (e.g., those in bladder-like epidermal outgrowth called the epidermal
quinoa or Atriplex species) (Figure 4).238,323 Salt glands in bladder cell (EBC). Because EBCs are large (typically
the first three groups, which are characteristic of exo-re- 100–200 mm in diameter),325,326 each EBC has a volume
cretohalophytes, release salt periodically. NaCl is that is three orders of magnitude larger than that of a
thought to be transported into the salt gland through mesophyll cell or an epidermal cell; the large volume fa-
both the plasmodesmata and the regions that are not cilitates external salt storage, away from metabolically
covered by the cuticle.323 The salt secretion per se inactive photosynthetic tissues.327 EBC density is higher
volves membrane-bound transport proteins. Several in younger leaves than in older leaves.326 During
such transporters were postulated to exist in salt glands ontogeny, EBCs increase in size and operate as salt de-
of various halophyte species.324 None of them, however, pots. Once an EBC accumulates a certain threshold
19
quantity of salt, it ruptures and releases the salt into the Leaf Photochemistry
external environment.328 The causal link between EBCs Both PSII and PSI are inactivated by increasing NaCl
and salinity stress tolerance was demonstrated when the levels in the cytosol.276,338 The dark reactions of photo-
mechanical removal of bladder cells in quinoa resulted synthesis are also affected by salinity,339 with many key
in a salt-sensitive phenotype.329 The molecular identities photosynthetically related enzymes being inactivated.134
of key transporters involved in accumulation of Na+ and Such inactivation, however, appears to differ between
Cl in EBCs in quinoa have recently been postulated330 halophytic and glycophytic species. The transport of
and characterized at the functional level.331 Salt bladders some key metabolites such as pyruvate, ascorbate, and
may also function as a secondary epidermis to reduce phosphate into chloroplasts in halophytes requires the
water loss and prevent excessive UV damage in addition presence of Na+.134 Chloroplastic fructose 1,6-bisphos-
to functioning as reservoirs for the storage of water and phatase (FruP2ase) from the halophyte Porteresia coarc-
various metabolic compounds.332,333 tata was less sensitive to NaCl in vitro compared with
its domesticated relative Oryza sativa (cultivated
Osmotic Adjustment rice);340 this difference was attributed to mutations in
Plants may achieve osmotic adjustment via two major some amino acid residues in the FruP2ase gene.341
avenues, i.e., by de novo synthesis of organic osmolytes Some halophytes require high concentrations of Cl to
and by increased uptake of inorganic ions. Because the enhance electron transport and oxygen evolution during
production of organic osmolytes has a very high carbon salt stress;134 they also demonstrate a higher extent of
cost,334,335 plants that use this strategy may be able to sur- attachment of Rubisco activase to the thylakoid mem-
vive stress conditions but may grow poorly. The carbon brane.342,343 The sensitivity of grana unstacking to the
cost of osmotic adjustment via inorganic ion uptake is ionic strength of the stroma also differs significantly be-
an order of magnitude lower than that via organic osmo- tween glycophytes and halophytes.344,345 Salinity also
lyte synthesis334,336 and is generally preferred, assuming has a greater effect on rETR and maximal photochem-
that the problem of Na+ toxicity is resolved. This is the ical efficiency of PSII in isolated chloroplasts of glyco-
case for halophytes.250,314,337 Among inorganic osmo- phytes than of halophytes.276 There seems to be some
lytes, K+ is the most abundant in the cell and non-toxic important differences in the structure of the PSII com-
so is preferred. However, K+ uptake under saline condi- plex between halophytes and glycophytes, with PsbQ
tions has an additional cost,281 while Na+ is present in the protein (one of the extrinsic proteins mediating binding
soil in high concentration and thus can be taken affinity of Cl to the Mn-Ca-Cl complex) being
passively. Thus, halophytes rely on Na+ as a “cheap os- completely absent in halophytes.345,346
moticum” to maintain cell turgor pressure (hence, elon-
gation growth and stomatal operation). This trait is com- Stomatal Patterning and Operation
plemented by the superior ability of halophytes to safely The low soil-water potential imposed by salinity causes
sequester toxic Na+ and Cl ions in the vacuole and to a marked decline in stomatal conductance (Gs); the
thereby maintain their cytosolic and organellar concen- physiological rationale behind this reduction is the
trations below toxic levels (as discussed in previous sec- plant's attempt to minimize water loss under the condi-
tions). The osmotic potential of the cytosol is then tions of reduced water availability (“physiological
adjusted by an increased accumulation of organic osmo- drought”) imposed by salinity. This reduction in Gs
lytes to match that of the vacuole. As the volume of the comes, however, with a reduction in net CO2 assimila-
cytosol is only 10% of the total cell volume, such a tion, and therefore a reduction in plant growth. To un-
strategy is energetically more favorable than one in derstand how this problem is solved by halophytes,
which the cell deposits large amounts of organic osmo- consider that Gs may be reduced by a decrease in stoma-
lytes into its vacuole in order to maintain its turgor. tal aperture or stomatal density.250 Halophytes seem to
20
be highly efficient in controlling both stomatal aperture altering stomatal production in response to environ-
and density. Stomatal aperture is controlled by many mental change, with numerous transcriptional regula-
environmental and internal signals; among these, ABA tors, cell-to-cell signaling, and polarity proteins
and H2O2 are the most important. Salt stress-induced involved.359,360 An increased understanding of this pro-
ABA production is highly dynamic, with peak ABA levels cess in halophytes could suggest ways to increase
detected within 15 min of salinity exposure in plant roots WUE (and therefore overall salinity stress tolerance)
and within 30 min in leaves.347 However, while all crop in crops.
species respond to salinity by a rapid increase in the xy-
lem sap ABA content,348–350 this seems not to be the case Salt Cress as Model Halophytic Organisms
for halophytes.351,352 It also appears that the basal leaf More than 15 years ago, two close relatives of Arabidopsis
ABA content (i.e., content under non-saline conditions) from the genus of Thellungiella were proposed as model
is much lower in halophytes than in glycophytes353 halophytes for molecular genetics studies, because of
and is increased only slightly in salt-grown plants, while their ease of genetic transformation, short life cycle,
in glycophytes, salinity stress results in a 2- to 3-fold in- and relatively small genome.361,362 One of them is Schren-
crease in leaf ABA content. It was suggested that modu- kiella parvula (formerly known as Eutrema parvulum and
lation of the stomatal aperture by altering ABA levels op- before that as Thellungiella parvula), and the other one is
erates over a much lower concentration range in Eutrema salsugineum (formerly known as T. salsuginea).
halophytes than in glycophytes.353 Another difference Consistent with the notion that the same molecular ma-
concerns the stress-induced increases in ROS levels, chinery for salt tolerance operates in both glycophytes
which are accelerated in halophytes compared with gly- and halophytes, loss-of-function mutants of the SOS1
cophytes.354 Consequently, the ROS sensitivity of the homolog in E. salsugineum lost halophytism.363 The
guard cell channels and antioxidant systems should genomic sequences for both E. salsugineum and
differ between halophytes and glycophytes.353 Another S. parvula have been reported. Although both genomes
striking difference comes from the ability of halophytes are diploid and contain a similar number of genes,
to substitute K+ by Na+ in stomatal operations.355 they differ significantly in their content of repeat/trans-
posable elements (TEs).261,364,365 About 50% of the
Leaves can lose water even when stomata are fully E. salsugineum genome is composed of TEs, and it re-
closed. This process, which is termed residual transpira- mains to be investigated whether these TEs contribute
tion, is controlled by several factors, one of which is sto- to the evolution of its salt tolerance traits. Certain phys-
matal density. Stomatal density is positively correlated iological traits are associated with high salt tolerance in
with Gs,356 and it was argued that a reduction in stomatal salt cress, including high accumulation of the osmopro-
density may represent a fundamental mechanism by tectant proline, duplication or increased expression of
which plants can optimize water-use efficiency salt stress-associated genes, swollen roots with addi-
(WUE).250 Consistent with this idea are observations tional layers of endodermis and cortex, and efficient
by Franks et al.,357 who found that WUE was increased management of the Na+/K+ ratio.366,367 In particular,
by 20% in Arabidopsis mutants that had a reduced sto- the expression of SOS1 and the vacuolar H+-pyrophos-
matal density as a result of overexpressing the EPF2 phatase VP1 are increased in response to high salinity
(epidermal pattering factor) gene. Salinity causes a in E. salsugineum.363,368 EsSOS1 is under positive selec-
marked (about 30%) decrease in stomatal density in tion and operates more efficiently than SOS1 from Ara-
quinoa,250,326,358 and a negative correlation between sto- bidopsis.369 Interestingly, a single amino acid substitution
matal density and salt tolerance has been reported for determines the ion selectivity of EsHKT1;2, which pre-
many other halophytic species (reviewed in Shaba- fers K+ over Na+ and confers salt tolerance in Arabidop-
la250).The stomatal lineage is dynamic and flexible, sis.370 These findings indicate that evolution acts on
21
multiple levels to enhance the function of salinity- in the sensing of salt stress. The status of cell wall integ-
related genes in halophytes. rity under salt stress is crucial for plants to determine
the strength and duration of salt stress response.
Currently little is known about the salt-induced cell
Future Perspective wall changes and the mechanisms underlying the
Soil salinity will continue to threaten crop production sensing and repair of cell wall integrity under salt stress.
and food security in the future. Cultivation of salt- Engineering of crops with enhanced cell wall biosyn-
tolerant crops is the most effective way to overcome thesis may not only increase the biomass but also
this environmental problem. In the last three decades, improve the tolerance to a variety of environmental
extensive efforts have contributed to our understanding stresses. At the transcriptional level, it is critical to un-
of the mechanisms of salt stress tolerance in plants. derstand the expression of a specific gene in a strict tis-
However, application of this fundamental knowledge sue- and cell-based context and also study the gene reg-
to improve salt stress tolerance of crops in the field is a ulatory network at the whole-plant level. The molecular
slow and challenging process. With the aid of gene edit- mechanisms underlying root-to-shoot signaling need to
ing technologies and advances in efficient genetic trans- be further elucidated. It has been shown that multiple
formation in different species, improvement of salt phytohormones are involved in the response to high
stress tolerance of crops will become more feasible. Hal- salinity. Systemic studies on the crosstalks between
ophytes have developed special molecular mechanisms different hormones in response to salt stress need to
or special cellular structures to tolerate high concentra- be emphasized in the future.
tion of salts. Growing halophytes in saline soils can
greatly increase the area of arable land and also improve
salt conditions in the soil. Knowledge of the molecular
Acknowledgments
We are grateful to Zichen Xu for assistance in the prep-
mechanisms underlying the formation and function of
aration of the figures. This work was supported by the
salt tolerance structures, such as EBCs, in halophytes
Strategic Priority Research Program (grant no.
can be potentially applied in crops to improve their ca-
XDB27040101) of the Chinese Academy of Sciences.
pacity to accumulate high concentrations of ions.
Identification of salt stress sensor(s) is one of the most

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The Innovation Review

Mechanisms of Plant Responses

homeostasis, hormonal and gene expression regulation, metabolic changes, as

Figure 1 Salt Stress Signaling Pathways

Subclass I SnRK2s, including SnRK2.1, SnRK2.4, Cell Wall Stress

Figure 2 The Biological Functions of Phytohormones in

Figure 3 Major Transporters Mediating Na+ Homeostasis

Two major pathways mediate salinity-induced K+ loss Salt Stress-Induced Metabolite

Application of trehalose reduces ROS accumulation, Succulence

Identiﬁcation of salt stress sensor(s) is one of the most

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