Mechanism of Salt Stress Tolerance in Plants: Role of Cation/H+ Antiporters

INTRODUCTION

The soil salt of salinity is mostly found as NaCl (sodium chloride) which is one of the most adverse and negative effect causing problems in environmental factors of and ecosystem that caused to reduce crop production and productivity worldwide (Mickelbart, Hasegawa, & Bailey- Serres, 2015; Roy, Negrão, & Tester, 2014). It has been estimated that there is about 20% of all of the irrigated soils of the world which may be increased up to 50% of land growing areas due to changing environmental conditions of the globe.

The salinity is causing a loss of about 12 billion US$

each year for agriculture and its products (Munns

& Gilliham, 2015; Pitman & Läuchli, 2006). There are two different stages in plants to which the salty stress caused to decrease or effects to block the morphological and physiological functioning of cells.

The first one is called as osmotic stress phase under which as there are higher salts concentrations in the

soil as compared with the plant root cells caused a reduction of water potential in the soil which caused reduced uptake of water by plant roots (Ali, Rafique, Ali, & Malik, 2020; Miller, Suzuki, Ciftci-Yilmaz, &

Mittler, 2010; Munns & Tester, 2008). The osmotic stage starts just after the initiation of the salt stress on plants due to higher salt concentration in the soil.

It is mostly independent with the salt concentration or ion concentration in the roots hairs, root tips, or in leaves of plants which may cause the stomata closure under salinity stress (Hasanuzzaman, Nahar, Alam, Roychowdhury, & Fujita, 2013; Iqra, Rashid, Ali, Latif, & Malik, 2020; Suzuki, Rivero, Shulaev, Blumwald, & Mittler, 2014).

The second stage or phase is usually ion- dependent in which there is an accumulation of ions like H

⁺

, Na

⁺

, Ca

⁺²

and K

⁺

takes place in the root tip cells, root hairs, leaves, and cell organelles. However, the accumulation of extra Na

⁺

in the leaves, roots, and cells may cause the cell injury which ultimately reduced the plant growth and development. The crop

ARTICLE INFO

Keywords:

AtNHX1 gene Cation H⁺

Homeostasis Salt tolerance Article History:

Received: May 10, 2019 Accepted: August 18, 2020

*⁾ Corresponding author:

E-mail: saim1692@gmail.com

ABSTRACT

Salinity is an important adverse environmental problem that caused a loss in the sense of reducing yield per plant, morphological, and physiological functions of crop plants. The plants compete with environmental stress conditions to withstand following normal growth and development. The exchange of cations or protons (H

⁺

) takes place across the cell membrane to maintain the osmotic pressure of cells under salt stress conditions. There is a huge number of cation/

H

⁺

antiporter 1 protein-producing gene by plant cells under salt stress conditions has been identified. However, a few have been characterized and sequenced which contributes to ion homeostasis and osmotic adjustment of cells. These cation/H

⁺

antiporters are produced and stored in the vacuoles, endosomal forms and in the cytoplasm. The cation/H

⁺

antiporters are involved in the homeostasis of K

⁺

, Na

⁺

, and pH of the cell under salinity stress conditions. The cation/H

⁺

antiporters help plants cells to regulate all physiological functions under salt stress conditions.

ISSN: 0126-0537Accredited First Grade by Ministry of Research, Technology and Higher Education of The Republic of Indonesia, Decree No: 30/E/KPT/2018

Cite this as: Ali, Q., Azhar, M. M., Malik, A., Ahmad, S., Saleem, M. Z., & Waseem, M. (2020). Mechanism of salt stress tolerance in plants: role of cation/H⁺ antiporters. AGRIVITA Journal of Agricultural Science, 42(3), 593–606.

https://doi. org/10.17503/agrivita.v42i3.2242

Mechanism of Salt Stress Tolerance in Plants: Role of Cation/H

⁺

Antiporters

Qurban Ali^1*), Muzammal Mateen Azhar¹⁾, Arif Malik¹⁾, Shahbaz Ahmad²⁾, Muhammad Zafar Saleem³⁾ and Muhammad Waseem⁴⁾

1)

Institute of Molecular Biology and Biotechnology, University of Lahore, Lahore, Pakistan

2)

Institute of Agricultural Sciences, University of the Punjab Lahore, Lahore, Pakistan

3)

Centre for Applied Molecular Biology (CAMB), University of the Punjab, Lahore, Pakistan

4)

Department of Agronomy, Faculty Agriculture, Lasbela University of Agriculture, Water and Marine

Science, Uthal, Lasbela, Pakistan

plants mostly show the stress tolerance mechanisms which may be signals caused by the production of hormones, cation exchange in the cells with the outer environment like the timely transport of Na

⁺

in the cells caused reduced cell injury in the root and cells, and tolerance at the tissue level in which the accumulation of Na

⁺

takes place in the leaves where the Na

⁺

compartmentalization at intracellular and cellular levels take place mostly in the vacuoles of cells for saving cells from higher accumulation of Na

⁺

in the cytoplasm and other organelles of the cell. The Na

⁺

compartmentalization in vacuoles provides an additional osmotic adjustment to the cell for keeping osmotic pressure under saline conditions (Abdel Latef & Ahmad, 2015; Amagaya, Shibuya, Nishiyama, Kato, & Kanayama, 2020;

Djanaguiraman & Vara Prasad, 2013; Haseeb, Nawaz, Rao, Ali, & Malik, 2020; Noreen, Siddiq, Hussain, Ahmad, & Hasanuzzaman, 2017). The class of cation/proton antiporter1 (CPA1) is a transmembranes antiporters which adds to cations the Na

⁺

or K

⁺

particle transmembrane operate for proton (H

⁺

) utilizing electrochemical slopes created by various translocating chemicals, for example, proton ATPase in the cell membrane or plasma layer, phosphatase and vacuolar ATPase in intracellular compartments of cells (Bölter, Mitterreiter, Schwenkert, Finkemeier, & Kunz, 2020;

Horie, Karahara, & Katsuhara, 2012; Morgan, Platt, Lloyd-Evans, & Galione, 2011; Rodríguez- Rosales et al., 2009). It has been found that the first most K

⁺

/Na

⁺

proton (H

⁺

) cation antiporter was identified as AtNHX1 in Arabidopsis thaliana which has also been cloned (Hasegawa, Bressan, Zhu, &

Bohnert, 2000). These ATPase, phosphatases, and vacuolar ATPase are available in cells, for example, microorganisms, plants, organisms, and creature cells. Every single eukaryotic genome which has been sequenced up to now has shown a large number of isoforms of these antiporters, except for yeast (Brett, Donowitz, & Rao, 2005; Ismail, Riemann, & Nick, 2012).

The cation/H

⁺

antiporter1 plant qualities were doled out to either the Na

⁺

/H

⁺

exchanger (NHX) or Na

⁺

/H

⁺

(NhaP) clade (Chanroj et al., 2012; Pardo, Cubero, Leidi, & Quintero, 2006; Wang, Wu, Liu, &

Qiu, 2015). Qualities doled out to the previous clade encode proteins that are situated in the plasma layer and are like the NHE-1 protein or human sodium hydrogen exchanger isoform-1 proteins (Chanroj et al., 2012; Mahajan & Tuteja, 2005; Qiu,

Guo, Dietrich, Schumaker, & Zhu, 2002) whoever;

the intracellular (IC) films are situated in the NHX clade. The intracellular class I Na

⁺

/H

⁺

exchanger or NHX1s are kept in the tonoplast of the cell which is plant-specific explicit (Brett, Donowitz, & Rao, 2005;

Mahajan & Tuteja, 2005); the intracellular class IIs which may be found within cell endosomes and which are firmly connected to the ScNHX1 protein of yeast (Bowers, Levi, Patel, & Stevens, 2000;

Tester & Davenport, 2003) while for human sodium protein (hydrogen) exchange proteins like NHE6 and NHE7 (Chanroj et al., 2012; Xiong, Schumaker,

& Zhu, 2002). It has been found that the rice and Arabidopsis thaliana cation/proton antiporter1 are nearly the equivalents in size: which have two NhaP isoforms in Arabidopsis thaliana (NHX8 and NHX7 or salt overly sensitive1 (SOS1)) while there is one salt overly sensitive1 (SOS1) in rice. Six qualities in A speak to the NHX clad. Thaliana and rice by five:

Intracellular-Is (IC-Is) OsNHX1-4 and atNHX1-4, while IC-IIs AtNHX6, OsNHX5, and atNHX5.

The Arabidopsis thaliana IC-Is and rice share 54-87 percent polypeptide likeness, while the closeness of the three IC-IIs which ranged from 72- 79 percent. The IC-II and IC-I successions share a ikeness of just around 22 percent (Bartels & Sunkar, 2005; Modareszadeh, Bahmani, Kim, & Hwang, 2020; Zhu, 2003). Particle and pH homeostasis are basic to the activity of numerous cell forms basic plant advancement and development. CPA1 movement is the main determining factor of cell osmotic condition and accordingly of cell weight.

Strain to direct vacuolar and endosomal pH and particle piece influences the handling and dealing of proteins just as the arrangement and development of vesicular payload (Bowers, Levi, Patel, &

Stevens, 2000; Pardo, Cubero, Leidi, & Quintero, 2006; Vinocur & Altman, 2005). The proposal is to keep its compartment qualities. This audit centers on the physiological significance of the CPA1 plant classes (Deinlein et al., 2014; Hrabak et al., 2003;

Naseem, Ali, & Malik, 2020; Rodríguez-Rosales et al., 2009; Sajid, Rashid, Ali, & Husnain, 2018).

Cation/H⁺ Antiporter1 for Salt Stress Tolerance

At the point when presented to a saline

situation, plants unavoidably collect Na

⁺

particles

(in spite of the fact that to changing degrees),

compelled by the main Na

⁺

inclination among the dirt

arrangement and plant’s interior. The competency to

limit the retaining of Na

⁺

in the roots is an essential

segment of plant saltiness resilience. Interspecific correlations of Na

⁺

transition and the rate of the Na

⁺

aggregation recommend that 70 to 95% of Na

⁺

that enters to roots symplast is effectively come back to rhizospheres by means of an enthusiastically exorbitant procedure (Jiang, Leidi, & Pardo, 2010;

Muqadas, Ali, & Malik, 2020; Park, Kim, & Yun, 2016; Tester & Davenport, 2003). To date, just the plasma layer trade Na

⁺

/H

⁺

exchanger SOS1 was thoroughly evaluated (Pardo & Rubio, 2011; Pinedo, Ledger, Greve, & Poupin, 2015; Zhang, Yao, & Zhu, 2010). The over-articulation of its encoding quality (or some homologs) expands the resilience of saltiness in both tobacco and Arabidopsis thaliana (Shi & Massagué, 2003; Veldhoen, Hocking, Atkins, Locksley, & Stockinger, 2006; Yue, Zhang, Zhang, Duan, & Li, 2012). Vesicles of plasma film framed by Arabidopsis thaliana SOS1 freak loss of capacity have some trade action of Na

⁺

/H

⁺

(Feki et al., 2014;

Ma et al., 2014; Yadav, Shukla, Jha, Agarwal, & Jha, 2012). Firmly correlated protein AtNHX8 is viewed as a plasma film found Li

⁺

/H

⁺

anti-porter which reacts explicitly to the worry of overabundance Li

⁺

particles, as T-DNA inclusion freaks the encoding of Li

⁺

quality is less sensitive to wild types as compared with Li

⁺

; Outcomes do not spread to extra monovalent cation’s Na

⁺

, Cs

⁺

or K

⁺

(An et al., 2007;

Chien, Nam, & Chen, 2015).

The suggestion is that there are likely extra plasma layer exchangers; in any case, the hereditary resistant affirms that SOS1 makes a critical commitment to saltiness resilience. Na

⁺

trades just fuel the ionic and osmotic irregularity, provoking the essential pressure. In this manner, returning Na

⁺

to the medium must be a between time arrangement and can’t give delayed resistance to soil saltiness all alone. Since the productivity of Na

⁺

evacuation isn’t 100%, Na

⁺

particles will definitely gather after some time, first in the roots and late in the whole plant. Plants utilize the IC-I compound NHX as a second line of a barrier to repossess Na

⁺

particles in their cell vacuoles, Both ensuring cytosol against Na

⁺

lethality and advancing osmotic water retention (Apse & Blumwald, 2007; Ohta et al., 2002;

Yamaguchi & Blumwald, 2005). The overexpression of either NHX AtNHX1 or encoding qualities builds the resilience of saltiness in an assortment of plant- animal types (Ashraf, Athar, Harris, & Kwon, 2008;

Fukuda et al., 2004; He et al., 2005; Martínez- Atienza et al., 2007). Synchronous over articulation of AtSOS1 and AtNHX1 fundamentally decrease

the loss of saltiness stretch instigated biomass (Li et al., 2017; Pehlivan et al., 2016). Interestingly, both tomato plant needs NHX2 (IC-II NHX) and NHX1 while Arabidopsis thaliana plant NHX2. The twofold freak Arabidopsis thaliana nhx5nhx6 is extremely sensitive to saltiness (Baghour et al., 2019; Jia et al., 2018; Jiang et al., 2017; Yousef, Shafique, Ali, &

Malik, 2020; Zhou et al., 2018). V-ATPase vacuolar deficient plants have decreased nitrate stockpiling limit and don’t over accumulate Zn

²⁺

and are not excessively delicate to saltiness.

Plants with expanded endosomal or trans- Golgi arrange (TGN) movement restricted V-ATPase, then again, are delicate to saltiness (Deinlein et al., 2014; Hedrich, 2012; Krebs et al., 2010).

The suggestion is that the endosomal/vesicles framework gives a critical method for shielding plants from the harm caused by saltiness worry, as different examinations have upheld (Abogadallah, 2010; Ma & Bohnert, 2007; Mazel, Leshem, Tiwari, & Levine, 2004). The saltiness resilience of NHX over-communicating plant gives off an impression of being autonomous of both the cause of transgene species and character of encoded iso- form: IC-II and IC-I anti-porters seem to having a comparative job in resistance of saltiness. Since NHX transporters likewise convey K

⁺

particles, they are relied upon to influence intercellular K

⁺

content, especially on account of IC-II antiporters explicit to K

⁺

. The overexpression of either AtNHX1 or AtNHX2 has appeared together K

⁺

and Na

⁺

content in ENA is expanded (principle arrangement of Na

⁺

efflux) and ScNHX1-disturbed yeast cell developed in NaCl (Mäser et al., 2001; Steiner & Sazanov, 2020;

Quintero, Blatt, & Pardo, 2000; Yokoi et al., 2002).

Constitutive articulations of LeNHX2 and AtNHX5 encoding the IC-II anti-porter increment K

⁺

’s cell content, however, decrease Na

⁺

’s content binding locales associated with K

⁺

take-up (Quintero, Ohta, Shi, Zhu, & Pardo, 2002; Rus et al., 2001). The Na

⁺

expulsion from cytoplasm accomplished via SOS1 in this way shield cells from the loss of the layer transport limit of K

⁺

. This applies particularly to the K

⁺

channel AKT1 (Arabidopsis K

⁺

transporter1) (Qiu et al., 2004; Serrano & Rodriguez-Navarro, 2001).

Cation/H⁺ Antiporter1 for Homeostasis of K⁺ in Cells

The derivation is that the CPA1-intervened

saltiness resilience of the plant isn’t only a result of

the aggregation of the Na

⁺

inside of vacuoles and

expulsion of Na

⁺

from the cell; be that as it may, at any rate, some portion of this resistance mirrors the impact of CPA1 on the cytoplasmic substance of K

⁺

. Some CPA1s, especially NHXs, was recommended to take an interest in K

⁺

homeostasis under ordinary states of development (Olías et al., 2009). Other than being a basic supplement, the K

⁺

adjusts intracellular load and is additionally a co-factor in certain cytosolic chemicals. Most of the K

⁺

cell is found in the vacuole, where it keeps up weight and hence in a roundabout way drives cell extension (Leidi et al., 2010). Cytoplasm fermentation can be utilized as a flag to actuate either high liking K

⁺

soil ingestion or K

⁺

vacuole efflux (Chauhan et al., 2000; Venema, Belver, Marín-Manzano, Rodríguez-Rosales, &

Donaire, 2003). The decrease in the pH inclination over the tonoplast film might lessen the collection of vacuolar K

⁺

compelled by IC-I NHX1. The statement of NHX1s in grapes was altogether up-regulated for the ripening of grapes and the cell extension, with the aggregation of grapes K

⁺

in vacuoles and descent in acridity (Aharon, Apse, Duan, Hua,

& Blumwald, 2003; Gao, Ren, Zhao, & Zhang, 2003). There is a decrease in anti-port movement in Arabidopsis thaliana NHX1 invalid freaks that shape littler cells and demonstrate a diminished development of exceedingly vacuolated cells;

these impacts might be identified with K

⁺

vacuum shortage required to guarantee cell extension weight potential (Dhar, Sägesser, Weikert, Yuan, & Wagner, 2011; Jiang, Leidi, & Pardo, 2010). Micro-array based transcriptomic investigation demonstrated that qualities encoding great proclivity K

⁺

take-up transporters are uncontrolled without a practical NHX1 duplicate, which underpins the possibility that AtNHX1 is associated with K

⁺

homeostasis (Janz et al., 2010; Shabala & Munns, 2012).

Although, when the firmly related NHX2 isoform is thumped out, no reasonable phenotype is actuated. Twofold nhx1nhx2 freak fundamentally decreases cell development and development, especially in the quickly extending fiber (Ohnishi et al., 2005; Pardo & Rubio, 2011). The vacuolar K

⁺

+ Double freak component is just a single third in the wild plants, both in the leaf and in the root (Baghour et al., 2019; Deinlein et al., 2014). The opening of stomata relies upon expansion in K

⁺

vacuum cell contents; a procedure is dependent on NHX vacuum (An et al., 2007; Fukuda et al., 2004).

These perceptions underscore the significance of vacuolar NHX for the K

⁺

homeostasis of cells. NHX

knockdown/knockout prompts genuine development deserts. In tomatoes, for instance, the crumple of LeNHX2 causes development delays (Chauhan et al., 2000; Jiang, Leidi, & Pardo, 2010), and likewise in

Arabidopsis thaliana, NHX5 and NHX6 misfortunes

all the while decrease cell estimate and moderate both botanical advancement and root development (Qiu et al., 2004). The K

⁺

substance of the twofold freak nhx5nhx6 is fundamentally lower than that of wild tissue (Padmanaban et al., 2007; Wang, Wu, Liu, & Qiu, 2015; Yamaguchi & Blumwald, 2005).

The constituent appearance of NHX6 and NHX5 in the two freaks safeguards the development of the root. Endosomal NHXs hence contribute generously to development and extension, possibly by means of their subsidizing of K

⁺

homeostasis.

Though, the inadequacy of coordinated K

⁺

positive microprobe obliges the degree of K

⁺

placated in vesicles, keeping away from the identity of a piece of endosomal/vesicular NHXs in K

⁺

homeostasis (Ohta et al., 2002; Rajagopal et al., 2007).

Cation/H⁺ Antiporter1 for Homeostasis of pH in Cell

For all types of cell functions, cell pH homeostasis is an extremely basic component for normal cell functioning and regulation. The pH of the cytoplasm is well-ordered essential by proton siphons and metabolic procedures delivering hydroxyl or protons particles. Luminal pH isn’t constant all throughout the cell; it is also in focus on the intracellular compartments of cells (Paroutis, Touret, & Grinstein, 2004; Shen et al., 2013). In- vivo estimation uncovered that the pH varies from 7.1 within the endoplasmic reticulum to almost 5.5 pH in the vacuoles; the trans-Golgi network is extra acidic than the pre-vacuolar compartment that is the middle of the cell transporting organelles wherever secretory and endocytic traffic prompts the vacuoles (Bassil & Blumwald, 2014; Orij, Brul, & Smits, 2011).

Certain the inclusion of CPA1s in proton spillage, it’s not really astounding that they can manage pH in the vesicle or in the cytoplasm relying upon their sub-cell confinement. Proof for intra-cellular NHX-subordinate pH direction previously emerged from an investigation of pigmentation of Ipomea sp.

petals (Martinière et al., 2013; Yoshida et al., 2005;

Zhao, Barkla, Marshall, Pittman, & Hirschi, 2008).

Along with improvement, petal starts to

gather the anthocyanins in the cell vacuoles: these

outcomes in red shading at lesser vacuolar blue

shading as pH increase. The expansion of petal vacuolar pH which ranged from 6.5-7.5 is joined by an enhanced proton-PPase, NHX1, and V-ATPase action. Coordinate vacuolar pH estimations in NHX freaks emphatically show that vacuolar NHX antiporters are vital in vacuolar pH direction. Twofold freak thaliana nhx1nhx2, the vacuolar condition is fundamentally a greater amount of acidic than in the wild type cells of stretching and development zone, particularly in the cortical or surface cells of leaves and roots (Hamaji et al., 2009; Pittman, 2012).

Root tip cells will in general have more corrosive pH than develop cells of the root zone. There is, nonetheless, little distinction between nhx1nhx2 cell pH and wild plants in root tip cells (Li, Li, Li, &

Wu, 2011; Reguera, Bassil, & Blumwald, 2014). The result is that NHX anti-porter action is increasingly articulated in cells that essential to expand their vacuum volume so as to lengthen them. To gauge luminal pH in the Golgi locale body, trans-Golgi network, and late pre-vacuolar compartment.

Luorin based pH sensors were utilized (Reguera, Bassil, & Blumwald, 2014; Senadheera, Singh,

& Maathuis, 2009; Tester & Davenport, 2003);

their outcomes are that pH in such compartment is lower than in wild sort in the nhx5nhx6 twofold freak, which suggests that vesicular/endosomal NHX1s increased the vesicle pH of cell. Wang and his colleagues exhibited that the nhx5nhx6 showed a lower vacuolar pH as estimated by the half electrical microelectrode (Wang, Wu, Liu, & Qiu, 2015). Despite the fact that the contribution of NHX plant transporters in cytoplasmic pH control still can’t seem to be illustrated, utilization of fluorescent examples demonstrated that passing of a practical duplicate of AtSOS1 consequences in adjusted pH homeostasis in both root and stem cells, most likely because of a change in proton transition over the plasma layer (Ahmadi, Corso, Weber, Verbruggen,

& Clemens, 2018; Manohar, Shigaki, & Hirschi, 2011; Mei et al., 2009).

Plant Cation/H⁺ Antiporter1 (CPA1s)

As of late found usefulness of the endosome localized proteins, AtNHX6 and AtNHX5 are principally entrancing. Much same as the yeast cells (Baghour et al., 2019; Chauhan et al., 2000;

Li, Li, Li, & Wu, 2011) and animal cells (Casey, Grinstein, & Orlowski, 2010; Krulwich, Sachs, &

Padan, 2011), quality difference nhx5nhx6 twofold freak articulation is to a great extent identified with

vesicular and vacuole transport system (Cao et al., 2016). Endocytotic tracer lipophilic styryl color (FM4-64), and checking the dynamic fluorescence naming of endo-membranes has been appeared to have been extremely deferred in nhx5nhx6 naming of the vacuole. Likewise, recently blended carboxypeptidase Y-green fluorescent protein (CPY-GFP) dealing, that regularly aggregates in the vacuole, transported towards the apoplast in the nhx5nhx6 containing plants (Adams & Shin, 2014;

Kumar, Kumar, Kim, Ryu, & Cho, 2013). A practical connection among based on broad co-area of TGN-restricted, the VATPase complex, NHX6 and NHX5 have also been studied (Joshi, Jha, Mishra,

& Jha, 2013; Reguera, Bassil, & Blumwald, 2014).

The proposition is that endosomal NHXs control vesicular dealing through their endosomal particle direction and pH homeostasis. In any case, pH isn’t the main maintainer of the endosomal catalyst action and protein security, since it additionally adds to the identity of the vesicle, direction of receptor and freight communications, and, at last, endomembrane dealing (Huertas et al., 2013;

Reddy, Kim, Yoon, Kim, & Kwon, 2017). The in-vivo estimations of the vesicular pH standing of the endo- membrane compartment and their commitment to the control of the development of proteins should set up the biochemical reason for these procedures.

In the endoplasmic reticulum, the seed storage proteins which are incorporated as forerunners and transported into protein stockpiling vacuoles are also involved to develop organelles of the cell. Many findings have demonstrated that proteins transported to the vacuole via a vesicle- interceded dealing course that incorporates pre- vacuolar compartment endoplasmic reticulum, trans-Golgi network, Golgi, and multi-cycle bodies.

Along these lines, the trans-Golgi network, Golgi

and multi-cycle bodies, pre-vacuolar compartment

are major vesicular protein arranging stations

(Almeida, Margarida Oliveira, & Saibo, 2017; Qiu et

al., 2004). In the protein dealing pathway, AtNHX6

and AtNHX5 are limited to the trans-Golgi network,

Golgi, and the pre-vacuolar compartment. IC-I anti-

porters may likewise take part in intracellular vesicle

dealing, as an NHX1 T-DNA inclusion freak changes

the translation of an extensive amount of qualities

encoding a protein-related with intra-vesicular

dealing, core dealing, and preparing in the Golgi

bodies (Gharsallah, Fakhfakh, Grubb, & Gorsane,

2016; Zheng, Pan, Fan, & Qiu, 2013). To date, the

fundamental focal point of CPA1 articulation has been on saltiness worry, for instance, the salt-initiated AtCAPE1 contrarily controlled salt resistance by smothering a few salt-resilience qualities that work in osmolyte generation, detoxification, and control of stomatic conclusion and protection of the phone layer. Intravacuolar control assumes an essential job in the cell extension and blossom advancement of AtNHX1 and AtNHX2 K

⁺

substance and pH (McCubbin, Bassil, Zhang, & Blumwald, 2014; Shin, 2014; Wang et al., 2016). In any case, a few individuals from this quality family give off an impression of being inducible by abscisic acid (Wu, Ebine, Ueda, & Qiu, 2016; Yokoi et al., 2002), KCl (Fukuda et al., 2004), drying out (Li, Li, Li, & Wu, 2011) as well as hyper-osmotic pressure (Yokoi et al., 2002). Disconnection of definite NHX qualities from Morus atropurpurea has as of late exhibited that they are inducible by saltiness, dry season, and abscisic acid, as well as by salicylic acid, methyl jasmonate, and hydrogen peroxide (Cai et al., 2016;

Ma, Augé, Dong, & Cheng, 2017; Wu et al., 2016).

Cation/ H⁺ Antiporters and Regulation of Cell Structures

It has been identified that the Na

⁺

/H

⁺

antiporters played an important role in the regulation of cellular Na

⁺

, Ca

⁺

, K

⁺

, pH, and cell homeostasis under environmental conditions. The genetic studies of NHX1 and NHX2 have shown that under double knocked out of NHX1 and NHX2 caused a reduction in the plant growth under stress environment (Bassil et al., 2011; Chanroj et al., 2012; Hanin, Ebel, Ngom, Laplaze, & Masmoudi, 2016). It also caused a reduction of cell size, short hypocotyls, the abnormal stamens produced in the flowers. The NHX1 and NHX2 caused reduced growth of pollen tubes which caused hindrance in pollination, while the pollen viability and germination were not affected even under stress conditions. The NHX1 and NHX2 play important role in the development of flower and cell expansion under stress conditions (Almeida, Margarida Oliveira, & Saibo, 2017; Assaha, Ueda, Saneoka, Al-Yahyai, & Yaish, 2017; Ismail & Horie, 2017; Yang & Guo, 2018). The salt stress caused damage in the roots and shoot of maize seedlings, the production of osmolytes in the roots and shoots of seedling lead towards the repairing of damage.

The use of yeast and carrot extracts help to maintain the concentrations of K

⁺

, Na

⁺

, and Ca

⁺²

in the cells to regulate the antioxidant enzymes and cation/

H

⁺

antiporters which also help to maintain the cell membrane, and membrane-bounded organelles of cells under stress environment (Abdel Latef, Mostofa, Rahman, Abdel-Farid, & Tran, 2019; Jiang et al., 2019; Ye, Zhao, Bao, Cao, & Zou, 2019).

The reduction in photosynthesis was reported in watermelon under salinity and alkalinity stress conductions due to the damage of chloroplast cells, the destruction in the thylakoid membranes under the formation of reactive oxygen species. The production of cation/H

⁺

antiporters helps to maintain the ion concentration in the matrix and within the membrane-bounded organelles. There is also the release of osmolytes in the cytosol to prevent damage or cell structures (Arnao & Hernández- Ruiz, 2019; Jiang et al., 2019; Tian et al., 2019; Ye, Zhao, Bao, Cao, & Zou, 2019). Hereditary studies give convincing proof that the three classes of CPA1 (cell membrane or plasma membrane, vacuolar and endosomal) control an assortment of cell and physiological procedures, containing cell extension, cation homeostasis, and osmotic procedures (Tian et al., 2019; Yang & Guo, 2018). Also, it involved the potential for weight, pH homeostasis, and dealing with vesicles, stomata capacity, and flower advancement (Bafeel, 2014; Bassil et al., 2011).

CONCLUSION

The accessibility of numerous CPA1 knockout lines and the improvement of stages equipped for estimating in vivo pH and particle contents in many intracellular compartments have made it conceivable deeper comprehension or understanding of the protein potentials and ability to function in cells. To illuminate the hidden instruments, the distinguishing proof of the protein accomplices that direct the exercises of these bearers is important. In light of the worry of saltiness, the three CPA1 classes seem to cooperate. They are additionally vital for keeping up pH and K

⁺

cell content. They coordinate in managing an assortment of procedures from bladder dealing and cell extension to plant development.

REFERENCES

Abdel Latef, A. A. H., & Ahmad, P. (2015). Legumes and breeding under abiotic stress: An overview. In M. M. Azooz & P. Ahmad (Eds.), Legumes under Environmental Stress: Yield, Improvement and Adaptations (pp. 1–20). West Sussex, UK: John Wiley & Sons, Inc. https://doi.

org/10.1002/9781118917091.ch1

Abdel Latef, A. A. H., Mostofa, M. G., Rahman, M. M., Abdel-Farid, I. B., & Tran, L. S. P. (2019).

Extracts from yeast and carrot roots enhance maize performance under seawater-induced salt stress by altering physio-biochemical characteristics of stressed plants. Journal of Plant Growth Regulation, 38, 966–979. https://

doi.org/10.1007/s00344-018-9906-8

Abogadallah, G. M. (2010). Insights into the significance of antioxidative defense under salt stress. Plant Signaling & Behavior, 5(4), 369–374. https://doi.

org/10.4161/psb.5.4.10873

Adams, E., & Shin, R. (2014). Transport, signaling, and homeostasis of potassium and sodium in plants.

Journal of Integrative Plant Biology, 56(3), 231–

249. https://doi.org/10.1111/jipb.12159

Aharon, G. S., Apse, M. P., Duan, S., Hua, X., & Blumwald, E. (2003). Characterization of a family of vacuolar Na+/H+ antiporters in Arabidopsis thaliana.

Plant and Soil, 253(1), 245–256. https://doi.

org/10.1023/A:1024577205697

Ahmadi, H., Corso, M., Weber, M., Verbruggen, N., &

Clemens, S. (2018). CAX1 suppresses Cd- induced generation of reactive oxygen species in Arabidopsis halleri. Plant Cell and Environment, 41(10), 2435–2448. https://doi.org/10.1111/

pce.13362

Ali, M., Rafique, F., Ali, Q., & Malik, A. (2020). Genetic modification for salt and drought tolerance in plants through SODERF3. Biological and Clinical Sciences Research Journal, 2020, e022.

Retrieved from https://bcsrj.com/wp-content/

uploads/2020/08/MSBCSRJ202005100e022.

pdf

Almeida, D. M., Margarida Oliveira, M., & Saibo, N. J. M.

(2017). Regulation of Na+ and K+ homeostasis in plants: Towards improved salt stress tolerance in crop plants. Genetics and Molecular Biology, 40(suppl. 1), 326–345. https://doi.

org/10.1590/1678-4685-gmb-2016-0106

Amagaya, K., Shibuya, T., Nishiyama, M., Kato, K., &

Kanayama, Y. (2020). Characterization and expression analysis of the Ca2+/cation antiporter gene family in tomatoes. Plants, 9(1), 25. https://

doi.org/10.3390/plants9010025

An, R., Chen, Q. J., Chai, M. F., Lu, P. L., Su, Z., Qin, Z. X.,

… Wang, X. C. (2007). AtNHX8, a member of the monovalent cation: Proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li+/H+

antiporter. Plant Journal, 49(4), 718–728. https://

doi.org/10.1111/j.1365-313X.2006.02990.x

Apse, M. P., & Blumwald, E. (2007). Na+ transport in plants. FEBS Letters, 581(12), 2247–2254.

https://doi.org/10.1016/j.febslet.2007.04.014 Arnao, M. B., & Hernández-Ruiz, J. (2019). Melatonin

and reactive oxygen and nitrogen species: a model for the plant redox network. Melatonin Research, 2(3), 152–168. https://doi.

org/10.32794/11250036

Ashraf, M., Athar, H. R., Harris, P. J. C., & Kwon, T.

R. (2008). Some prospective strategies for improving crop salt tolerance. Advances in Agronomy, 97, 45–110. https://doi.org/10.1016/

S0065-2113(07)00002-8

Assaha, D. V. M., Ueda, A., Saneoka, H., Al-Yahyai, R.,

& Yaish, M. W. (2017). The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Frontiers in Physiology, 8, 509.

https://doi.org/10.3389/fphys.2017.00509 Bafeel, S. O. (2014). Physiological parameters of salt

tolerance during germination and seedling growth of Sorghum bicolor cultivars of the same subtropical origin. Saudi Journal of Biological Sciences, 21(4), 300–304. https://doi.

org/10.1016/j.sjbs.2014.05.005

Baghour, M., Gálvez, F. J., Sánchez, M. E., Aranda, M. N., Venema, K., & Rodríguez-Rosales, M.

P. (2019). Overexpression of LeNHX2 and SlSOS2 increases salt tolerance and fruit production in double transgenic tomato plants.

Plant Physiology and Biochemistry, 135, 77–86.

https://doi.org/10.1016/j.plaphy.2018.11.028 Bartels, D., & Sunkar, R. (2005). Drought and salt

tolerance in plants. Critical Reviews in Plant Sciences, 24(1), 23–58. https://doi.

org/10.1080/07352680590910410

Bassil, E., & Blumwald, E. (2014). The ins and outs of intracellular ion homeostasis: NHX-type cation/

H+ transporters. Current Opinion in Plant Biology, 22, 1–6. https://doi.org/10.1016/j.

pbi.2014.08.002

Bassil, E., Tajima, H., Liang, Y.-C., Ohto, M., Ushijima, K., Nakano, R., … Blumwald, E. (2011). The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. The Plant Cell, 23(9), 3482–3497.

https://doi.org/10.1105/tpc.111.089581

Bölter, B., Mitterreiter, M. J., Schwenkert, S., Finkemeier, I., & Kunz, H.-H. (2020). The topology of plastid inner envelope potassium cation efflux antiporter KEA1 provides new insights into its regulatory

features. Photosynthesis Research, 145, 43–54.

https://doi.org/10.1007/s11120-019-00700-2 Bowers, K., Levi, B. P., Patel, F. I., & Stevens, T. H.

(2000). The sodium/proton exchanger Nhx1p is required for endosomal protein trafficking in the yeast Saccharomyces cerevisiae. Molecular Biology of the Cell, 11(12), 4277–4294. https://

doi.org/10.1091/mbc.11.12.4277

Brett, C. L., Donowitz, M., & Rao, R. (2005). Evolutionary origins of eukaryotic sodium/proton exchangers.

American Journal of Physiology-Cell Physiology, 288(2), C223–C239. https://doi.org/10.1152/

ajpcell.00360.2004

Cai, X., Zhang, C., Shu, W., Ye, Z., Li, H., & Zhang, Y.

(2016). The transcription factor SlDof22 involved in ascorbate accumulation and salinity stress in tomato. Biochemical and Biophysical Research Communications, 474(4), 736–741. https://doi.

org/10.1016/j.bbrc.2016.04.148

Cao, B., Long, D., Zhang, M., Liu, C., Xiang, Z., &

Zhao, A. (2016). Molecular characterization and expression analysis of the mulberry Na+/

H+ exchanger gene family. Plant Physiology and Biochemistry, 99, 49–58. https://doi.

org/10.1016/j.plaphy.2015.12.010

Casey, J. R., Grinstein, S., & Orlowski, J. (2010). Sensors and regulators of intracellular pH. Nature Reviews Molecular Cell Biology, 11, 50–61.

https://doi.org/10.1038/nrm2820

Chanroj, S., Wang, G., Venema, K., Zhang, M. W., Delwiche, C. F., & Sze, H. (2012). Conserved and diversified gene families of monovalent cation/H+ antiporters from algae to flowering plants. Frontiers in Plant Science, 3, 25. https://

doi.org/10.3389/fpls.2012.00025

Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D. E., & Bohnert, H. J. (2000). Na+/

myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum. Plant Journal, 24(4), 511–522. https://doi.org/10.1046/

j.1365-313X.2000.00903.x

Chien, P. S., Nam, H. G., & Chen, Y. R. (2015). A salt- regulated peptide derived from the CAP superfamily protein negatively regulates salt- stress tolerance in Arabidopsis. Journal of Experimental Botany, 66(17), 5301–5313.

https://doi.org/10.1093/jxb/erv263

Deinlein, U., Stephan, A. B., Horie, T., Luo, W., Xu, G.,

& Schroeder, J. I. (2014). Plant salt-tolerance mechanisms. Trends in Plant Science,

19(6), 371–379. https://doi.org/10.1016/j.

tplants.2014.02.001

Dhar, R., Sägesser, R., Weikert, C., Yuan, J., & Wagner, A. (2011). Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. Journal of Evolutionary Biology, 24(5), 1135–1153. https://doi.org/10.1111/j.1420- 9101.2011.02249.x

Djanaguiraman, M., & Vara Prasad, P. V. (2013). Effects of salinity on ion transport, water relations and oxidative damage. In P. Ahmad, M. Azooz, & M.

Prasad (Eds.), Ecophysiology and Responses of Plants under Salt Stress (pp. 89–114). New York: Springer. https://doi.org/10.1007/978-1- 4614-4747-4_3

Feki, K., Quintero, F. J., Khoudi, H., Leidi, E. O., Masmoudi, K., Pardo, J. M., & Brini, F. (2014). A constitutively active form of a durum wheat Na+/

H+ antiporter SOS1 confers high salt tolerance to transgenic Arabidopsis. Plant Cell Reports, 33(2), 277–288. https://doi.org/10.1007/s00299- 013-1528-9

Fukuda, A., Nakamura, A., Tagiri, A., Tanaka, H., Miyao, A., Hirochika, H., & Tanaka, Y. (2004). Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant and Cell Physiology, 45(2), 146–

159. https://doi.org/10.1093/pcp/pch014

Gao, X., Ren, Z., Zhao, Y., & Zhang, H. (2003).

Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiology, 133(4), 1873–

1881. https://doi.org/10.1104/pp.103.026062 Gharsallah, C., Fakhfakh, H., Grubb, D., & Gorsane, F.

(2016). Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB PLANTS, 8, plw055. https://doi.org/10.1093/

aobpla/plw055

Hamaji, K., Nagira, M., Yoshida, K., Ohnishi, M., Oda, Y., Uemura, T., … Mimura, T. (2009). Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis. Plant and Cell Physiology, 50(12), 2023–2033. https://doi.

org/10.1093/pcp/pcp143

Hanin, M., Ebel, C., Ngom, M., Laplaze, L., & Masmoudi, K. (2016). New insights on plant salt tolerance mechanisms and their potential use for breeding.

Frontiers in Plant Science, 7, 1787. https://doi.

org/10.3389/fpls.2016.01787

Hasanuzzaman, M., Nahar, K., Alam, M. M., Roychowdhury, R., & Fujita, M. (2013).

Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants.

International Journal of Molecular Sciences, 14(5), 9643–9684. https://doi.org/10.3390/

ijms14059643

Haseeb, A., Nawaz, A., Rao, M. Q. A., Ali, Q., & Malik, A.

(2020). Genetic variability and association among seedling traits of Zea mays under drought stress conditions. Biological and Clinical Sciences Research Journal, 2020, e020. Retrieved from https://bcsrj.com/wp-content/uploads/2020/08/

MSBCSRJ202005100e020.pdf

Hasegawa, P. M., Bressan, R. A., Zhu, J. K., & Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 463–499. https://doi.org/10.1146/annurev.

arplant.51.1.463

He, C., Yan, J., Shen, G., Fu, L., Holaday, A. S., Auld, D., … Zhang, H. (2005). Expression of an arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field.

Plant and Cell Physiology, 46(11), 1848–1854.

https://doi.org/10.1093/pcp/pci201

Hedrich, R. (2012). Ion channels in plants. Physiological Reviews, 92(4), 1777–1811. https://doi.

org/10.1152/physrev.00038.2011

Horie, T., Karahara, I., & Katsuhara, M. (2012). Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plants.

Rice, 5, 11. https://doi.org/10.1186/1939-8433- 5-11

Hrabak, E. M., Chan, C. W. M., Gribskov, M., Harper, J. F., Choi, J. H., Halford, N., … Harmon, A. C. (2003).

The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology, 132(2), 666–

680. https://doi.org/10.1104/pp.102.011999 Huertas, R., Rubio, L., Cagnac, O., García-Sánchez, M.

J., Alché, J. D. D., Venema, K., … Rodríguez- Rosales, M. P. (2013). The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato. Plant, Cell

& Environment, 36(12), 2135–2149. https://doi.

org/10.1111/pce.12109

Iqra, L., Rashid, M. S., Ali, Q., Latif, I., & Malik, A. (2020).

Evaluation of genetic variability for salt tolerance in wheat. Biological and Clinical Sciences Research Journal, 2020, e016. Retrieved from https://bcsrj.com/wp-content/uploads/2020/07/

MSBCSRJ202005070e016.pdf

Ismail, A. M., & Horie, T. (2017). Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annual Review of Plant Biology, 68, 405–434. https://doi.org/10.1146/

annurev-arplant-042916-040936

Ismail, A., Riemann, M., & Nick, P. (2012). The jasmonate pathway mediates salt tolerance in grapevines.

Journal of Experimental Botany, 63(5), 2127–

2139. https://doi.org/10.1093/jxb/err426

Janz, D., Behnke, K., Schnitzler, J. P., Kanawati, B., Schmitt-Kopplin, P., & Polle, A. (2010). Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biology, 10, 150.

https://doi.org/10.1186/1471-2229-10-150 Jia, Q., Zheng, C., Sun, S., Amjad, H., Liang, K., & Lin, W.

(2018). The role of plant cation/proton antiporter gene family in salt tolerance. Biologia Plantarum, 62(4), 617–629. https://doi.org/10.1007/s10535- 018-0801-8

Jiang, J.-L., Tian, Y., Li, L., Yu, M., Hou, R.-P., & Ren, X.-M. (2019). H(2)S alleviates salinity stress in cucumber by maintaining the Na(+)/K(+) balance and regulating H(2)S metabolism and oxidative stress response. Frontiers in Plant Science, 10, 678. https://doi.org/10.3389/fpls.2019.00678 Jiang, W., Sun, L., Yang, X., Wang, M., Esmaeili, N.,

Pehlivan, N., … Zhao, Y. (2017). The effects of transcription directions of transgenes and the gypsy insulators on the transcript levels of transgenes in transgenic Arabidopsis. Scientific Reports, 7, 14757. https://doi.org/10.1038/

s41598-017-15284-x

Jiang, X., Leidi, E. O., & Pardo, J. M. (2010). How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signaling and Behavior, 5(7), 792–795. https://doi.org/10.4161/psb.5.7.11767 Joshi, M., Jha, A., Mishra, A., & Jha, B. (2013). Developing

transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS ONE, 8(8), e71136.

https://doi.org/10.1371/journal.pone.0071136 Krebs, M., Beyhl, D., Görlich, E., Al-Rasheid, K. A. S.,

Marten, I., Stierhof, Y. D., … Schumacher, K.

(2010). Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences of the United States of America, 107(7), 3251–3256. https://

doi.org/10.1073/pnas.0913035107

Krulwich, T. A., Sachs, G., & Padan, E. (2011). Molecular aspects of bacterial pH sensing and homeostasis.

Nature Reviews Microbiology, 9(5), 330–343.

https://doi.org/10.1038/nrmicro2549

Kumar, K., Kumar, M., Kim, S. R., Ryu, H., & Cho, Y. G. (2013). Insights into genomics of salt stress response in rice. Rice, 6, 27. https://doi.

org/10.1186/1939-8433-6-27

Leidi, E. O., Barragán, V., Rubio, L., El-Hamdaoui, A., Ruiz, M. T., Cubero, B., … Pardo, J. M. (2010).

The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant Journal, 61(3), 495–506. https://

doi.org/10.1111/j.1365-313X.2009.04073.x Li, M., Li, Y., Li, H., & Wu, G. (2011). Overexpression of

AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree Physiology, 31(3), 349–357. https://

doi.org/10.1093/treephys/tpr003

Li, N., Wang, X., Ma, B., Du, C., Zheng, L., & Wang, Y. (2017). Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. Journal of Plant Physiology, 218, 109–120. https://doi.org/10.1016/j.

jplph.2017.07.015

Ma, D. M., Xu, W. R., Li, H. W., Jin, F. X., Guo, L. N., Wang, J., … Xu, X. (2014). Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma, 251(1), 219–231. https://

doi.org/10.1007/s00709-013-0540-9

Ma, S., & Bohnert, H. J. (2007). Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biology, 8, R49. https://doi.

org/10.1186/gb-2007-8-4-r49

Ma, Y.-C., Augé, R. M., Dong, C., & Cheng, Z.-M.

(Max). (2017). Increased salt tolerance with overexpression of cation/proton antiporter 1 genes: A meta-analysis. Plant Biotechnology Journal, 15(2), 162–173. https://doi.org/10.1111/

pbi.12599

Mahajan, S., & Tuteja, N. (2005). Cold, salinity and drought stresses: An overview. Archives of Biochemistry and Biophysics, 444(2), 139–158.

https://doi.org/10.1016/j.abb.2005.10.018 Manohar, M., Shigaki, T., & Hirschi, K. D. (2011). Plant

cation/H+ exchangers (CAXs): Biological functions and genetic manipulations. Plant

Biology, 13(4), 561–569. https://doi.org/10.1111/

j.1438-8677.2011.00466.x

Martínez-Atienza, J., Jiang, X., Garciadeblas, B., Mendoza, I., Zhu, J. K., Pardo, J. M., & Quintero, F. J. (2007). Conservation of the salt overly sensitive pathway in rice. Plant Physiology, 143(2), 1001–1012. https://doi.org/10.1104/

pp.106.092635

Martinière, A., Bassil, E., Jublanc, E., Alcon, C., Reguera, M., Sentenac, H., … Paris, N. (2013). In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell, 25(10), 4028–4043. https://doi.org/10.1105/

tpc.113.116897

Mäser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., … Guerinot, M. L. (2001).

Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology, 126(4), 1646–1667. https://doi.

org/10.1104/pp.126.4.1646

Mazel, A., Leshem, Y., Tiwari, B. S., & Levine, A. (2004).

Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiology, 134(1), 118–128. https://doi.

org/10.1104/pp.103.025379

McCubbin, T., Bassil, E., Zhang, S., & Blumwald, E.

(2014). Vacuolar Na⁺/H⁺ NHX-type antiporters are required for cellular K⁺ homeostasis, microtubule organization and directional root growth. Plants (Basel, Switzerland), 3(3), 409–426. https://doi.

org/10.3390/plants3030409

Mei, H., Cheng, N. H., Zhao, J., Park, S., Escareno, R.

A., Pittman, J. K., & Hirschi, K. D. (2009). Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4.

New Phytologist, 183(1), 95–105. https://doi.

org/10.1111/j.1469-8137.2009.02831.x

Mickelbart, M. V., Hasegawa, P. M., & Bailey-Serres, J.

(2015). Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability.

Nature Reviews Genetics, 16, 237–251. https://

doi.org/10.1038/nrg3901

Miller, G., Suzuki, N., Ciftci-Yilmaz, S., & Mittler, R.

(2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell and Environment, 33(4), 453–467. https://doi.org/10.1111/j.1365- 3040.2009.02041.x

Modareszadeh, M., Bahmani, R., Kim, D., & Hwang, S., (2020). CAX3 (cation/proton exchanger) mediates a Cd tolerance by decreasing ROS through Ca elevation in Arabidopsis. Plant Molecular Biology, 2020, 1-18. https://doi.

org/10.1007/s11103-020-01072-1

Morgan, A. J., Platt, F. M., Lloyd-Evans, E., & Galione, A.

(2011). Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease.

Biochemical Journal, 439(3), 349–374. https://

doi.org/10.1042/BJ20110949

Munns, R., & Gilliham, M. (2015). Salinity tolerance of crops - what is the cost? New Phytologist, 208(3), 668–673. https://doi.org/10.1111/nph.13519 Munns, R., & Tester, M. (2008). Mechanisms of salinity

tolerance. Annual Review of Plant Biology, 59, 651–681. https://doi.org/10.1146/annurev.

arplant.59.032607.092911

Muqadas, S., Ali, Q., & Malik, A. (2020). Genetic association among seedling traits of Zea mays under multiple stresses of salts, heavy metals and drought. Biological and Clinical Sciences Research Journal, 2020, e026. Retrieved from https://bcsrj.com/wp-content/uploads/2020/09/

MSBCSRJ202003070e026.pdf

Naseem, S., Ali, Q., & Malik, A. (2020). Evaluation of maize seedling traits under salt stress. Biological and Clinical Sciences Research Journal, 2020, e025.

Retrieved from https://bcsrj.com/wp-content/

uploads/2020/09/MSBCSRJ202003050e025.

pdf

Noreen, S., Siddiq, A., Hussain, K., Ahmad, S., &

Hasanuzzaman, M. (2017). Foliar application of salicylic acid with salinity stress on physiological and biochemical attributes of sunflower (Helianthus annuus L.) crop. Acta Scientiarum Polonorum, Hortorum Cultus, 16(2), 57–74.

Retrieved from http://agro.icm.edu.pl/agro/

element/bwmeta1.element.agro-58df429a- 09e4-48da-8127-a685ba0039ed

Ohnishi, M., Fukada-Tanaka, S., Hoshino, A., Takada, J., Inagaki, Y., & Iida, S. (2005). Characterization of a novel Na+/H+ antiporter gene InNHX2 and comparison of InNHX2 with InNHX1, which is responsible for blue flower coloration by increasing the vacuolar pH in the Japanese morning glory. Plant and Cell Physiology, 46(2), 259–267. https://doi.org/10.1093/pcp/pci028 Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A.,

Tanaka, A., Nakamura, T., & Hayakawa, T.

(2002). Introduction of a Na+/H+ antiporter gene

from Atriplex gmelini confers salt tolerance to rice. FEBS Letters, 532(3), 279–282. https://doi.

org/10.1016/S0014-5793(02)03679-7

Olías, R., Eljakaoui, Z., Li, J., De Morales, P. A., Marín- Manzano, M. C., Pardo, J. M., & Belver, A. (2009). The plasma membrane Na+/H+

antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+

between plant organs. Plant, Cell & Environment, 32(7), 904–916. https://doi.org/10.1111/j.1365- 3040.2009.01971.x

Orij, R., Brul, S., & Smits, G. J. (2011). Intracellular pH is a tightly controlled signal in yeast. Biochimica et Biophysica Acta - General Subjects, 1810(10), 933–944. https://doi.org/10.1016/j.

bbagen.2011.03.011

Padmanaban, S., Chanroj, S., Kwak, J. M., Li, X., Ward, J. M., & Sze, H. (2007). Participation of endomembrane cation/H+ exchanger AtCHX20 in osmoregulation of guard cells.

Plant Physiology, 144(1), 82–93. https://doi.

org/10.1104/pp.106.092155

Pardo, J. M., & Rubio, F. (2011). Na+ and K+ transporters in plant signaling. In M. Geisler & K. Venema (Eds.), Transporters and Pumps in Plant Signaling (pp.

65–98). Berlin, Heidelberg: Springer. https://doi.

org/10.1007/978-3-642-14369-4_3

Pardo, J. M., Cubero, B., Leidi, E. O., & Quintero, F. J.

(2006). Alkali cation exchangers: Roles in cellular homeostasis and stress tolerance. Journal of Experimental Botany, 57(5), 1181–1199. https://

doi.org/10.1093/jxb/erj114

Park, H. J., Kim, W. Y., & Yun, D. J. (2016). A new insight of salt stress signaling in plant. Molecules and Cells, 39(6), 447–459. https://doi.org/10.14348/

molcells.2016.0083

Paroutis, P., Touret, N., & Grinstein, S. (2004). The pH of the secretory pathway: Measurement, determinants, and regulation. Physiology, 19(4), 207–215.

https://doi.org/10.1152/physiol.00005.2004 Pehlivan, N., Sun, L., Jarrett, P., Yang, X., Mishra, N., Chen,

L., … Zhang, H. (2016). Co-overexpressing a plasma membrane and a vacuolar membrane sodium/proton antiporter significantly improves salt tolerance in transgenic Arabidopsis plants.

Plant & Cell Physiology, 57(5), 1069–1084.

https://doi.org/10.1093/pcp/pcw055

Pinedo, I., Ledger, T., Greve, M., & Poupin, M. J. (2015).

Burkholderia phytofirmans PsJN induces long- term metabolic and transcriptional changes involved in Arabidopsis thaliana salt tolerance.

Frontiers in Plant Science, 6, 466. https://doi.

org/10.3389/fpls.2015.00466

Pitman, M. G., & Läuchli, A. (2006). Global impact of salinity and agricultural ecosystems. In A. Läuchli

& U. Lüttge (Eds.), Salinity: Environment - Plants - Molecules (pp. 3–20). Dordrecht: Springer.

https://doi.org/10.1007/0-306-48155-3_1 Pittman, J. K. (2012). Multiple transport pathways for

mediating intracellular pH homeostasis: The contribution of H(+)/ion exchangers. Frontiers in Plant Science, 3, 11. https://doi.org/10.3389/

fpls.2012.00011

Qiu, Q.-S., Guo, Y., Dietrich, M. A., Schumaker, K. S., &

Zhu, J.-K. (2002). Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences of the United States of America, 99(12), 8436–8441. https://

doi.org/10.1073/pnas.122224699

Qiu, Q.-S., Guo, Y., Quintero, F. J., Pardo, J. M., Schumaker, K. S., & Zhu, J.-K. (2004). Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. Journal of Biological Chemistry, 279(1), 207–215. https://

doi.org/10.1074/jbc.M307982200

Quintero, F. J., Blatt, M. R., & Pardo, J. M. (2000).

Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Letters, 471(2–3), 224–228. https://doi.org/10.1016/

S0014-5793(00)01412-5

Quintero, F. J., Ohta, M., Shi, H., Zhu, J. K., & Pardo, J. M. (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+

homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 99(13), 9061–9066. https://doi.

org/10.1073/pnas.132092099

Rajagopal, D., Agarwal, P., Tyagi, W., Singla-Pareek, S. L., Reddy, M. K., & Sopory, S. K. (2007). Pennisetum glaucum Na+/H+ antiporter confers high level of salinity tolerance in transgenic Brassica juncea.

Molecular Breeding, 19(2), 137–151. https://doi.

org/10.1007/s11032-006-9052-z

Reddy, I. N. B. L., Kim, B. K., Yoon, I. S., Kim, K. H., &

Kwon, T. R. (2017). Salt tolerance in rice: Focus on mechanisms and approaches. Rice Science, 24(3), 123–144. https://doi.org/10.1016/j.

rsci.2016.09.004

Reguera, M., Bassil, E., & Blumwald, E. (2014).

Intracellular NHX-type cation/H+ antiporters in plants. Molecular Plant, 7(2), 261–263. https://

doi.org/10.1093/mp/sst091

Rodríguez-Rosales, M. P., Gálvez, F. J., Huertas, R., Aranda, M. N., Baghour, M., Cagnac, O., &

Venema, K. (2009). Plant NHX cation/proton antiporters. Plant Signaling & Behavior, 4(4), 265–276. https://doi.org/10.4161/psb.4.4.7919 Roy, S. J., Negrão, S., & Tester, M. (2014). Salt resistant

crop plants. Current Opinion in Biotechnology, 26, 115–124. https://doi.org/10.1016/j.

copbio.2013.12.004

Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B. H., Matsumoto, T. K., … Hasegawa, P. M. (2001).

AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences of the United States of America, 98(24), 14150–14155.

https://doi.org/10.1073/pnas.241501798

Sajid, M., Rashid, B., Ali, Q., & Husnain, T. (2018).

Mechanisms of heat sensing and responses in plants. It is not all about Ca2+ ions. Biologia Plantarum, 62, 409–420. https://doi.org/10.1007/

s10535-018-0795-2

Senadheera, P., Singh, R. K., & Maathuis, F. J. M. (2009).

Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. Journal of Experimental Botany, 60(9), 2553–2563. https://doi.org/10.1093/jxb/

erp099

Serrano, R., & Rodriguez-Navarro, A. (2001). Ion homeostasis during salt stress in plants. Current Opinion in Cell Biology, 13(4), 399–404. https://

doi.org/10.1016/S0955-0674(00)00227-1 Shabala, S., & Munns, R. (2012). Salinity stress:

Physiological constraints and adaptive mechanisms. In Plant Stress Physiology (pp. 59–93). CAB International. https://doi.

org/10.1079/9781845939953.0059

Shen, J., Zeng, Y., Zhuang, X., Sun, L., Yao, X., Pimpl, P., & Jiang, L. (2013). Organelle pH in the Arabidopsis endomembrane system. Molecular Plant, 6(5), 1419–1437. https://doi.org/10.1093/

mp/sst079

Shi, Y., & Massagué, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus.

Cell, 113(6), 685–700. https://doi.org/10.1016/

S0092-8674(03)00432-X

Shin, R. (2014). Strategies for improving potassium use efficiency in plants. Molecules and Cells, 37(8), 575–584. https://doi.org/10.14348/

molcells.2014.0141

Steiner, J., & Sazanov, L., (2020). Structure and mechanism of the Mrp complex, an ancient

cation/proton antiporter. Elife, 9, e59407. https://

doi.org/10.7554/eLife.59407

Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E.,

& Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytologist, 203(1), 32–43.

https://doi.org/10.1111/nph.12797

Tester, M., & Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants. Annals of Botany, 91(5), 503–527. https://doi.org/10.1093/aob/

mcg058

Tian, S., Guo, R., Zou, X., Zhang, X., Yu, X., Zhan, Y., … Si, T. (2019). Priming with the green leaf volatile (Z)-3-hexeny-1-yl acetate enhances salinity stress tolerance in peanut (Arachis hypogaea L.) seedlings. Frontiers in Plant Science, 10, 785.

https://doi.org/10.3389/fpls.2019.00785

Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R.

M., & Stockinger, B. (2006). TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity, 24(2), 179–189. https://doi.

org/10.1016/j.immuni.2006.01.001

Venema, K., Belver, A., Marín-Manzano, M. C., Rodríguez- Rosales, M. P., & Donaire, J. P. (2003). A novel intracellular K+/H+ antiporter related to Na+/H+

antiporters is important for K+ ion homeostasis in plants. Journal of Biological Chemistry, 278(25), 22453–22459. https://doi.org/10.1074/

jbc.M210794200

Vinocur, B., & Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress:

Achievements and limitations. Current Opinion in Biotechnology, 16(2), 123–132. https://doi.

org/10.1016/j.copbio.2005.02.001

Wang, B., Zhai, H., He, S., Zhang, H., Ren, Z., Zhang, D., & Liu, Q. (2016). A vacuolar Na+/H+

antiporter gene, IbNHX2, enhances salt and drought tolerance in transgenic sweetpotato.

Scientia Horticulturae, 201, 153–166. https://doi.

org/10.1016/j.scienta.2016.01.027

Wang, L., Wu, X., Liu, Y., & Qiu, Q. S. (2015). AtNHX5 and AtNHX6 control cellular K+ and pH homeostasis in Arabidopsis: Three conserved acidic residues are essential for K+ transport. PLoS ONE, 10(12), e0144716. https://doi.org/10.1371/

journal.pone.0144716

Wu, X. X., Li, J., Wu, X. D., Liu, Q., Wang, Z. K., Liu, S. S., … Su, A. Y. (2016). Ectopic expression of Arabidopsis thaliana Na+(K+)/H+ antiporter gene, AtNHX5, enhances soybean salt tolerance.

Genetics and Molecular Research, 15(2), 1–12.

https://doi.org/10.4238/gmr.15027483

Wu, X., Ebine, K., Ueda, T., & Qiu, Q. S. (2016). AtNHX5 and AtNHX6 are required for the subcellular localization of the SNARE complex that mediates the trafficking of seed storage proteins in Arabidopsis. PLoS ONE, 11(3), e0151658.

https://doi.org/10.1371/journal.pone.0151658 Xiong, L., Schumaker, K. S., & Zhu, J. K. (2002). Cell

signaling during cold, drought, and salt stress.

Plant Cell, 14(suppl. 1), S165–S183. https://doi.

org/10.1105/tpc.000596

Yadav, N. S., Shukla, P. S., Jha, A., Agarwal, P. K., & Jha, B. (2012). The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+

loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biology, 12, 188.

https://doi.org/10.1186/1471-2229-12-188 Yamaguchi, T., & Blumwald, E. (2005). Developing

salt-tolerant crop plants: Challenges and opportunities. Trends in Plant Science, 10(12), 615–620. https://doi.org/10.1016/j.

tplants.2005.10.002

Yang, Y., & Guo, Y. (2018). Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist, 217(2), 523–539.

https://doi.org/10.1111/nph.14920

Ye, L., Zhao, X., Bao, E., Cao, K., & Zou, Z. (2019). Effects of arbuscular mycorrhizal fungi on watermelon growth, elemental uptake, antioxidant, and photosystem ii activities and stress-response gene expressions under salinity-alkalinity stresses. Frontiers in Plant Science, 10, 863.

https://doi.org/10.3389/fpls.2019.00863

Yokoi, S., Quintero, F. J., Cubero, B., Ruiz, M. T., Bressan, R. A., Hasegawa, P. M., & Pardo, J.

M. (2002). Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. The Plant Journal, 30(5), 529–539. https://doi.org/10.1046/j.1365- 313X.2002.01309.x

Yoshida, K., Kawachi, M., Mori, M., Maeshima, M., Kondo, M., Nishimura, M., & Kondo, T. (2005).

The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal color during flower opening of morning glory, Ipomoea tricolor cv. heavenly blue. Plant and Cell Physiology, 46(3), 407–415. https://doi.

org/10.1093/pcp/pci057

Yousef, F., Shafique, F., Ali, Q., & Malik, A. (2020). Effects of salt stress on the growth traits of chickpea (Cicer arietinum L.) and pea (Pisum sativum L.) seedlings. Biological and Clinical Sciences Research Journal, 2020, e029. Retrieved from