The Crop Journal 10 (2022) 13–25

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The Crop Journal

journal homepage: www.elsevier.com/locate/cj

Salt tolerance in rice: Physiological responses and molecular

mechanisms
Citao Liu a, Bigang Mao b, Dingyang Yuan b, Chengcai Chu c, Meijuan Duan a,⇑
a
College of Agriculture, Hunan Agricultural University, Changsha 410128, Hunan, China
b
State Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha 410125, Hunan, China
c
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy for Seed Design, Chinese Academy of Sciences, Beijing
100101, China

a r t i c l e i n f o a b s t r a c t

Article history: Crop yield loss due to soil salinization is an increasing threat to agriculture worldwide. Salt stress dras-
Received 30 November 2020 tically affects the growth, development, and grain productivity of rice (Oryza sativa L.), and the improve-
Revised 21 January 2021 ment of rice tolerance to salt stress is a desirable approach for meeting increasing food demand. The main
Accepted 17 March 2021
contributors to salt toxicity at a global scale are Na+ and Cl
ions, which affect up to 50% of irrigated soils.
Available online 6 April 2021
Plant responses to salt stress occur at the organismic, cellular, and molecular levels and are pleiotropic,
involving (1) maintenance of ionic homeostasis, (2) osmotic adjustment, (3) ROS scavenging, and (4)
Keywords:
nutritional balance. In this review, we discuss recent research progress on these four aspects of plant
Salt stress
Rice (Oryza sativa L.)
physiological response, with particular attention to hormonal and gene expression regulation and salt
Salt tolerance genes tolerance signaling pathways in rice. The information summarized here will be useful for accelerating
Physiological response the breeding of salt-tolerant rice.
Salt signal transduction Ó 2021 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by
Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
2. Effects of salt stress on rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
3. Mechanisms underlying rice salt stress tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
3.1. Regulation of ionic balance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
3.2. Osmotic adjustment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
3.3. ROS scavenging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
3.4. Nutrient imbalance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
3.5. Developmental adjustment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
4. Salt stress signaling in rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
4.1. The SOS signaling pathway. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
4.2. Hormonal regulation during salt stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
4.2.1. Abscisic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
4.2.2. Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
4.2.3. Gibberellic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
4.2.4. Auxin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
4.2.5. Cytokinins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
4.2.6. Brassinosteroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
4.2.7. Jasmonic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
4.2.8. Salicylic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
4.3. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
5. Future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

⇑ Corresponding author.
E-mail address: duanmeijuan@163.com (M. Duan).

https://doi.org/10.1016/j.cj.2021.02.010
2214-5141/Ó 2021 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

Declaration of competing interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

CRediT authorship contribution statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

1. Introduction Calvin cycle and other pathways [27,28]. Excess Na+ in the cyto-
plasm also interferes with the uptake and transport of potassium
Soil salinity is an environmental factor that has severe negative (K+) and other macro- and micronutrients, including nitrogen (N),
effects on seed germination, crop growth, and productivity [1], and phosphorus (P), potassium (K+), calcium (Ca2+) and zinc (Zn2+)
it is becoming a serious problem worldwide [1,2]. Of the 230 mil- [13,29–32]. In addition to osmotic and ionic stresses, salt stress
lion hectares of farmland currently in use around the world, 20% is causes the cellular accumulation of reactive oxygen species
affected by salt, and this percentage increases every year as a result (ROS), which can severely damage cellular structures and macro-
of inappropriate crop irrigation practices, overfertilization, and molecules such as DNA, lipids, and enzymes [33,34].
excessive plowing, as well as natural causes such as salt intrusion Under salt stress, plants must adjust the physiological and bio-
into coastal zones resulting from rising sea levels [2–4]. The threats chemical processes involved in the regulation of ion and osmotic
of salinity are more obvious in arid and semiarid regions where homeostasis, oxidative stress, and nutritional balance [1,25].
limited rainfall, high evapotranspiration, and extreme tempera-
tures coupled with poor water and soil management are the main 3. Mechanisms underlying rice salt stress tolerance
contributing factors [5,6]. In China, there are as many as 100 mil-
lion hectares of saline farmland [7]. Globally, salinity is a signifi- 3.1. Regulation of ionic balance
cant abiotic stress that affects one-quarter to one-third of the
crop productivity of on agricultural soils [8]. As the world popula- Salt stress is commonly caused by high concentrations of Na+
tion increases, more food is needed to meet the rising demand, and and Cl
in the soil [9,35]. Na+ and K+ are imported into the cell
the use of saline land to make up for the resulting food shortage is using the same suite of transporters, and the two cations compete
becoming more urgent [9]. Scientists are attempting to increase with each other [36]. K+ is important for the catalytic activities of
food production by 70% in order to avoid the risk of food shortages many central enzymes, and excess Na+ competes with K+ for
for 9.3 billion people by 2050 [10]. Rice, an important cereal crop uptake across the plasma membranes of plant cells [37]. K+ is also
that feeds half of the world’s population, is sensitive to salt stress necessary for osmoregulation and protein synthesis, the preserva-
[11,12]. Improvement of rice salt stress tolerance is therefore of tion of cell turgor, and optimal photosynthetic activity [6,38,39].
paramount importance for global food security. The maintenance of cellular Na+/K+ homeostasis is therefore a cru-
Combating salt stress to increase rice production requires a cial factor that determines the plant’s ability to survive during salt
thorough understanding of physiology, biochemistry, metabolism, stress [1,25].
and gene expression under salt stress conditions. In this review, we Mechanisms to reduce cytoplasmic Na+ include restriction of
systematically summarize the current understanding of salt stress Na+ uptake, increase of Na+ efflux, and compartmentalization of
effects on rice, the mechanisms that underlie rice salt stress toler- Na+ in the vacuole [1,40]. The rice plasma membrane Na+/H+ anti-
ance, and salt stress signaling in rice. This information may be porter (OsSOS1) excludes Na+ from the shoot, promoting a lower
helpful for developing salt-tolerant rice varieties. cellular Na+/K+ ratio and increasing salt tolerance [41,42]. The vac-
uolar Na+/H+ antiporters OsNHX1, OsNHX2, OsNHX3, OsNHX4,
2. Effects of salt stress on rice OsNHX5, and OsARP/OsCTP play important roles in the vacuolar
compartmentalization of Na+ and K+ that accumulate in the cyto-
Plant morphological changes under high salt conditions include plasm and thereby determine rice salt tolerance [43–45]. Members
impaired root system establishment, leaf rolling, chlorosis, fewer of the rice high-affinity K+ transporter (HKT) family, OsHKT1;1,
tillers per plant, reduced biomass, shorter plant height, lower thou- OsHKT1;4/OsHKT7, and SKC1/OsHKT1;5/OsHKT8, help to reduce
sand grain weight, fewer spikelets per panicle, and more sterile flo- Na+ accumulation in leaves during salt stress [46–48]. OsHKT1;1,
rets, ultimately leading to reductions in harvest index and grain OsHKT2;1, OsHKT2;3/OsHKT3, OsKAT1, OsKAT2, OsHAK5, and
yield [13–16]. OsHAK21/qSE3 transport Na+ or both Na+ and K+, helping to main-
Salt stress affects plant physiology and biochemistry at all tain Na+/K+ homeostasis in the cytoplasm and regulate rice
developmental stages from germination to senescence [6,17,18]. response to salt stress [46,49–58]. The vacuolar H+-translocating
Salt stress has both osmotic and ionic or ion-toxicity effects on inorganic pyrophosphatase OsVP1 pumps H+ from the cytosol into
plants, ultimately causing oxidative stress and nutrient depletion the vacuole, increasing the electrochemical potential gradient of H+
in plant cells [6,19]. Continuous salt stress reduces plant cell turgor between the cytoplasm and vacuole, thereby promoting the
pressure, which in turn reduces cell growth, and plants must exchange of Na+/H+ and improving rice tolerance to salt stress
osmotically adjust to maintain cell expansion and growth [20– [43]. Researchers have demonstrated that Cl
induces deficiencies
22]. Osmotic stress (caused by lower water potential of the exter- in key macronutrients (e.g., N and S) because the uptake of NO
3
nal solution) is rapidly sensed by the plant soon after exposure to and SO2
4 is mediated by the same (non-selective) anion trans-
saline conditions and leads to plant water and solute deficits [9,21– porters as Cl
[23,59]. OsCLC1, OsCLC-1, and OsCLC-2 encode rice
23]. Osmotic stress also results in rapid stomatal closure, which chloride channel proteins that promote plant growth under ionic
reduces the plant’s ability to assimilate CO2 and inhibits photosyn- stress and improve salt stress tolerance [60,61] (Table 1; Fig. 1).
thesis [24]. Ionic stress causes sodium (Na+) and chlorine (Cl
) A number of genes influence rice salt tolerance by regulating
accumulation in plant cells, eventually resulting in premature leaf the expression of HKT, NHX, and CLC genes. These include tran-
senescence and even plant death [1,25,26]. The most common scription factors such as OsMYBc, OsbZIP71, OsNF-YC13, and the
explanation for Na+ toxicity is that it has an inhibitory effect on sucrose nonfermenting 1-related protein kinase2 (SnRK2) SAPK4,
enzyme activities, negatively affecting metabolism, including the which directly activate the expression of K+/Na+ transporters,
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C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

Table 1
Proteins that function in Na+/K+ homeostasis during salt stress.

Family Effect on Selectivity Relevant genes Cellular References

tolerance localization
Na+/H+ antiporter Positive Na+ OsNHX1, OsNHX2, OsNHX3, OsNHX4, Tonoplast Liu et al. [43], Fukuda et al. [44], Uddin et al. [45]
OsNHX5, OsARP/OsCTP
+
Positive Na OsSOS1 Plasma El Mahi et al. [41], Martínez-Atienza et al. [42]
membrane
Na+-transporter Positive Na+ OsHKT1;1, OsHKT2;3/OsHKT3, OsHKT1;4/ Plasma Wang et al. [46], Suzuki et al. [47], Ren et al. [48],
OsHKT7, SKC1/OsHKT1;5/OsHKT8 membrane Huang et al. [51]
Negative Na+ OsHKT2;1 Plasma Ardie et al. [49], Horie et al. [50]
membrane
Potassium transporter Positive Na+, K+ OsKAT1, OsKAT2, OsHAK5, OsHAK21/qSE3 Plasma Obata et al. [53], Hwang et al. [54], Yang et al. [55],
membrane Horie et al. [56], He et al. [58]
+ +
H -pyrophosphatase Positive H OsVP1 Tonoplast Liu et al. [53]
Cl
channel Positive Cl
OsCLC1, OsCLC-1, OsCLC-2 Tonoplast Nakamura et al. [60], Diedhiou and Golldack. [61]
Transcription factor Positive – OsMYBc, OsbZIP71, OsNF-YC13 Nucleus Wang et al. [46], Liu et al. [62], Manimaran et al.
[63]
Protein kinase Positive – OsSAPK4, OsSOS2/OsCIPK24, OsSOS3/OsCBL4 – El Mahi et al. [41], Diédhiou et al. [64]
Negative – OsMAPK33 – Lee et al. [65]

‘‘–” Not reported.

Fig. 1. Genes involved in the regulation of salt tolerance in rice, including Na+/K+ ion homeostasis (upper right), osmotic adjustment (upper left), ROS scavenging (lower left),
and nutritional balance (lower right). The middle yellow layer contains functional genes whose encoded proteins directly protect membranes and macromolecules under
stress conditions. The outer gray layer contains regulatory genes whose products protect plants from adversity by regulating the expression of functional genes under stress
conditions.

thereby improving the K+/Na+ ratio and positively regulating salt vating the Na+/H+ antiporter OsSOS1 and promoting rice tolerance
tolerance [46,62–64]. The myristoylated Ca2+-binding protein to salt stress [41,66]. The mitogen-activated protein kinase (MAPK)
OsSOS3/OsCBL4 phosphorylates OsSOS2/OsCIPK24, thereby acti- OsMAPK33 plays a negative role in salt tolerance by promoting

15
C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

higher sodium uptake into cells and thereby lowering the K+/Na+ (hydrogen peroxide), and OH
(hydroxyl radical) [9,34]. Although
ratio [65] (Table 1; Fig. 1). The results above suggest that the mod- low ROS concentrations can function as a signal to activate salt
ulation of Na+/K+ homeostasis under salt stress may provide an stress responses, excess ROS accumulation causes phytotoxic reac-
effective way to improve salt tolerance in rice. tions including DNA mutation, protein degradation, and the perox-
idation of carbohydrates and lipids [1,34]. Plants use enzymatic
3.2. Osmotic adjustment and nonenzymatic antioxidants to mitigate ROS stress [34,83,84].
Enzymatic scavengers include nicotinamide adenine dinucleotide
Salt stress also causes osmotic stress and promotes the biosyn- phosphate oxidases (NOXs, also called respiratory burst oxidase
thesis and accumulation of compatible osmolytes such as sugar, homologs [Rbohs]), superoxide dismutase (SOD), ascorbate perox-
proline, glycine betaine, polyamines, and proteins from the late idase (APX), catalase (CAT), glutaredoxin (GRX), glutathione perox-
embryogenesis abundant (LEA) superfamily. These osmolytes play idase (GR), glutathione S-transferase (GST), and glutathione
a dominant role in osmotic adjustment under salt stress by reduc- peroxidases (GPXs) [1,85–90]. Nonenzymatic scavengers include
ing cell osmotic potential and stabilizing proteins and cellular ascorbic acid (ASH), alkaloids, carotenoids, flavonoids, glutathione
structures [1,23]. The proline synthesis genes OsP5CS1 and OsP5CR (GSH), phenolic compounds, and tocopherol [83,91,92]. OsRbohA
increase proline accumulation and improve rice tolerance to salt and OsRbohI are induced by salt treatment, whereas OsRbohB, OsR-
stress [67]. OsTPS1, OsTPS2, OsTPS4, OsTPS5, OsTPS8, and OsTPS9, bohC, OsRbohE, and OsNox6 are repressed [93]. OsMn-SOD1 and
which encode trehalose-6-phosphate synthase (TPS), enhance rice OsCu/Zn-SOD overexpression lines show lower accumulation of
tolerance to cold, salt, and drought stresses by increasing trehalose O
2 and H2O2 under salt stress [94,95]. OsAPX2, OsAPX7, OsAPx8,
and proline contents under abiotic stress [68]. OsGMST1, which OsAPXa, and OsAPXb increase APX activity, lower H2O2 and malon-
encodes a monosaccharide transporter, increases monosaccharide dialdehyde (MDA) levels, decrease oxidative stress damage, and
accumulation and improves salt tolerance in plants [69]. The enhance rice tolerance to salt stress [96–99]. OsGST4 is induced
Sugars Will Eventually be Exported Transporters (SWEETs) OsS- by heavy metals, hypoxia, and salt stress in rice [100]. Glutathione
WEET13 and OsSWEET15 regulate the transport and distribution responsive rice glyoxalase II (OsGLYII-2) functions in salinity adap-
of sucrose and maintain sugar homeostasis in rice under drought tation by maintaining better photosynthetic efficiency and increas-
and salinity stresses [70]. Rice glycine betaine is synthesized by ing the antioxidant pool [101]. OsGR2, OsGR3, and OsGRX8 increase
the choline monooxygenase OsCMO and the betaine aldehyde GSH content and enhance tolerance to various abiotic stresses,
dehydrogenase OsBADH1, which enhance rice tolerance to salt including salinity, osmotic, and oxidative stress [99,102–106].
stress by promoting glycine betaine accumulation [71,72]. The The cytosolic dihydroorotate dehydrogenase gene OsDHODH1
LEA genes OsLEA3-2, OsLEA4, OsLEA5, and OsEm1 significantly improves rice tolerance to salt and osmotic stresses [107]. Rice
improve plant tolerance to salt and osmotic stresses [73–76]. GDP-mannose pyrophosphorylase OsVTC1-1 and dehydroascor-
The salt-regulated gene OsSALP1 encodes a small plant-specific bate reductase (OsDHAR) play critical roles in plant salt tolerance
membrane protein that improves salt tolerance by increasing by promoting the ASH scavenging of excess ROS [108,109]. OsGSA1
OsP5CS expression and free proline content under salt stress [77]. encodes a UDP-glucosyltransferase that causes plants to accumu-
The transcription factors OsZFP252, OsZFP179, OsZFP182, OsNF- late flavonoid glycosides, which protect rice against abiotic stress
YC13, OsCOIN, and OsNAC5 increase the amount of free proline [110] (Table 3; Fig. 1).
and soluble sugars, upregulate the expression of stress tolerant A number of genes improve the salt tolerance of rice by regulat-
genes, and enhance rice tolerance to salt stress [63,78–82] (Table 2; ing genes involved in ROS biosynthesis and scavenging pathways.
Fig. 1). The calcium-dependent protein kinases OsCPK4 and OsCPK12
and the receptor-like kinase OsSIK1 promote tolerance to salt
3.3. ROS scavenging stress by reducing the accumulation of ROS [111–113]. The tran-
scription factors OsZFP179, OsZFP182, OsZFP213, OsHBP1b/Osb-
Plant exposure to salt stress can upregulate the production of ZIP3, OsMADS25, OsMyb2, and OsMyb6 positively regulate salt
ROS such as 1O2 (singlet oxygen), O
2 (superoxide radical), H2O2
tolerance by increasing ROS-scavenging ability [79,80,114–118],
whereas the zinc-finger proteins DST and DCA1 negatively affect
rice salt tolerance by regulating the transcription of ROS-
Table 2 scavenging genes [119,120] (Table 3; Fig. 1). All these studies sug-
Proteins and metabolites that function in osmotic adjustment during salt stress.
gest that enhancing ROS-scavenging ability can efficiently increase
Group Effect on Relevant genes References the salt tolerance of rice.
tolerance
Proline Positive OsP5CS1, OsP5CR, Sripinyowanich et al.
OsSALP1 [67], Yuan et al. [77]
Trehalose Positive OsTPS1, OsTPS2, Li et al. [68] 3.4. Nutrient imbalance
OsTPS4, OsTPS5,
OsTPS8, OsTPS9
Monosaccharides Positive OsGMST1 Cao et al. [69] Salt stress causes plant nutritional deficiencies due to reduced
SWEETs Positive OsSWEET13, Mathan et al. [70] transport efficiency and decreased uptake of nutrients such as N,
OsSWEET15 P, K, Ca, Zn, and magnesium (Mg) [6,13,29,121]. Mg2+ transport
Glycine betaine Positive OsCMO, OsBADH1 Hasthanasombut et al.
by OsMGT1 in the mature root zone synchronously enhances
[71], Tang et al. [72]
LEA Positive OsLEA3-2, OsLEA4, Duan and Cai. [73], Hu OsHKT1;5 activity, which restricts Na+ accumulation in the shoots
OsLEA5, OsEm1 et al. [74], He et al. [75], and improves salt tolerance [122]. The rice aminotransferase
Yu et al. [76] OsAMTR1 interacts with stress associated protein 1 (OsSAP1) and
Membrane Positive OsSALP1 Yuan et al. [77] regulates abiotic stress responses [123]. The cytokinin type-B
protein
Transcription Positive OsZFP252, Manimaran et al. [63],
response regulator (RR) OsRR22 regulates Zn acquisition by
factor OsZFP179, Xu et al. [78], Sun et al. directly modulating the expression of Zn-regulated transporter
OsZFP182, OsNF- [79], Huang et al. [80], genes and the sensitivity to salt stress [124,125]. OsMADS27 regu-
YC13, OsCOIN, Liu et al. [81], Song et al. lates root development in a NO
3 -dependent manner and modu-
OsNAC5 [82]
lates salt tolerance in rice [126] (Table 4, Fig. 1).
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Table 3
Proteins and metabolites that function in ROS homeostasis during salt stress.

Group Effect on Relevant genes References

tolerance
Respiratory burst oxidase homolog (Rboh) Induced OsRbohA, OsRbohI Wang et al. [93]
Repressed OsRbohB, OsRbohC, OsRbohE, OsNox6 Wang et al. [93]
Superoxide dismutase (SOD) Positive OsMn-SOD1, OsCu/Zn-SOD Li et al. [94], Guan et al. [95]
Ascorbate peroxidase (APX) Positive OsAPX2, OsAPX7, OsAPx8, OsAPXa, OsAPXb Zhang et al. [96], Lu et al. [97], Hong et al. [98],
Chou et al. [99]
Glutathione S-transferase (GST) Induced OsGST4 Lee et al. [100]
Positive OsGLYII-2 Lee et al. [100]
Glutathione reductase (GR) Positive OsGR2, OsGR3 Chou et al. [99], Wu et al. [105], Kaminaka et al. [106]
Glutathione peroxidase (GRX) Positive OsGPX1, OsGRX8 Sharma et al. [102], Wu et al. [103], Lima Melo et al. [104]
UDP-glucosyltransferase Positive OsGSA1 Dong et al. [110]
Dihydroorotate dehydrogenase Positive OsDHODH1 Liu et al. [107]
Ascorbic acid (ASH) Positive OsVTC1-1, OsDHAR Qin et al. [108], Ushimaru et al. [109]
Protein kinase Positive OsCPK4, OsCPK12, OsSIK1 Asano et al. [111], Campo et al. [112], Ouyang et al. [113]
Transcription factor Positive OsZFP179, OsZFP182, OsZFP213, Sun et al. [79], Huang et al. [80], Zhang et al. [114],
OsHBP1b/OsbZIP3, OsMADS25, Lakra et al. [115], Xu et al. [116], Yang et al. [117],
OsMyb2, OsMyb6 Tang et al. [118]
Negative DST, DCA1 Cui et al. [119], Huang et al. [120]

4.1. The SOS signaling pathway

Table 4
Proteins that function in nutritional adjustment during salt stress.
Plants use a calcium-dependent protein kinase pathway known
Group Effect on Relevant References as the salt overly sensitive (SOS) pathway for salt stress signaling
tolerance genes
and the development of Na+ tolerance [138,139]. The SOS pathway
Mg transporter Positive OsMGT1 Chen et al. [122]) was the first abiotic stress signaling pathway to be characterized in
Aminotransferase Positive OsAMTR1 Kothari et al. [123]
Regulator of Zn Negative OsRR22 Gao et al. [124], Zhang
plants [139]. It is a major mechanism for the exclusion of Na+ from
transport et al. [125] the cytosol, and its elucidation was a milestone in our understand-
Regulator of NO
3 Positive OsMADS27 Chen et al. [126] ing of how plants deal with salt load [140,141]. In this pathway, the
transport calcium-binding protein OsSOS3/CBL4 senses the cytosolic calcium
signal elicited by salt stress, then interacts with and activates a
3.5. Developmental adjustment sucrose non-fermenting-1-related protein kinase-3 (SnRK3),
OsSOS2/OsCIPK24. Activated OsSOS2/OsCIPK24 phosphorylates
Plant response to salinity is the collective outcome of intricate and activates OsSOS1, a Na+/H+ antiporter at the plasma mem-
communications among various processes linked to plant mor- brane, which in turn controls Na+ homeostasis and improves rice
phology, biochemistry, and physiology, as well as the inhibition tolerance to salt stress [41] (Fig. 2).
of growth and photosynthesis and the reduction of grain yield Other Ca2+ signal response proteins also play a role in salt stress
[1,127,128]. Roots take up water and nutrients and have a key role signaling. The calmodulin protein OsMSR2, OsCam1-1, OsCCD1,
in plant growth, development, and survival. The root system is the OsCam1, and the CML protein OsCBL8 act as Ca2+ sensors and
first tissue to perceive salt stress [129]. Transgenic rice lines that improve rice tolerance to salt stress [142–146]. The CDPK/CPK pro-
overexpressed OsAHL1, OsHAL3, and OsMADS25 had greater root teins OsCPK4, OsCPK7, and OsCPK12 help to lower Na+ accumula-
volume under saline conditions and exhibited enhanced salt avoid- tion and maintain osmotic balance under salt stress conditions
ance [116,130,131]. Transgenic lines that overexpressed OsiSAP8 [112,147,148].
and OsCFM2 had higher chlorophyll contents and photosynthetic
rates than wild-type plants under abiotic stress [132,133]. 4.2. Hormonal regulation during salt stress

Downstream of the early salt signaling phase, phytohormone

4. Salt stress signaling in rice
levels change, and the salt-induced signaling cascade ultimately
result in adaptive responses [14]. Phytohormones are crucial
As sessile organisms, plants must cope with abiotic stresses
endogenous chemical signals that coordinate plant growth and
such as soil salinity [19]. To adapt to salt stress, plants have devel-
development under both optimal conditions and environmental
oped various strategies to integrate exogenous salinity stress sig-
challenge [14]. Response and adaptation to salt stress require the
nals with endogenous developmental cues to optimize the
integration and coordination of multiple phytohormones, includ-
balance between growth and stress response [134]. Na+ influx
ing abscisic acid (ABA), ethylene (ETH), jasmonic acid (JA), gib-
occurs through voltage-insensitive monovalent cation channels
berellic acid (GA), cytokinin (CK), and salicylic acid (SA), which
(VICs) [135,136]. These channels are regulated using bivalent
regulate normal growth and mediate responses to abiotic stress
cations such as Ca2+ to maintain ion homeostasis [31]. Early salt
[14,149–151].
signaling responses are induced, including Ca2+ signaling, and
these early Na+-induced signals reduce Na+ import [14]. Ca2+ acts
as a second messenger, and its levels are rapidly elevated when 4.2.1. Abscisic acid
plants encounter abiotic stresses [31]. An initial Ca2+-dependent ABA is the central regulator of abiotic stress tolerance in plants
signaling network is involved in salt stress responses and includes [151–153]. It has a major role in the salt stress response, regulating
both Ca2+ transport and downstream targets such as calmodulin stomatal closure, ion homeostasis, salt stress–responsive gene
(CaM), CMLs (CaM-like proteins), CDPK/CPK (calcium-dependent expression, and metabolic changes [14]. Salt stress causes an
protein kinase), CBLs (calcineurin B-like proteins), and CIPKs increase in ABA accumulation, and exogenous ABA may alleviate
(CBL-interacting protein kinases) [31,137]. the deleterious effects of salt stress [154,155]. ABA signal transduc-
17
C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

Fig. 2. Known salt stress signaling pathways in rice. (1) The most classic pathway is the SOS signaling pathway (left), which consists of OsSOS3/OsCBL4, OsSOS2/OsCIPK24,
and OsSOS1. It is important for sensing salt-induced Ca2+ signals and regulating ion homeostasis by removing excess Na+ from cells or compartmentalizing it in the vacuole.
(2) In the ABA-dependent pathway (middle), salt stress induces ABA accumulation and promotes ABA binding to PYR/PYL ABA receptors such as OsPYR/RCAR5, leading to the
inactivation of core ABA-signaling components (PP2Cs such as PP108). The PYL-ABA-PP2C complex forms, releasing SnRK2s such as SAPK4 from association with and
inhibition by PP2Cs. The released SnRK2s are activated through autophosphorylation and in turn activate the expression of many downstream effectors. (3) In one typical
ABA-independent pathway (right), ethylene regulates stress responses. OsSIT1 mediates salt sensitivity by activating MPK3/6, thereby promoting ethylene biosynthesis and
ROS accumulation. The ethylene-response genes MHZ6/OsEIL1 and OsEIL2 negatively regulate salt tolerance by controlling OsHKT2;1 expression and Na+ uptake in rice roots.

tion requires three core components: PYR/PYL/RCAR ABA receptors
(PYLs), type 2C protein phosphatases (PP2Cs), and class III SNF-1-
related protein kinase 2 s (SnRK2s) [156]. Under salt stress condi-
tions, ABA binds to PYR/PYL/RCAR receptors, which then interact
with PP2Cs and inhibit their activity, thus releasing SnRK2s from
repression [157–159]. SnRK2s phosphorylate various ABA-
responsive element (ABRE)-binding protein/ABRE-binding factor
(AREB/ABF) transcription factors, which further regulate ROS scav-
enging, ion homeostasis, and stomatal closure in response to salt
stress [14,160–162]. The ABA biosynthesis genes OsNCED3 and
OsNCED5, encoding 9-cis-epoxycarotenoid dioxygenases, increase
ABA levels and enhance salt stress tolerance [163,164]. The rice
18
ABA receptor gene OsPYL/RCAR5 is a positive regulator of the ABA
signal transduction pathway in abiotic stress tolerance [165,166]
(Fig. 2). The PP2C genes (such as OsPP108) negatively regulate
ABA signaling but positively regulate abiotic stress signaling
[167] (Table 5; Fig. 2). The transcription factors OsABF1/OsbZIP12,
OsABF2/OsbZIP46, OsBZ8/OsbZIP05, OsbZIP71, OsWRKY45, SNAC1,
OsNAC2, ONAC022, OsMADS25, OsMYB48-1, OsMYB91, and
OsRHP1 play positive roles in ABA-mediated salt tolerance of rice
[62,116,168–179], whereas OsABI5/OsbZIP10, ZFP185, and
Oshox22 play negative roles [180–183]. OsbZIP23 directly targets
the ABA synthesis gene OsNCED4 and the ABA signaling component
gene OsPP2C49, which act as positive and negative regulators,
C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

Table 5
Phytohormones that mediate salt stress responses.

Family Group Effect on Relevant genes References

tolerance
ABA Synthesis Positive OsNCDE3, OsNCED5 Huang et al. [163], Huang et al. [164]
Signal Positive OsPYL/RCAR5, OsABF1/OsbZIP12, OsABF2/OsbZIP46, OsBZ8/ Liu et al. [62], Xu et al. [116], Kim et al. [166], Hossain et al. [168],
OsbZIP05, OsbZIP71, OsWRKY45, SNAC1, OsNAC2, ONAC022, Hossain et al. [169], RoyChoudhury et al. [170], Mukherjee et al.
OsMADS25, OsMYB48-1, OsMYB91, OsRHP1 [171], Nakagawa et al. [172], Amir Tao et al. [173], Hu et al. [174],
Shen et al. [175], Hong et al. [176], Zhu et al. [177], Xiong et al.
[178], Zeng et al. [179]
Negative OsPP108, OsABI5/OsbZIP10, ZFP185, Oshox22 Singh et al. [167], Zou et al. [180], Bhattacharjee et al. [182], Zhang
et al. [183]
Feedback OsbZIP23 Zong et al. [184]
regulation
ETH Signal Negative MHZ6/OsEIL1, OsEIN2, OsSIT1, OsAP23, OsERF922, OsEREBP1, Yang et al. [185], Yang et al. [186], Li et al. [187], Serra et al. [188],
OsEREBP2 Zhuang et al. [189], Liu et al. [190], Jisha et al. [191]
Positive OsDOF15, OsBIERF3 Qin et al. [192], Cao et al. [193], Cao et al. [194]
GA Catabolism Positive OsGA2ox5, OsCYP71D8L Shan et al. [195]
Signal Negative OsSLR1 Mo et al. [196]
Auxin Signal Positive RBG1 Lo et al. [197]
Negative OsNAC2, OsTIR1, OsAFB2 Shen et al. [175], Xia et al. [198], Mao et al. [199])
CK Catabolism Negative OsCKX2 Joshi et al. [200]
Signal Negative OsRR9, OsRR10, OsRR22 Gao et al. [124], Zhang et al. [125], Wang et al. [201]
Positive OsAGO2, OsBG3, OsAHP1, OsAHP2, OsNAC2 Shen et al. [175], Mao et al. [199], Yin et al. [202], Xiao et al. [203],
Sun et al. [204]
BR Signal Negative GW5L, osa-miR1848 Tian et al. [205], Xia et al. [206]
Positive GSK2, OsCYP51G3 Xia et al. [206], Koh et al. [207]
JA Catabolism Positive OsCYP94C2b Kurotani et al. [208]
Signal Positive OsJAZ8, OsJAZ9 Wu et al. [209], Peethambaran et al. [210]
SA Signal Positive RSOsPR10 Yamamoto et al. [211], Takeuchi et al. [212]

respectively, and it can therefore feedback-regulate ABA signaling
and biosynthesis in response to abiotic stress [184] (Table 5).
4.2.2. Ethylene
Etiolated seedlings treated with ethylene exhibit a double
response, i.e. the promotion of coleoptile growth and the inhibition
of root elongation [213]. The function of ethylene in rice salt toler-
ance has been studied extensively. Promotion of ethylene biosyn-
thesis and signal transduction can enhance plant salinity
tolerance, whereas their inhibition increases sensitivity to salinity
in Arabidopsis and soybean [214,215]. However, in tomato, the
direct ethylene precursor ACC causes Na+ accumulation and oxida-
tive stress in leaves and promotes leaf senescence under salinity
stress [216–218]. Ethylene treatment of Nipponbare rice seedlings
increased their sensitivity to salinity, whereas treatment with 1-
MCP (a blocker of ethylene perception) enhanced salinity tolerance
[185,219]. Salt Intolerance 1 (OsSIT1), a lectin receptor-like kinase,
is an ethylene sensor that positively mediates salt sensitivity by
activating MITOGEN-ACTIVATED PROTEIN KINASE3/6 (MPK3/6),
thereby promoting ethylene biosynthesis, ROS accumulation, and
sensitivity to salt stress [187] (Table 5; Fig. 2). The ethylene
response factors (AP2/ERFs), such as OsAP23, OsERF922, OsEREBP1,
and OsEREBP2, as well as the ethylene signaling component genes
MHZ6/OsEIL1 and OsEIL2, are positively regulated by ethylene sig-
naling and negatively affect salt tolerance in rice [185,188–191]
(Table 5; Fig. 2). The DOF transcription factor OsDOF15 and the
ethylene-responsive element binding protein (EREBP) transcrip-
tion factor OsBIERF3 positively regulate primary root elongation
under salt stress by restricting ethylene biosynthesis [192–194]
(Table 5).
4.2.3. Gibberellic acid
GA is an important hormone that regulates plant growth and
has been linked to the regulation of growth under abiotic stress
[220]. The GA catabolic pathway genes gibberellin 2-oxidase 5
(OsGA2ox5) and OsCYP71D8L reduced GA accumulation and
enhanced plant salt tolerance by retarding growth [195,221], sug-
gesting a negative role for GA in rice salt tolerance. The rice homo-
19
log of the Arabidopsis DELLA gene Slender rice1, OsSLR1, encodes a
GA signaling component that regulates mesocotyl and root growth,
specifically in the dark and under salt stress [196] (Table 5). There-
fore, rice growth inhibition under salt stress may be an active
adaptation mechanism whereby rice reduces GA levels or GA sig-
naling in response to changing environmental conditions [134].
4.2.4. Auxin
Auxin plays an important role in root system growth in
response to local soil conditions [134,222]. Rice Big Grain 1
(RBG1) regulates cell division, auxin accumulation, and tolerance
to drought, salt, and heat stresses [197]. The two rice auxin recep-
tor genes OsTIR1 and OsAFB2 are targeted by OsmiR393, downreg-
ulated the expression of OsAUX1 (an auxin transporter) and OsTB1
(a tillering inhibitor), repressing auxin signaling and leading to
more tillers, earlier flowering, and reduced salt and drought toler-
ance [198]. The NAC transcription factor OsNAC2 decreases auxin
biosynthesis, content, and gene responses while increasing cytoki-
nin (CK) biosynthesis gene expression and CK content, thereby
integrating the auxin and CK pathways to modulate rice root devel-
opment under normal and saline conditions [175,199] (Table 5).
4.2.5. Cytokinins
CKs function in the control of plant adaptation to environmental
stress. In Arabidopsis, plants with reduced levels of various CKs
exhibit enhanced salt tolerance [223], whereas exogenous CK
application increases salt tolerance in Solanum melongena [224].
The cytokinin oxidase OsCKX2, an enzyme of the CK degradation
pathway, negatively regulates salt stress tolerance by controlling
CK levels [200]. The CK response regulators OsRR9, OsRR10, and
OsRR22 inhibit the response to CK signaling by a negative feedback
mechanism and improve rice tolerance to salt stress [124,125,201].
OsAGO2 increases salt tolerance by activating the expression of
OsBG3 and altering CK distribution [202,203]. Two rice authentic
histidine phosphotransferases, OsAHP1 and OsAHP2, and the NAC
transcription factor OsNAC2 mediate CK signaling and enhance
plant tolerance to salt stress [199,204] (Table 5).
C. Liu, B. Mao, D. Yuan et al.
4.2.6. Brassinosteroids
Brassinosteroids (BRs) are plant steroid hormones that play
essential roles in plant growth, development, and abiotic stress
responses [225]. Exogenous application of BR enhances salt toler-
ance in rice [226]. GW5-Like (GW5L) positively regulates BR sig-
naling by repressing the phosphorylation activity of GSK2 and
confers salt stress sensitivity [205,207]. The rice microRNA osa-
miR1848 targets the obtusifoliol 14a-demethylase gene OsCYP51G3
and mediates the biosynthesis of phytosterols and BR during
development and in response to stress [206] (Table 5).
4.2.7. Jasmonic acid
Jasmonic acid (JA) is required for the inhibition of root elonga-
tion and the activation of antioxidant enzymes upon exposure to
high salinity [227]. Endogenous JA accumulates in rice roots under
salt stress, and exogenous JA improves salt stress tolerance in both
rice and wheat [228,229]. Overexpression of the Cyt P450 family
gene OsCYP94C2b, encoding a JA-catabolizing enzyme, reduces JA
content and improves performance at high salt concentrations
[208]. The plant-specific TIFY transcription factors OsJAZ8 and
OsJAZ9 act as negative regulators of jasmonic signaling but posi-
tively modulate salt stress tolerance in rice [209,210] (Table 5).
4.2.8. Salicylic acid
Salicylic acid (SA) plays an important role in plant salt toler-
ance. Exogenous SA application enhances the antioxidant system,
increases the synthesis of osmolytes, and promotes photosynthesis
and nitrogen fixation under salt stress [230–232]. The
pathogenesis-related protein RSOsPR10 (root specific rice PR10)
is regulated antagonistically by JA/ethylene and SA signaling and
improves plant tolerance to salt stress [211,212] (Table 5).
4.3. Conclusions
Over the course of evolution, plants have developed the capac-
ity to detoxify the excessive Na+ levels that accompany high salt
concentrations and to utilize multiple strategies for the alleviation
of salt stress damage [31]. Plant salt responses caused by hyperos-
motic tension are closely linked to Ca2+ channels and Ca2+ signaling
[31,233]. (1) The most typical Ca2+ signaling pathway is the SOS
pathway, in which OsSOS3/OsCBL4 senses the cytosolic Ca2+ signal
elicited by salt stress and phosphorylates OsSOS2/OsCIPK24, which
activates OsSOS1, a plasma membrane Na+/H+ antiporter that reg-
ulates ion homeostasis by transporting excess Na+ out of cells or
compartmentalizing it in the vacuole [41] (Fig. 2). (2) Phytohor-
mones mediate the response to various environmental stresses,
including salt stress, and thus regulate plant growth adaptation
[9,134]. ABA is the hormone usually associated with major plant
responses to stress [153]. In the ABA-dependent pathway, the
PYL-ABA-PP2C complex forms, releasing SnRK2s such as SAPK4
to phosphorylate many downstream effectors (Fig. 2). (3) Ethylene
is also a widely known abiotic stress signal. For example, the
receptor-like kinase OsSIT1 mediates salt sensitivity by activating
MPK3/6, which promotes ethylene biosynthesis and ROS accumu-
lation [187] (Fig. 2). OsEIL1 and OsEIL2 are ethylene response genes
that repress the expression of K+ transporters [185] (Fig. 2). In brief,
plants have developed various signaling cascades for sustaining ion
homeostasis and cell turgor pressure, avoiding cellular oxidative
damage or nutritional imbalances, and optimizing the balance
between growth and stress responses under salt stress.
5. Future perspectives
Ongoing soil salinity threatens rice production and future food
security, and breeding and cultivation of salt-tolerant varieties is
20
The Crop Journal 10 (2022) 13–25
the most effective means for overcoming this environmental chal-
lenge [23]. Many salt response genes have been cloned and identi-
fied in the past three decades, and mechanisms of rice salt stress
tolerance have been characterized. Two major approaches have
been used to improve crop salt tolerance: (1) exploitation of natu-
ral genetic variation between tolerant and sensitive varieties, and
(2) generation of transgenic plants with novel genes or altered
expression levels of existing genes [234]. However, the application
of this fundamental knowledge to improve salt stress tolerance of
crops in the field is a slow and challenging process.
Because salt tolerance is a complex quantitative trait, only a few
haplotypes of genes or loci have been reported that could be used
for molecular marker–assisted breeding. For example, the T67K
and P140A mutations may destabilize the transmembrane domain
or alter the phosphorylation probability, respectively, of
OsHKT1;5/SKC1, thereby influencing rice tolerance to salt stress
[235–237]. The K24E mutation in the SalT protein appears to alter
its interactions with other proteins, affecting its function and influ-
encing salinity tolerance [235,238]. The Saltol quantitative trait
locus (QTL) contributes to salinity tolerance and has been fine
mapped on chromosome 1 using a Pokkali/IR29 recombinant
inbred line (RIL) population, and the simple sequence repeat
(SSR) markers RM493 and RM3412b have been used effectively
in marker-assisted breeding [239–243].
However, marker-assisted breeding has two problems: first,
QTL mapping results based on specific parents are not usually uni-
versal and cannot readily be applied to breeding populations. Sec-
ond, salt tolerance is controlled by multiple minor genes, and these
genes or loci cannot be used effectively to improve quantitative
traits. Genome selection (GS) using SNPs or alleles of the whole rice
genome can be used to predict genomic estimated breeding value
(GEBV) of individuals in rice populations based on allele effects
using a genetic relationship matrix. GS is time-efficient and can
combine pedigree and genotype information, making it superior
to other methods of plant breeding [244,245].
Improvements in crop salt stress tolerance will become more
feasible with the aid of gene editing technologies and advances
in the efficient genetic transformation of different species [246].
Genes that confer salt sensitivity, such as DST, OsRR22, OsEIL1,
OsEIN2, and OsSIT1, could be knocked out to improve rice salt
tolerance [120,125,185,187]. The OsbZIP23 promoter has a
35-nucleotide deletion in the 50 -UTR in the drought-sensitive
IR20 cultivar, and the deleted sequence is associated with
decreased OsbZIP23 expression and reduced tolerance to abiotic
stress relative to Oryza rufipogon [247]. We can also use genome
editing technology for knock-in of the deleted sequence in
cultivated rice.
An understanding of the molecular mechanisms of rice salt tol-
erance can now be combined with the development of molecular
salt tolerance markers, the complete sequencing of plant genomes,
and the widespread use of microarray analysis and genome editing
technology. These powerful techniques offer advantages and pro-
vide solutions to the complex and intriguing trait of plant salt
resistance.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
CRediT authorship contribution statement
Citao Liu wrote the manuscript. Bigang Mao, Dingyang Yuan,
Chengcai Chu, and Meijuan Duan revised and edited the
manuscript.
C. Liu, B. Mao, D. Yuan et al. The Crop Journal 10 (2022) 13–25

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