Hormonal and epigenetic regulation of root responses to salinity stress

Abstract

Salinity stress is a major environmental stress affecting crop productivity, and its negative impact on global food security is only going to increase, due to current climate trends. Salinity tolerance was present in wild crop relatives but significantly weakened during domestication. Regaining it back requires a good understanding of molecular mechanisms and traits involved in control of plant ionic and ROS homeostasis. This review summarizes our current knowledge on the role of major plant hormones (auxin, cytokinins, abscisic acid, salicylic acid, and jasmonate) in plants adaptation to soil salinity. We firstly discuss the role of hormones in controlling root tropisms, root growth and architecture (primary root elongation, meristematic activity, lateral root development, and root hairs formation). Hormone-mediated control of uptake and sequestration of key inorganic ions (sodium, potassium, and calcium) is then discussed followed by regulation of cell redox balance and ROS signaling in salt-stressed roots. Finally, the role of epigenetic alterations such as DNA methylation and histone modifications in control of plant ion and ROS homeostasis and signaling is discussed. This data may help develop novel strategies for breeding and cultivating salt-tolerant crops and improving agricultural productivity in saline regions.

Headnote

ABSTRACT

Salinity stress is a major environmental stress affecting crop productivity, and its negative impact on global food security is only going to increase, due to current climate trends. Salinity tolerance was present in wild crop relatives but significantly weakened during domestication. Regaining it back requires a good understanding of molecular mechanisms and traits involved in control of plant ionic and ROS homeostasis. This review summarizes our current knowledge on the role of major plant hormones (auxin, cytokinins, abscisic acid, salicylic acid, and jasmonate) in plants adaptation to soil salinity. We firstly discuss the role of hormones in controlling root tropisms, root growth and architecture (primary root elongation, meristematic activity, lateral root development, and root hairs formation). Hormone-mediated control of uptake and sequestration of key inorganic ions (sodium, potassium, and calcium) is then discussed followed by regulation of cell redox balance and ROS signaling in salt-stressed roots. Finally, the role of epigenetic alterations such as DNA methylation and histone modifications in control of plant ion and ROS homeostasis and signaling is discussed. This data may help develop novel strategies for breeding and cultivating salt-tolerant crops and improving agricultural productivity in saline regions.

Keywords:

Phytohormone

Root development

Sodium

Potassium

ROS signal

Keywords:

Phenotyping

Breeding

Reactive oxygen species

Tissue tolerance

Sodium exclusion

Potassium retention

Keywords:

Phytohormone

Root development

Sodium

Potassium

ROS signal

1. Introduction

Salinity stress is a major environmental hurdle affecting crop productivity [1,2]. The root is the first organ of plant that is directly exposed to a hyperosmotic and toxic conditions in the rhizosphere caused by soil salinity. The ability of plant roots to adjust to hostile soil conditions are, therefore, critical for the performance of the entire plant.

Root system architecture (RSA) is closely linked with plant productivity [3]. RSA response to salt stress includes alteration in the main root (elongation and root hair development) and lateral root (elongation and density) [4,5], which observed in staple crops such as rice [6], wheat [7], maize [8], and barley [9]. The restrain in the primary root elongation is the predominant factor in remodeling RSA in response to salt stress [10]. Salt stress also hindered formation of lateral roots [6,11]. Moreover, salinity stress reduces the root surface area, mainly attributed to shorter length and smaller density of root hairs [7]. Most of these changes occur via modulation of plant hormonal status caused by salinity. While there is no shortage of literature reporting hormonal cross-talks and signaling in plant adaptative responses to hostile environment [12–16], the specific details of the hormonal control of root halotropism, development, and ionic and ROS homeostasis under saline conditions are dispersed amongst numerous papers. In this review, we have tried to summarize our current knowledge on this matter by focusing on five major hormones involved in root adaptive responses to salinity-namely auxin, cytokinin (CK), abscisic acid (ABA), salicylic acid (SA), and jasmonate (JA). We also discussed the role of epigenetic modifications in this process.

2. Na+ sensing and halotropism

The molecular identity of Na+ sensors remains a mystery [17,18]. Due to multifaceted nature of salt stress, plants experience multiple constraints under saline conditions. These include elevated Na+ levels in the rhizosphere, reduced water availability due to the hyperosmotic stress imposed by salinity, a dramatic increase in reactive oxygen species (ROS) accumulation in plant tissues and a massive disturbance to the cytosolic Ca2+ and K+ homeostasis [19]. These sensors are most likely localized in a root meristem [20], where each of these constraints may be sensed and trigger a broad array of physiological and genetic alterations aimed to optimize plant performance under saline conditions. Also, a typical hallmark of plant sensing of salinity is a rapid (within seconds) elevation in cytosolic Ca2+ levels [21] mediated by glucuronosyltransferase MONOCATION-INDUCED Ca2þ h i i INCREASE

1 (MOCA1). At the same time, it is known that Ca2+ can crosstalk to auxin modulating root development and plasticity. This includes regulation of both lateral root [6,22] and meristem [23] development. Auxin, in turn, could also elicit cellular Ca2+ to mediate downstream genes, thus forming a feedback loop to modulate root development [24].

After sensing the salinity, roots tend to grow away from the saline environment, a phenomenon called halotropism, even if the growth direction is against gravity. This directional change is attributed to redistributing auxin on the side that faces higher NaCl concentrations, achieved by relocating the auxin exporter PINFORMED2 (PIN2) via phospholipase D type (PLD) enzyme PLDf1/2-stimulated endocytosis [25,26] (Fig. 1). Under salinity stress, Ca2+ signal regulates activity of several PLDs [27], which can directly catalyze the formation of phosphatidic acid (PA) [28]. PA signaling then modulates auxin transporters (e.g., PIN2, AUXIN RESISTANT 1 (AUX1), and ATP-BINDING CASSETTE TRANSPORTER type B (ABCB4)), resulting in the auxin asymmetry and contributes to root directional growth under salinity [26,29] (Fig. 1).

Apart from halotropism, plants tend to develop shallower roots by reducing the gravitropic response to cope with salinity [30,31]. In Arabidopsis, growing on a saline medium resulted in a gravistimulation resistance, ascribed to localization and transcriptional level of PIN2. This weakened gravitropism response is NaCl dosedependent and likely involves SOS signaling pathway [31]. The RSA with shallow roots mitigates the yield penalty of plants that grow in the saline field. DEEPER ROOTING 1 (DRO1) is predominantly expressed in root tips and controls lateral root angles in plants. The loss function mutant atdro1 exhibited shorter primary root and horizontally orientated lateral roots in Arabidopsis via disrupting auxin gradient formation [32]. In rice, a DRO1 homolog qSOR1 (quantitative trait locus for SOIL SURFACE ROOTING 1), which is negatively regulated by auxin signaling, controls the soil surface-root development. Compared to the rice without soilsurface roots, the near-isogenic line with homozygous of qSOR1 showed less yield reduction under saline conditions [30].

3. Inhibition of primary root elongation

Salinity-induced modulation of auxin distribution/transportation, including relocation or concentration change of auxin efflux (PINs) and influx (AUX1/Like AUX1) transporters, also affects primary root elongation (Fig. 2A). Acyl acid amido synthetases, encoded by group Ⅱ of GRETCHEN HAGEN 3 (GH3) genes, catalyze IAA to conjugate with amino acids, mediating cellular auxin concentration. Casanova-Sáez et al. [33] demonstrated that a mutant without group Ⅱ GH3 pathway exhibits longer primary roots under saline conditions. It remains to be answered of how the change in auxin polarity/concentration affects root growth. The plausible model is that auxin modulates downstream gene expressions via direct interaction with TRANSPORT INHIBITOR RESPONSE1 (TIR1)/ AUXIN-SIGNALING F-BOX (AFB) receptors. The latter are involved in salinity-induced inhibition of root elongation (Fig. 2A). Mutation of tir1 afb2 showed longer roots than that in wild type under saline conditions [34]. TIR1/AFB has also recently been identified as controlling H+ flux to modulate auxin-induced root growth inhibition. Auxin regulates root growth by activating two antagonistic signaling pathways: (1) cell surface TRANSMEMBRANE KINASE1(TMK1)mediated H+ efflux acidifying the apoplast to prompt root growth and (2) more dominant intracellular TIR1/AFB-dependent apoplast alkalinization leading to auxin-induced rapid growth inhibition [35].

Several studies also pointed out at the critical role of ROS in interaction between salt stress and auxin response and their contribution to RSA. Auxin could induce a redox balance in root tissues. Auxin regulates ASCORBATE PEROXIDASE 1 (APX1) activity through S-nitrosylation/denitrosylation to alter H2O2 level in root, thus affecting RSA in Arabidopsis [36] (Fig. 2A). Auxin receptor mutant tir1 afb2 exhibited less ROS (H2O2 & O 2 ) accumulation in the root in response to NaCl treatment [34]. Redox status in turn affects auxin distribution in the root. An auxin-responsive gene IAA CONJUGATE RESISTANT 4 (IAR4) regulates main root growth in response to saline conditions via controlling ROS-related auxin distribution [37] (Fig. 2A). The primary root growth was remarkably restrained in iar4 mutants under salinity, which was concomitant with suppressed PINs expression and ROS scavenging. At the same time, exogenous glutathione or auxin supplementation recovers the iar4 phenotype [37]. Plants exposed to H2O2 treatment developed shorter primary roots and abundant lateral roots, which is attributed to auxin redistribution in the main root and less auxin accumulation in lateral roots primordia and emerging lateral root tips [38].

ABA induces growth inhibition via crosstalk to auxin (Fig. 2A). Recently, an ABA- ASPARAGINE-RICH PROTEIN (NRP)-related pathway was identified in response to stress conditions. Stresstriggered ABA accumulation induces the expression of NRP, which boosts vacuolar degradation of the PHYTOCHROME-ASSOCIATED SERINE/THREONINE PROTEIN PHOSPHATASE3 (FyPP3), subsequently resulting in dephosphorylation of transcription factor ABSCISIC ACID INSENSITIVE 5 (ABI5) [39] (Fig. 2A). ABI5 can negatively regulate PIN1 accumulation and inhibit root elongation [40]. Moreover, the protein phosphatase ABI1 dephosphorylates threonine residue (Thr947) on the C terminus of PM-localized ARABIDOPSIS PLASMA MEMBRANE H+ -DEPENDENT ADENOSINE TRIPHOSPHATASE 2 (AHA2), consequently resulting in less H+ efflux [41], which will result in apoplastic alkalinization thus inhibiting root growth [35] (Fig. 2A). Wu et al. [42] found that ABA employs the NRP-FyPP3 pathway to inhibit primary root elongation under stress conditions by modulating auxin transportation. NRP and FyPP3 are involved in the polarity formation of PIN2. The former also controls PIN2 degradation speed in the vacuole. The lost function of NRP or FyPP3 resulted in short roots due to the accumulation of auxin in the root meristem and the inhibition of auxin transport [42]. ABA-induced NRP can interact with FyPP3 and get dephosphorylated [39], thus promoting vacuolar degradation of PIN2 and suppressing auxin transfer to the elongation zone, restraining the primary root growth [42] (Fig. 2A).

4. Suppression of meristematic activity

The salinity-induced shorter roots is also attributed to reduced cell numbers of the root meristem. Under normal conditions, CK controls meristem activity, alongside of auxin [43]. CK is perceived by ARABIDOPSIS HISTIDINE KINASE (AHKs) receptors, which the latter activate ARABIDOPSIS HISTIDINE PROTEINS (AHPs) to phosphorylate B-type ARABIDOPSIS RESPONSE REGULATORs (ARRs) to induce the downstream genes [44]. In root meristem, CK regulates auxin via ARRs. CK-induced ARR1/12 upregulate auxin repressor gene SHORT HYPOCOTYL2 (SHY2/IAA3) to suppress PINs and cause auxin redistribution [43,45] (Fig. 2A). ARR1 could also upregulate GH3 to catalyze IAA conjugation [46] or induce auxin biosynthesis enzyme L-TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA1) [47] to mediate auxin level (Fig. 2A). CKs therefore modulate auxin levels in the root transition zone and set the boundary of cell division and differentiation [46]. As auxin could induce the degradation of SHY2 to maintain auxin transport and cell division [43], a crosstalk between CK and auxin controls root meristem size, and stress-induced alteration in either of them would affect meristem growth (Fig. 2A).

Salinity results in a decrease in endogenous CK levels [48], and the CK receptor AHK1 acts as a positive regulator in response to salt stress [49]. Interestingly, the CK deficient phenotype, whether achieved by overexpression of CK conjugation enzymes genes (CYTOKININ OXIDASES/DEHYDROGENASES, CKXs) [48,50] or mutation of CK receptor genes (AHKs) [48], AHPs [51], B-type ARRs [52], show enhanced salinity tolerance.

Likewise, salinity reduces auxin level by downregulating PIN 1/3/7 expression and suppresses auxin signal by stabilizing auxin signal repressor AUXIN RESISTANT 3 (AXR3)/INDOLE-3-ACETIC ACID 17 (IAA17) in root meristem, consequently resulting in inhibition of meristem development [53]. This process likely involves NaCl-induced NO accumulation [53,54]. Salinity rapidly alters redox potential of the root cap and the quiescent center as well as impacts auxin distribution (via AUX1 and PINs), subsequently altering meristem structure and development [55]. Auxin mediates downstream genes through DNA-binding transcription factors (TFs) named ARABIDOPSIS RESPONSE FACTORS (ARFs) [56], of which ARF2 plays a role in regulating ABA response in root meristem growth. ABA restrains root meristem growth and PINs expressions in root tip, where the ABA-induced ARF2 antagonistically regulates the response [57,58]. Recently, Luo et al. [59] revealed that ABA-induced ABI4 binds to cell cycle genes CYCLIN B1;1 (CYCB1;1) and CYCLIN-DEPENDENT KINASE B2;2 (CDKB2;2) promoters to suppress their expression, thus impairing cell division and inhibit meristem size (Fig. 2A).

Jasmonate signaling also contributes to inhibition of meristem growth by salt. Salinity induces JA signaling by upregulating JASMONATE-ZIM DOMAIN 3 (JAZ3), CORONATINE INSENSITIVE 1 (COI1), and JASMONATE RESPONSE LOCUS 1 (JAR1) genes in root meristem and stele of differentiation zone to inhibit root elongation in Arabidopsis [60]. In wheat, a salinity-inducible JA biosynthesis gene ALLENE OXIDE CYLASE 1 (AOC1) mediates JA signaling component MYC2 (a basic-helix-loop-helix (bHLH) TF) thus inducing JA accumulation and shortening main root, concurrently enhancing salinity tolerance [61]. JA-induced short root predominantly attributed to perturb quiescent cells division in the root meristem, of which AP2-domain TFs PLETHORA (PLT1/2) play an essential role in the process, especially for growth recovery under salinity stress [62]. Jasmonate represses the PLT1/2 expressions via direct interaction of MYC2 and PLT1/2 promoters [63] (Fig. 2A). Furthermore, auxin and its responsive TF ARF2 also regulate the expression and activity of PLTs [57,64], suggesting that crosstalk between JA and auxin regulates root meristem activity in response to salinity stress.

5. Modulation of the lateral root development

Salinity induces accumulation of ABA and auxin in the lateral roots (LRs) [8]. Mild salinity (25/50 mmol L1 NaCl) treatments cause the proliferation of lateral roots and a shorter primary root in Arabidopsis, where the proliferated LRs were abolished in mutant aux1-7 [65]. The increased LR is owed to more LR primordia formed from pre-emergence to the emergence stage [65]. This stressinduced morphogenic response is likely because a lower-level ABA was induced in mild salt stress, thus prompting LR primordia via auxin signal [14]. Severe salt stress results in an extensive ABA accumulation in LRs, where ABA mediates asymmetric localization of PIN1 to control auxin distribution in LR primordia, inhibiting LR initiation [8] (Fig. 2B). ABA signal also controls the LR elongation in response to NaCl treatment. The postemergence lateral root entered a quiescent stage due to a suppressed cell cycle, which greatly reduced the LR elongation rate in Arabidopsis for the first several days after salinity occurred [66]. This phenomenon is attributed to NaCl-induced ABA signal in the root endodermal layer [66] (Fig. 2B). The salt stress-triggered endodermal ABA signal was also found to be critical to the endodermal suberization process, as the formation of the suberized layer is considered as a protective mean under saline conditions to reduce Na+ loading [67,68].

Auxin and ABA modulate several types of TFs to control LR developments. NAC proteins are a TF family with the NAC domain. Several NAC TFs are involved in lateral root growth via crosstalk to phytohormone signaling, such as auxin and CK [69–71]. In Arabidopsis, NAC1/2 transduce auxin signal to boost LR formation [69,71], OsNAC2 interacts with auxin/ CK downstream genes (GH3, ARF, CKX) to manipulate root development in rice [70]. LATERAL ORGAN BOUNDARIES (LOB) DOMAIN/ASYMMETRIC LEAVES2-LIKE (LBD/ASL) are TFs that control plant growth, including lateral root development, of which several (LBD16/ASL18 [72], LBD18/ASL20 [73], LBD29/ASL16 [74]) are under regulation of the auxin-ARF pathway. LBD14, on the other hand, was found specifically downregulated by ABA (rather than auxin), thus inhibiting LR formation [75]. Another LR primordia-localized TF WRKY46 was found to control LR development via regulating auxin levels and ABI4 activity under salt stress conditions [76]. The expression of WRKY46 was downregulated by ABA, thus restraining LR initiation and emergence [76] (Fig. 2B).

6. Root hair formation

Salinity inhibits root hair development and growth, which is considered as an adaptative response to reduce exposure surface area to salt. Arabidopsis halophytic relative Schrenkiella parvula exhibited fewer root hair when growing at 100 mmol L1 NaCl than in no-salt environment [77], and the same results have been reported for barley [9]. Root hair formation can be categorized into three types based on the different developmental patterns: random root hair (e.g., rice [78]), asymmetric-distributed root hair (e.g., Brachypodium distachyon [79]), and hair cell line intersperse with non-hair cell line (e.g., Arabidopsis [80]). The regulation of root hair development and elongation is intricate [58,81], including different key components such as GLABRA2 (GL2) [82], Rho-type GUANOSINE TRIPHOSPHATASES (GTPase) OF PLANTS (ROPs) [83,84], and ROOT HAIR DEFECTIVE/ROOT HAIR DEFECTIVE SIX LIKE (RHDs/RSLs) [85]. ROP2 positively induces root hair initiation [86], through activating RHD2/RBOHC and ROS signal [87]. GL2 is an upstream regulator to suppress RHD6 [88], which mediates downstream RSLs and other gene expressions to control root hair initiation and elongation. The root hair formation also involves phytohormone signals [89].

Salt stress restrains RHD6-facilitated root hair development in both numbers and length [90]. Jasmonate signaling interferes with RHD6 activity [91] (Fig. 2C). Jasmonate repressor JAZ8 physically associates with RHD6 and inhibits RHD6-RSL1 interaction, leading to defective root hairs. Activation of salt-inducible jasmonate receptor COI1 (by exogenous jasmonate) leads to JAZ proteins degradation [92], consequently upregulating RHD6, RSL1/2/4/5 gene expressions and inducing root hair elongation [91].

ABA directly and indirectly controls root hair growth (Fig. 2C). Under salt conditions, ABSCISIC ACID-RESPONSE ELEMENT (ABRE) BINDING FACTOR 3 (ABF3), which is a crucial component in the ABA signaling pathway, physically interacts with RHD6 protein and suppresses the RHD6-mediated RSL4 activation, consequently inhibiting root hair development [90]. ABA induces OBF BINDING PROTEIN4 (OBP4), a TF repressing cell growth, which suppresses RSL2 expression by interacting with its promoter, therefore perturbing root hair growth [93]. Furthermore, ABA can induce root hair elongation indirectly via regulating auxin polarity transport [94].

Auxin signaling are involved in root hair development, including auxin transporters, auxin-responsive TF, and auxin repressors (Fig. 2C). Mutation of auxin transporter aux1 alters root hair growth in rice [95] and Arabidopsis [96]. Auxin-inducible ARF5 directly binds to the RSL4 promoter and upregulates its expression. The RSL4 subsequently regulates RBOHC/H/J and class III peroxidases to induce ROS generation to mediate root hair development in Arabidopsis [97]. Similarly, auxin induces the RBOH-generated ROS signal to stimulate root hair formation [98]. Moreover, mutation of auxin repressors SHY2/IAA3 and AXR3/IAA17 exhibited opposite phenotypes, stimulated root hair development and defective root hair, respectively. Such difference relies on the cellular abundance of SHY2/IAA3 and AXR3/IAA17 [99].

7. Hormone-mediated ion and ROS homeostasis in salt-stressed roots

Salt stress causes ion imbalance (e.g., Na+ over accumulation and K+ loss) and disturbs root redox homeostasis. There is a growing bulk of evidence that stress hormones (such as ABA, SA, and JA) directly interfere with the above process thus modulating adaptative response in plants. This section reviews the molecular basis of this process.

Calcium. Stress-evoked Ca2+ signaling pathway in plants has been well-studied over the last decades, with downstream targets such as ion transporters and ROS generation [100,101]. Stress hormone ABA was demonstrated to interfere with stress-stimulated Ca2+ cascade [102–104]. ABA plays a predominant role in plant stress response. PYR/PYL/RCARs receptors, group A PROTEIN PHOSPHATASE 2C (PP2C), and SUCROSE NONFERMENTING1 (SNF1)RELATED PROTEIN KINASE 2 (SnRK2) are three key components in ABA signaling [105–107]. SnRK2s are suppressed by PP2C under non-stress conditions. Salinity induces endogenous ABA content. ABA and PYR/PYL/RCARs receptor interact with PP2Cs to form a complex, which releases SnRK2s from the inhibition by PP2Cs [108]. The SnRK2s then regulate downstream targets containing ABA-responsive element (ABRE) motifs in their promoter to transduce the ABA signal [109,110]. In some cases, PP2Cs could interact with other targets such as CIPKs [111]. A PM-localized protein PROLINE-RICH EXTRNSIN-LIKE RECEPTOR KINASE4 (PERK4) alters cytosolic free Ca2+ concentration and Ca2+ -permeable channel current to mediate ABA-inhibited root elongation [102]. Another PM kinase FERONIA (FER) elicits cellular Ca2+ when sensing salinity induced cell wall softening, which is essential for maintaining cell wall integrity [104]. A PP2C ABI2 inhibits the FER activity via dephosphorylation, whereas ABA could inactivate ABI2 to induce FER phosphorylation level and activity [103] (Fig. 3A).

Sodium. The Ca2+ signaling is pivotal for Na+ homeostasis in the root, for instance, the SALT OVERLY SENSITIVE (SOS) pathway for Na+ exclusion and Na+ /H+ EXCHANGER (NHX)-mediated vacuolar sequestration [112]. Although many studies documented hormone-induced phenotypic changes in Na+ contents, only a few papers reported direct regulation of Na+ transporters by hormones in the root (Fig. 3A). Exogenous CK induces cytokinin response regulators ARR1/12 to negatively control the expression of sodium transporter encoded gene HIGH-AFFINITY K+ TRANSPORTER (HKT1;1) in root, leading to Na+ accumulation. A mutation of arr1/12 showed more robust CK-induced expression of HKT1;1 and less Na+ accumulation in shoot [52]. Furthermore, mutation of ABA signaling component abi4 resulted in a salt-tolerant phenotype with less Na+ accumulation due to higher expression of HKT1;1 in root [113]. The PP2C ABI2 physically interacts with the phosphatase interaction (PPI) motif of SOS2 kinase, thus suppressing its activity on activating SOS1, with the evidence that abi2 mutant, which with disrupted interaction to SOS2, showed enhanced tolerance to 150 mmol L1 NaCl treatment [114]. Likewise, impairment of NON-EXPRESSOR of PR GENE1 (NPR1) expression blocks NPR1-dependent SA signaling. The mutant npr1 had higher Na+ influx in the root mature zone, which causes higher Na+ accumulation under prolonged salt stress [115].

Potassium. Under saline conditions, Na+ accumulation in the root leads to PM depolarization, which concomitantly activates depolarization-activated GUARD CELL GATED OUTWARDLYRECTIFYING (GORK) potassium efflux channels that are abundant in root epidermis. This reduces availability of K+ for plants, with the negative impact on growth and development. Moreover, unless the stress-induced K+ loss from the cytosol is compensated by enhanced uptake via HAK/KUP transporters, root cells may undergo a programmed cell death, due to concomitant activation of cell-degrading endonucleases and proteases [116,117]. The ability of root to retain K+ was shown to be tightly regulated by phytohormones (Fig. 3A). Exogenous application of SA prevented K+ loss through the GORK channel and enhances salt stress tolerance in both short (1 h) and long-term (2 weeks) manners [118]. SA pretreatment rapidly reduces NaCl-induced PM depolarization and K+ efflux from the root, contributing to higher shoot K+ content and K+ /Na+ ratio in response to long-term salinity stress [118]. In addition, mutation of SA receptor npr1 showed exaggerated PM depolarization and K+ loss compared with wild type in response to NaCl treatment [115]. ABA and NaCl induce SnRK2.6 (OPEN STOMATA 1, OST1) to activate K+ inward channel KAT1 and facilitate K+ uptake [119]. A clade A PP2C HIGHLY ABA-INDUCED2 (HAI2)/K+ TRANSPORTER 1 (AKT1)-INTERACTING PP2C1 (AIP1) is highly inducible by ABA-PYL5 [120], which also plays a role in Ca2+ CBLCIPK signaling to control K+ channel AKT1 [111,121]. The HAI2/ AIP1 physically interact with the kinase domain of CIPK6 and CIPK23, inhibiting their phosphorylation on downstream potassium AKT1 channel [111]. When stress occurs, both ABA-PYL5 or Ca2+-CBL1 could directly bind and inactivate HAI2/AIP1 to resume the CIPK6/23-induced AKT1 activity [111,120,121]. Likewise, AKT2 activity can be suppressed by an ABA-responsive PP2C, and ABA upregulates AKT2 expression [122]. K+ uptake transporter 6 (KUP6) and its homologs (KUP2, KUP8) activities are shown to operate under control of ABA and auxin [123,124]. Exogenous auxin alleviates salinity-induced adverse effects, partially via strengthening K+ retention in the root tissue [125]. The auxinresponsive TF ARF2 regulates K+ uptake via HAK5. ARF2 interacts with the promoter of HIGH AFFINITY K+ TRANSPORTER5 (HAK5) gene to suppress its expression. Phosphorylation of ARF2 could induce HAK5-mediated K+ uptake [126]. Auxin signal regulates apoplastic acidification via PM-localized H+ -ATPase-mediated H+ flux to control root growth [35].

ROS homeostasis. Effective control of redox homeostasis is essential for salt tolerance. NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE (NADPH) OXIDASE/RESPIRATORY BURST OXIDASE HOMOLOG (RBOH) primarily contributes to salinityinduced ROS generation, of which the activity could regulated by hormone signals [12] (Fig. 3B). Auxin stimulates ROS generation through ARF5-RSL4-activated RBOHC/J [97]. In addition, auxin inhibits APX1 activity via denitrosylation, leading to H2O2 accumulation in root [36]. ABA mediates ROS signal through RBOHD and RBOHF in guard cells and roots [127], and the ABA-activated SnRK2 (OST1) can phosphorylate Ser13 and Ser174 on RBOHF to induce ROS generation in Arabidopsis [109,128]. Salinity-induced RBOHD expression is ABI4 dependent. ABI4 binds with and facilitates RBOHD transcription, causing ROS overaccumulation [129].

Both JA and SA bolster ROS elimination. JA application mitigates salinity-induced oxidative damage in wheat seedlings by enhanced ROS scavenging, with upregulation of antioxidants activity and gene expression, such as SOD, POD, CAT, and APX [130,131]. Also, the TF MYC2 in JA signaling upregulates VITAMIN C DEFECTIVE (VTC) and GLUTATHIONE SYNTHETASE (GSH) gene families to activate ascorbate and glutathione synthesis pathways for antioxidants accumulation [132]. Exogenous SA reduces salinity-induced H2O2 accumulation [133]. Overexpression of SA receptor NONEXPRESSOR of PR GENE1 (NPR1) confers oxidative tolerance to plants through upregulation of ROS scavenging-related genes such as APX and SOD [134]. Nevertheless, mutation of npr1 is more sensitive to ROS stress than wild type [115]. CK has a negative effect on salinity stress tolerance in Arabidopsis, partially due to the fact that higher endogenous CK level (by overexpression of biosynthetic enzyme gene ISOPENTENYL TRANSFERASE8 (IPT8)) induces ROS production and decreases the activity of enzymatic antioxidants in root under saline conditions [135].

With regulating root development, ionic and ROS homeostasis in response to salinity, phytohormone also plays a role in epigenetic modifications, such as histone acetylation/methylation, chromatin and microRNA modification, and DNA methylation [136]. The salinity stress-induced epigenetic modification in root and feasible genetic approaches for salt tolerance improvement are discussed in the next section.

8. Epigenetic modifications and their contribution to plant adaptation under salinity stress

Epigenetics is the field of study that investigates how gene expression can be heritably altered without altering the DNA sequence [137]. DNA methylation and histone modifications are two epigenetic mechanisms that affect gene expression: DNA methylation attaches a methyl group to a DNA molecule, influencing transcription factor binding, while histone modifications alter protein structure around DNA, affecting DNA packaging and accessibility to TFs [138]. These mechanisms provide insights into the modulation and control of gene expression, allowing plants to adapt to environmental stressors like salinity and modulate growth and development [139]. Salinity stress can cause modifications to DNA methylation and histone alterations, resulting in altered expression of genes controlling ion balance and transport – hence, plant adaptive responses [140–142] (Table 1).

DNA methylation serves as a fundamental mechanism in modulating stress-induced gene expressions patterns, including many transporter genes. Methylation directly affects DNA structure and contributes to long-term regulation of gene expression patterns under different environmental conditions [143,144]. In a salttolerant ecotype of Arundo donax, DNA methylation allowed to maintain optimal ion homeostasis through the regulation of ion transporter expression, thereby preventing the build-up of harmful Na+ and Cl ions within the plant cells [145]. In rice plants, the expression of OsHKT1;5 in response to salinity was governed by a synergistic action of a transcriptional complex comprising OsSUVH7 (a reader of DNA methylation), OsBAG4 (a chaperone), and OsMYB106 (a TF) [146]. Specifically, the promoter region of OsHKT1;5 is bound by OsMYB106 and OsSUVH7, activating the expression of this gene.

DNA methylation also regulates the expression of MYB74, a salt-induced R2R3-MYB family TF that exerts a major influence on the plant's defense against salt stress by activating related genes in maintaining the balance of Na+ and K+ ions and enhancing the tolerance of a plant to salinity [147]. Similarly, Shahid [148] investigated the salt stress impact on the methylation pattern of Miniature Inverted Repeat Transposable Elements (MITEs) in the OsHKT1;5 genes of rice. MITEs are small DNA sequences that can move around the genome and influence gene expression. This study found that under salt stress, an elevation in methylation levels at the CHH and CHG sites of these MITEs was observed in the OsHKT1;5, thus affecting plant Na+ /K+ homeostasis and preventing salt damage to the plant.

Plants respond to salt stress by intricately interacting with different cellular processes, such as the dynamics of histone modification that results in modifications to the structure of chromatin [149]. In response to salinity, histone acetylation usually results in gene activation and histone deacetylation frequently results in gene repression. This complex balance between histone acetyltransferases (HATs) and histone deacetylases (HDACs) is essential for the plant's capacity to adapt to changing environments [150]. The genes responsible for maintaining ion homeostasis exhibited activation and distinctive histone modifications when subjected to salt stress. These chromatin alterations, encompassing methylation and acetylation, can affect the structure of chromatin, comprised of DNA and associated proteins found within chromosomes. Consequently, these changes may influence gene expression, potentially augmenting or diminishing the likelihood of gene transcription [151]. Similarly, pretreatment of cotton plants with 10 mol L1 SAHA (suberoylanilide hydroxamic acid; a powerful HDAC inhibitor) rescued cotton plants from 250 mmol L1 NaCl stress, resulting in lower Na+ buildup and enhanced expression of genes involved in ion homeostasis [152]. Additionally, it was shown that SAHA administration produced hyperacetylation of the histone proteins H3K9 and H4K5, suggesting that SAHA functions as an HDAC inhibitor in cotton plants. Furthermore, increased acetylation levels of H3K9 and H4K5 were linked to the elevated expression of genes linked to ion homeostasis; this increased accessibility of these genes' promoter regions to transcription factors resulted in an increase in gene expression. Sun et al. [153] investigated the roles of UBC1 and UBC2 in regulating plant salt tolerance by assessing ion homeostasis and histone modifications. The ubc mutants exhibited a substantial rise in Na+ content and a decline in K+ content in comparison to WT. This suggests that UBC1 and UBC2 serve as key regulators of ion homeostasis in plants under salinity, and additionally, they exert a positive regulatory effect on the expression of MYB42 and MPK4 genes induced by salinity. The chromatin immunoprecipitation assays revealed a weak enrichment of histone H2Bub1 (ubiquitinated histone H2B) levels on the chromatin from MYB42 and MPK4 in the UBC1/UBC2 mutants. This indicates that UBC1 and UBC2 are involved in the histone modification process.

Genome-wide profiling of three histone marks (H3K4me2 - (histone 3 lysine 4 dimethylations; H3K4me3 - histone 3 lysine 4 trimethylations; and H3K9ac- (histone 3 lysine 9 acetylation) was used to identify histone modifications induced by priming salinity treatment in soybeans [153]. Priming with salinity triggered significant modifications in these histone marks, with beneficial impact on ion homeostasis and cell wall regulation. Overall, epigenetic modifications, including DNA methylation and histone modifications, are clearly playing a role in modulation of gene expression and ion homeostasis in plants exposed to high salinity. Different ecotypes of a plant species have unique mechanisms to tolerate salinity, indicating that adaptation to environmental stresses involves complex genetic and epigenetic interactions. Understanding these mechanisms can help develop novel strategies for cultivating salt-tolerant crops and improving agricultural productivity in saline regions.

9. Conclusions and prospects

alinity stress is a major environmental constraint affecting crop productivity, and its negative impact on global food security is only going to increase, due to current climate trends. Salinity tolerance was present in wild crop relatives but significantly weakened during domestication. Regaining it back is a challenging task. Salinity tolerance trait is highly complex, both physiologically and genetically, and is composed of numerous sub-traits operating in highly tissue- and cell-specific manner [163,164]. Therefore, comprehensive studies such as combined single-cell multi-omics analysis would be one way to reveal the underlying mechanism [165]. What is interesting, however, is the fact that despite a massive difference in ability to handle salt load between halophytes (naturally salt-tolerant species) and glycophytes (all staple crops), the formers have no unique mechanisms or traits that are not found in crop species [166]. The only difference is in the efficiency of their operation, with halophytes possessing a set of highly complementary and well-orchestrated mechanisms in place to deal with salinity stress. In lay terms, it all comes to regulation and coordination of activity of various membrane transporters and genes that are present in all plants. Given the critical role of plant hormones in plant growth and development, it would be very surprising if they were not involved in above processes. Indeed, as shown in this work all hormones (auxin, cytokinins, abscisic acid, salicylic acid, and jasmonate) play an important role in controlling root architecture, uptake and sequestration of Na+ and K+ , and regulation of cell redox balance and ROS and Ca2+ signaling in saltstressed roots. A comparative analysis of these traits between halophytes and glycophytes might shed a light on different strategies employed by various plant groups and offer plant breeders new insights and targets for genetic improvement of salinity tolerance traits in major crops. Another aspect that warrants more attention in future studies is epigenetic regulation of salinity tolerance. As shown here, DNA methylation and histone modifications play an essential role if modulating plant ionic and redox balance. Future genome-wide studies and combined single-cell multi-omics studies, as well as comparative analysis of these processes between halophytes and glycophytes may unveil shared patterns and species-specific responses across diverse plant species, offering crop breeders new and previously unexplored opportunities.

CRediT authorship contribution statement

Ping Yun: Writing – original draft, Visualization, Validation.

Cengiz Kaya: Conceptualization, Writing – original draft, Visualization.

Sergey Shabala: Conceptualization, Writing – review & editing, Funding acquisition.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by Australian Research Council and National Natural Science Foundation of China grants to Sergey Shabala.

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ARTICLE INFO

Article history:

Received 16 October 2023

Revised 26 December 2023

Accepted 10 March 2024

Available online 13 March 2024

Footnote

* Corresponding author.

E-mail address: [email protected] (S. Shabala).

References

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