Designing salt stress-resilient crops: Current progress and future challenges

Abstract

Excess soil salinity affects large regions of land and is a major hindrance to crop production worldwide. Therefore, understanding the molecular mechanisms of plant salt tolerance has scientific importance and practical significance. In recent decades, studies have characterized hundreds of genes associated with plant responses to salt stress in different plant species. These studies have substantially advanced our molecular and genetic understanding of salt tolerance in plants and have introduced an era of molecular design breeding of salt-tolerant crops. This review summarizes our current knowledge of plant salt tolerance, emphasizing advances in elucidating the molecular mechanisms of osmotic stress tolerance, salt-ion transport and compartmentalization, oxidative stress tolerance, alkaline stress tolerance, and the trade-off between growth and salt tolerance. We also examine recent advances in understanding natural variation in the salt tolerance of crops and discuss possible strategies and challenges for designing salt stress-resilient crops. We focus on the model plant Arabidopsis (Arabidopsis thaliana) and the four most-studied crops: rice (Oryza sativa), wheat (Triticum aestivum), maize (Zea mays), and soybean (Glycine max).

Keywords

molecular design breeding / salt stress-resilient crop / salt tolerance

References

[1] Ali,A., Petrov, V., Yun,D.J., and Gechev,T. (2023). Revisiting plant salt tolerance: Novel components of the SOS pathway. Trends Plant Sci. 28: 1060-1069.

[2] Allwood,J.W., Ellis,D.I., and Goodacre,R. (2007). Metabolomic technologies and their application to the study of plants and plant-host interactions. Physiol. Plant. 132: 117-135.

[3] Apse,M.P., Sottosanto, J.B., and Blumwald,E. (2003). Vacuolar cation/H⁺ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na⁺/H⁺ antiporter. Plant J. 36: 229-239.

[4] Arabidopsis Genome Initiative. (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.

[5] Babu,N.N., Krishnan, S.G., Vinod,K.K., Krishnamurthy,S.L., Singh, V.K., Singh,M.P., Singh,R., Ellur,R.K., Rai,V., Bollinedi, H., et al. (2017). Marker aided incorporation of Saltol, a major QTL associated with seedling stage salt tolerance, into Oryza sativa “Pusa Basmati 1121”. Front. Plant Sci. 8: 41.

[6] Baek,D., Jiang,J., Chung,J.S., Wang, B., Chen,J., Xin,Z., and Shi, H. (2011). Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiol. 52: 149-161.

[7] Baetz,U., Eisenach, C., Tohge,T., Martinoia,E., and De Angeli, A. (2016). Vacuolar chloride fluxes impact ion content and distribution during early salinity stress. Plant Physiol. 172: 1167-1181.

[8] Bailey-Serres,J., Parker, J.E., Ainsworth,E.A., Oldroyd,G.E.D., and Schroeder, J.I. (2019). Genetic strategies for improving crop yields. Nature 575: 109-118.

[9] Barajas-Lopez,J.D., Moreno, J.R., Gamez-Arjona,F.M., Pardo,J.M., Punkkinen, M., Zhu,J.K., Quintero,F.J., and Fujii, H. (2018). Upstream kinases of plant SnRKs are involved in salt stress tolerance. Plant J. 93: 107-118.

[10] Barberon,M. (2017). The endodermis as a checkpoint for nutrients. New Phytol. 213: 1604-1610.

[11] Barragán,V., Leidi, E.O., Andrés,Z., Rubio,L., De Luca, A., Fernández,J.A., Cubero,B., and Pardo, J.M. (2012). Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24: 1127-1142.

[12] Bassil,E., Tajima, H., Liang,Y.C., Ohto,M.A., Ushijima, K., Nakano,R., Esumi,T., Coku,A., Belmonte,M., and Blumwald, E. (2011). The Arabidopsis Na⁺/H⁺ antiporters NHX1 and NHX2 control vacuolar pH and K⁺ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23: 3482-3497.

[13] Batelli,G., Verslues, P.E., Agius,F., Qiu,Q., Fujii,H., Pan,S., Schumaker, K.S., Grillo,S., and Zhu,J.K. (2007). SOS2 promotes salt tolerance in part by interacting with the vacuolar H⁺-ATPase and upregulating its transport activity. Mol. Cell. Biol. 27: 7781-7790.

[14] Bednarek,P., Schneider, B., SvatošA., Oldham,N.J., and Hahlbrock, K. (2005). Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiol. 138: 1058-1070.

[15] Bian,X.H., Li,W., Niu,C.F., Wei, W., Hu,Y., Han,J.Q., Lu,X., Tao,J.J., Jin, M., Qin,H., et al. (2019). A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis. New Phytol. 225: 268-283.

[16] Borjigin,C., Schilling, R.K., Bose,J., Hrmova,M., Qiu,J., Wege,S., Situmorang, A., Byrt,C., Brien,C., Berger, B., et al. (2020). A single nucleotide substitution in TaHKT1;5-D controls shoot Na⁺ accumulation in bread wheat. Plant Cell Environ. 43: 2158-2171.

[17] Brini,F., and Masmoudi, K. (2012). Ion transporters and abiotic stress tolerance in plants. ISRN Mol. Biol. 3: 1-13.

[18] Byrt,C.S., Munns,R., Burton,R.A., Gilliham, M., and Wege,S. (2018). Root cell wall solutions for crop plants in saline soils. Plant Sci. 269: 47-55.

[19] Byrt,C.S., Xu,B., Krishnan,M., Lightfoot, D.J., Athman,A., Jacobs,A.K., Watson-Haigh, N.S., Plett,D., Munns,R., Tester, M., et al. (2014). The Na⁺ transporter, TaHKT1;5-D, limits shoot Na⁺ accumulation in bread wheat. Plant J. 80: 516-526.

[20] Cao,Y., Liang,X., Yin,P., Zhang, M., and Jiang,C. (2019). A domestication-associated reduction in K⁺-preferring HKT transporter activity underlies maize shoot K⁺ accumulation and salt tolerance. New Phytol. 222: 301-317.

[21] Cao,Y., Zhang,M., Liang,X., Li, F., Shi,Y., Yang,X., and Jiang, C. (2020). Natural variation of an EF-hand Ca²⁺-binding-protein coding gene confers saline-alkaline tolerance in maize. Nat. Commun. 11: 186.

[22] Castiglioni,P., Bell,E., Lund,A., Rosenberg, A.F., Galligan,M., Hinchey,B.S., Bauer,S., Nelson,D.E., and Bensen, R.J. (2018). Identification of GB1, a gene whose constitutive overexpression increases glycinebetaine content in maize and soybean. Plant Direct 2: e00040.

[23] Cha,J.Y., Kim,J., Jeong,S.Y., Shin, G.I., Ji,M.G., Hwang,J.W., Khaleda, L., Liao,X., Ahn,G., Park,H.J., et al. (2022). The Na⁺/H⁺ antiporter SALT OVERLY SENSITIVE 1 regulates salt compensation of circadian rhythms by stabilizing GIGANTEA in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 119: e2207275119.

[24] Chai,H.X., Guo,J.F., Zhong,Y.L., Hsu, C.C., Zou,C.S., Wang,P.C., Zhu,J.K., and Shi,H.H. (2020). The plasma-membrane polyamine transporter PUT3 is regulated by the Na⁺/H⁺ antiporter SOS1 and protein kinase SOS2. New Phytol. 226: 785-797.

[25] Chen,C., He,G., Li,J., Perez-Hormaeche, J., Becker,T., Luo,M., Wallrad, L., Gao,J., Li,J., Pardo,J.M., et al. (2023). A salt stress-activated GSO1-SOS2-SOS1 module protects the Arabidopsis root stem cell niche by enhancing sodium ion extrusion. EMBO J. 42: e113004.

[26] Chen,K., Gao,J., Sun,S., Zhang, Z., Yu,B., Li,J., Xie,C., Li,G., Wang, P., Song,C.P., et al. (2020a). BONZAI proteins control global osmotic stress responses in plants. Curr. Biol. 30: 4815-4825.

[27] Chen,K., Li,G.J., Bressan,R.A., Song,C.P., Zhu,J.K., and Zhao,Y. (2020b). Abscisic acid dynamics, signaling, and functions in plants. J. Integr. Plant Biol. 62: 25-54.

[28] Chen,T., Cai,X., Wu,X., Karahara, I., Schreiber,L., and Lin,J. (2011). Casparian strip development and its potential function in salt tolerance. Plant Signal. Behav. 6: 1499-1502.

[29] Chen,W.K., Chen,L., Zhang,X., Yang, N., Guo,J.H., Wang,M., Ji,S.H., Zhao,X.Y., Yin, P.F., Cai,L.C., et al. (2022). Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science 375: eabg7985.

[30] Chen,X., Ding,Y., Yang,Y., Song, C., Wang,B., Yang,S., Guo,Y., and Gong,Z. (2021). Protein kinases in plant responses to drought, salt, and cold stress. J. Integr. Plant Biol. 63: 53-78.

[31] Christmann,A., Grill,E., and Huang,J. (2013). Hydraulic signals in long-distance signaling. Curr. Opin. Plant Biol. 16: 293-300.

[32] Chu,M., Chen,P., Meng,S., Xu, P., and Lan,W. (2021). The Arabidopsis phosphatase PP2C49 negatively regulates salt tolerance through inhibition of AtHKT1;1. J. Integr. Plant Biol. 63: 528-542.

[33] Colmenero-Flores,J.M., Martínez, G., Gamba,G., Vázquez,N., Iglesias, D.J., Brumós,J., and Talón,M. (2007). Identification and functional characterization of cation-chloride cotransporters in plants. Plant J. 50: 278-292.

[34] Cubero-Font,P., Maierhofer, T., Jaslan,J., Rosales,M.A., Espartero, J., Díaz-Rueda,P., Müller,H.M., Hürter,A.L., Al-Rasheid, K.A., Marten,I., et al. (2016). Silent S-type anion channel subunit SLAH1 gates SLAH3 open for chloride root-to-shoot translocation. Curr. Biol. 26: 2213-2220.

[35] Cui,M., Li,Y., Li,J., Yin, F., Chen,X., Qin,L., Wei,L., Xia,G., and Liu, S. (2023). Ca²⁺-dependent TaCCD1 cooperates with TaSAUR215 to enhance plasma membrane H⁺-ATPase activity and alkali stress tolerance by inhibiting PP2C-mediated dephosphorylation of TaHA2 in wheat. Mol. Plant 16: 571-587.

[36] Dangoor,I., Peled-Zehavi, H., Wittenberg,G., and Danon,A. (2012). A chloroplast light-regulated oxidative sensor for moderate light intensity in Arabidopsis. Plant Cell 24: 1894-1906.

[37] Das,K., and Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Env. Sci. 2: 1-13.

[38] De Angeli,A., Zhang,J., Meyer,S., and Martinoia, E. (2013). AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat. Commun. 4: 1804.

[39] Deng,P., Cao,C., Shi,X., Jiang, Q., Ge,J., Shen,L., Guo,C., Jiang,L., Jing, W., and Zhang,W. (2023). OsCYBDOMG1, a cytochrome b561 domain-containing protein, regulates salt tolerance and grain yield in rice. Theor. Appl. Genet. 136: 76.

[40] Deng,P., Jing,W., Cao,C., Sun, M., Chi,W., Zhao,S., Dai,J., Shi,X., Wu, Q., Zhang,B., et al. (2022). Transcriptional repressor RST1 controls salt tolerance and grain yield in rice by regulating gene expression of asparagine synthetase. Proc. Natl. Acad. Sci. U.S.A. 119: e2210338119.

[41] Do,T.D., Vuong,T.D., Dunn,D., Clubb, M., Valliyodan,B., Patil,G., Chen,P., Xu,D., Nguyen, H.T., and Shannon,J.G. (2019). Identification of new loci for salt tolerance in soybean by high-resolution genome-wide association mapping. BMC Genomics 20: 318.

[42] Dobrenel,T., Caldana, C., Hanson,J., Robaglia,C., Vincentz, M., Veit,B., and Meyer,C. (2016). TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67: 261-285.

[43] Dong,L., Hou,Z., Li,H., Li, Z., Fang,C., Kong,L., Li,Y., Du,H., Li, T., Wang,L., et al. (2022a). Agronomical selection on loss-of-function of GIGANTEA simultaneously facilitates soybean salt tolerance and early maturity. J. Integr. Plant Biol. 64: 1866-1882.

[44] Dong,Q., Wallrad, L., Almutairi,B., and Kudla,J. (2022b). Ca²⁺ signaling in plant responses to abiotic stresses. J. Integr. Plant Biol. 64: 287-300.

[45] Drozdowicz,Y.M., and Rea, P.A. (2001). Vacuolar Hþ pyrophosphatases: From the evolutionary backwaters into the mainstream. Trends Plant Sci. 6: 206-211.

[46] Du,F., Wang,Y., Wang,J., Li, Y., Zhang,Y., Zhao,X., Xu,J., Li,Z., Zhao, T., Wang,W., et al. (2023). The basic helix-loop-helix transcription factor gene, OsbHLH38, plays a key role in controlling rice salt tolerance. J. Integr. Plant Biol. 65: 1859-1873.

[47] Duan,L., Sebastian, J., and Dinneny,J.R. (2015). Salt-stress regulation of root system growth and architecture in Arabidopsis seedlings. Methods Mol. Biol. 1242: 105-122.

[48] Dubcovsky,J., María, G.S., Epstein,E., Luo,M.-C., and Dvořák, J. (1996). Mapping of the K⁺/Na⁺ discrimination locus Kna1 in wheat. Theor. Appl. Genet. 92: 448-454.

[49] Evans,M.J., Choi,W.G., Gilroy,S., and Morris, R.J. (2016). A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress. Plant Physiol. 171: 1771-1784.

[50] Falhof,J., Pedersen, J.T., Fuglsang,A.T., and Palmgren,M. (2016). Plasma membrane H⁺-ATPase regulation in the center of plant physiology. Mol. Plant 9: 323-337.

[51] Fang,S., Hou,X., and Liang,X. (2021). Response mechanisms of plants under saline-alkali stress. Front. Plant Sci. 12: 667458.

[52] Feki,K., Quintero, F.J., Pardo,J.M., and Masmoudi,K. (2011). Regulation of durum wheat Na⁺/H⁺ exchanger TdSOS1 by phosphorylation. Plant Mol. Biol. 76: 545-556.

[53] Feng,C., Gao,H., Zhou,Y., Jing, Y., Li,S., Yan,Z., Xu,K., Zhou,F., Zhang, W., Yang,X., et al. (2023). Unfolding molecular switches for salt stress resilience in soybean: Recent advances and prospects for salt-tolerant smart plant production. Front. Plant Sci. 14: 1162014.

[54] Feng,W., Kita,D., Peaucelle,A., Cartwright,H.N., Doan,V., Duan,Q., Liu, M.C., Maman,J., Steinhorst,L., Schmitz-Thom, I., et al. (2018). The FERONIA receptor kinase maintains cell wall integrity during salt stress through Ca²⁺ signaling. Curr. Biol. 28: 666-675.

[55] Feng,X.J., Li,J.R., Qi,S.L., Lin, Q.F., Jin,J.B., and Hua,X.J. (2016). Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 113: E8335-E8343.

[56] Franco-Navarro,J.D., Brumós, J., Rosales,M.A., Cubero-Font,P., Talón, M., and Colmenero-Flores,J.M. (2016). Chloride regulates leaf cell size and water relations in tobacco plants. J. Exp. Bot. 67: 873-891.

[57] Fu,H., Yu,X., Jiang,Y., Wang, Y., Yang,Y., Chen,S., Chen,Q., and Guo,Y. (2023). SALT OVERLY SENSITIVE 1 is inhibited by clade D protein phosphatase 2C D6 and D7 in Arabidopsis thaliana. Plant Cell 35: 279-297.

[58] Fuglsang,A.T., Guo,Y., Cuin,T.A., Qiu, Q., Song,C., Kristiansen,K.A., Bych, K., Schulz,A., Shabala,S., Schumaker, K.S., et al. (2007). Arabidopsis protein kinase PKS5 inhibits the plasma membrane H⁺-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19: 1617-1634.

[59] Galvan-Ampudia,C.S., Julkowska, M.M., Darwish,E., Gandullo,J., Korver, R.A., Brunoud,G., Haring,M.A., Munnik, T., Vernoux,T., and Testerink,C. (2013). Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23: 2044-2050.

[60] Gasulla,F., Barreno, E., Parages,M.L., Cámara,J., Jiménez, C., Dörmann,P., and Bartels,D. (2016). The Role of phospholipase D and MAPK signaling cascades in the adaption of lichen microalgae to desiccation: Changes in membrane lipids and phosphoproteome. Plant Cell Physiol. 57: 1908-1920.

[61] Geilfus,C.M. (2018). Chloride: From nutrient to toxicant. Plant Cell Physiol. 59: 877-886.

[62] Giacomello,S., Salmén, F., Terebieniec,B.K., Vickovic,S., Navarro, J.F., Alexeyenko,A., Reimegård,J., McKee, L.S., Mannapperuma,C., Bulone,V., et al. (2017). Spatially resolved transcriptome profiling in model plant species. Nat. Plants 3: 17061.

[63] Gierth,M., Mäser, P., and Schroeder,J.I. (2005). The potassium transporter AtHAK5 functions in K⁺ deprivation-induced high-affinity K⁺ uptake and AKT1 K⁺ channel contribution to K⁺ uptake kinetics in Arabidopsis roots. Plant Physiol. 137: 1105-1114.

[64] Gill,S.S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48: 909-930.

[65] Goff,S.A., Ricke,D., and Lan,T.-H. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100.

[66] Golani,Y., Kaye,Y., Gilhar,O., Ercetin, M., Gillaspy,G., and Levine,A. (2013). Inositol polyphosphate phosphatidylinositol 5-phosphatase9 (At5ptase9) controls plant salt tolerance by regulating endocytosis. Mol. Plant 6: 1781-1794.

[67] Gong,Z., Xiong,L., Shi,H., Yang, S., Herrera-Estrella,L.R., Xu,G., Chao, D.Y., Li,J., Wang,P.Y., Qin,F., et al. (2020). Plant abiotic stress response and nutrient use efficiency. Sci. China Life Sci. 63: 635-674.

[68] Grabov,A. (2007). Plant KT/KUP/HAK potassium transporters: Single family—Multiple functions. Ann. Bot. 99: 1035-1041.

[69] Guan,R., Qu,Y., Guo,Y., Yu, L., Liu,Y., Jiang,J., Chen,J., Ren,Y., Liu, G., Tian,L., et al. (2014). Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J. 80: 937-950.

[70] Guo,R., Shi,L., Yan,C., Zhong, X., Gu,F., Liu,Q., Xia,X., and Li,H. (2017). Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol. 17: 41.

[71] Halfter,U., Ishitani, M., and Zhu,J.K. (2000). The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. U.S.A. 97: 3735-3740.

[72] Hamaji,K., Nagira, M., Yoshida,K., Ohnishi,M., Oda,Y., Uemura,T., Goh, T., Sato,M.H., Morita,M.T., Tasaka, M., et al. (2009). Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis. Plant Cell Physiol. 50: 2023-2033.

[73] Hamilton,E.S., Jensen, G.S., Maksaev,G., Katims,A., Sherp,A.M., and Haswell,E.S. (2015). Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350: 438-441.

[74] Han,R., Ma,L., Lv,Y., Qi, L., Peng,J., Li,H., Zhou,Y., Song,P., Duan, J., Li,J., et al. (2023). SALT OVERLY SENSITIVE2 stabilizes phytochrome-interacting factors PIF4 and PIF5 to promote Arabidopsis shade avoidance. Plant Cell 35: 2972-2996.

[75] Hao,R., Zhou,W., Li,J., Luo, M., Scheres,B., and Guo,Y. (2023). On salt stress, PLETHORA signaling maintains root meristems. Dev. Cell 58: 1657-1669.

[76] Haruta,M., Sabat,G., Stecker,K., Minkoff, B.B., and Sussman,M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408-411.

[77] Hayes,S., Pantazopoulou, C.K., van Gelderen,K., Reinen,E., Tween,A.L., Sharma,A., de Vries, M., Prat,S., Schuurink,R.C., Testerink, C., et al. (2019). Soil salinity limits plant shade avoidance. Curr. Biol. 29: 1669-1676.

[78] He,Q., Jin,J., Lou,H., Dang, F., Xu,J., Zheng,S., and Yang, J. (2022). Abscisic acid-dependent PMT1 expression regulates salt tolerance by alleviating abscisic acid-mediated reactive oxygen species production in Arabidopsis. J. Integr. Plant Biol. 64: 1803-1820.

[79] He,Y., Yang,B., He,Y., Zhan, C., Cheng,Y., Zhang,J., Zhang,H., Cheng,J., and Wang, Z. (2019). A quantitative trait locus, qSE3, promotes seed germination and seedling establishment under salinity stress in rice. Plant J. 97: 1089-1104.

[80] Henderson,S.W., Wege,S., and Gilliham,M. (2018). Plant Cation-Chloride Cotransporters (CCC): Evolutionary origins and functional insights. Int. J. Mol. Sci. 19: 492.

[81] Henry,C., Bledsoe, S.W., Griffiths,C.A., Kollman,A., Paul,M.J., Sakr,S., and Lagrimini, L.M. (2015). Differential role for trehalose metabolism in salt-stressed maize. Plant Physiol. 169: 1072-1089.

[82] Hickey,L.T., N. Hafeez, A., Robinson,H., Jackson,S.A., Leal-Bertioli, S.C.M., Tester,M., Gao,C., Godwin, I.D., Hayes,B.J., and Wulff,B.B.H. (2019). Breeding crops to feed 10 billion. Nat. Biotechnol. 37: 744-754.

[83] Hong,Y., Guan,X., Wang,X., Kong, D., Yu,S., Wang,Z., Yu,Y., Chao,Z.F., Liu, X., Huang,S., et al. (2022). Natural variation in SlSOS2 promoter hinders salt resistance during tomato domestication. Hortic. Res. 10: uhac244.

[84] Horie,T., Costa,A., Kim,T.H., Han, M.J., Horie,R., Leung,H.Y., Miyao,A., Hirochika,H., An,G., and Schroeder, J.I. (2007). Rice OsHKT2;1 transporter mediates large Na⁺ influx component into K⁺-starved roots for growth. EMBO J. 26: 3003-3014.

[85] Hou,Z., Li,Y., Cheng,Y., Li, W., Li,T., Du,H., Kong,F., Dong,L., Zheng, D., Feng,N., et al. (2022). Genome-wide analysis of DREB genes identifies a novel salt tolerance gene in wild soybean (Glycine soja). Front. Plant Sci. 13: 821647.

[86] Huang,S., Spielmeyer, W., Lagudah,E.S., James,R.A., Platten, J.D., Dennis,E.S., and Munns,R. (2006). A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol. 142: 1718-1727.

[87] Huang,X., and Han, B. (2014). Natural variations and genome-wide association studies in crop plants. Annu. Rev. Plant Biol. 65: 531-551.

[88] Huang,X., Wei,X., Sang,T., Zhao, Q., Feng,Q., Zhao,Y., Li,C., Zhu,C., Lu, T., Zhang,Z., et al. (2010). Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42: 961-967.

[89] Ichimura,K., Shinozaki, K., Tena,G., Sheen,J., Henry,Y., et al. (2002). Mitogen-activated protein kinase cascades in plants: A new nomenclature. Trends Plant Sci. 7: 301-308.

[90] International Wheat Genome Sequencing Consortium (IWGSC). (2018). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361: eaar7191.

[91] Ishitani,M., Liu,J., Halfter,U., Kim, C.S., Shi,W., and Zhu,J.K. (2000). SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12: 1667-1678.

[92] Ismail,A., Takeda, S., and Nick,P. (2014). Life and death under salt stress: Same players, different timing? J. Exp. Bot. 65: 2963-2979.

[93] Ismail,A.M., and Horie, T. (2017). Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu. Rev. Plant Biol. 68: 405-434.

[94] James,R.A., Blake,C., Byrt,C.S., and Munns, R. (2011). Major genes for Na⁺ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na⁺ accumulation in bread wheat leaves under saline and waterlogged conditions. J. Exp. Bot. 62: 2939-2947.

[95] Javid,M., Ford,R., and Nicolas,M.E. (2012). Tolerance responses of Brassica juncea to salinity, alkalinity and alkaline salinity. Funct. Plant Biol. 39: 699-707.

[96] Jiang,C., Belfield, E.J., Cao,Y., Smith,J.A., and Harberd, N.P. (2013). An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25: 3535-3552.

[97] Jiao,Y., Zhao,H., Ren,L., Song, W., Zeng,B., Guo,J., Wang,B., Liu,Z., Chen, J., Li,W., et al. (2012). Genome-wide genetic changes during modern breeding of maize. Nat. Genet. 44: 812-815.

[98] Jin,T., Sun,Y., Shan,Z., He, J., Wang,N., Gai,J., and Li, Y. (2021). Natural variation in the promoter of GsERD15B affects salt tolerance in soybean. Plant Biotechnol. J. 19: 1155-1169.

[99] Jossier,M., Kroniewicz, L., Dalmas,F., Le Thiec,D., Ephritikhine, G., Thomine,S., Barbier-Brygoo,H., Vavasseur, A., Filleur,S., and Leonhardt,N. (2010). The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant J. 64: 563-576.

[100] Kim,B.G., Waadt,R., Cheong,Y.H., Pandey, G.K., Dominguez-Solis,J.R., Schültke,S., Lee, S.C., Kudla,J., and Luan,S. (2007a). The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52: 473-484.

[101] Kim,J.M., Woo,D.H., Kim,S.H., Lee, S.Y., Park,H.Y., Seok,H.Y., Chung,W.S., and Moon,Y.H. (2012). Arabidopsis MKKK20 is involved in osmotic stress response via regulation of MPK6 activity. Plant Cell Rep. 31: 217-224.

[102] Kim,S.G., Kim,S.Y., and Park,C.M. (2007b). A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226: 647-654.

[103] Kim,S.H., Woo,D.H., Kim,J.M., Lee, S.Y., Chung,W.S., and Moon,Y.H. (2011). Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem. Biophys. Res. Commun. 412: 150-154.

[104] Kim,W.Y., Ali,Z., Park,H.J., Park, S.J., Cha,J.Y., Perez-Hormaeche,J., Quintero, F.J., Shin,G., Kim,M.R., Qiang,Z., et al. (2013). Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 4: 1352.

[105] Knight,H., Trewavas, A.J., and Knight,M.R. (1997). Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12: 1067-1078.

[106] Kumar,R., Bohra,A., Pandey,A.K., Pandey, M.K., and Kumar,A. (2017). Metabolomics for plant improvement: Status and prospects. Front. Plant Sci. 8: 1302.

[107] Kurusu,T., Nishikawa, D., Yamazaki,Y., Gotoh,M., Nakano, M., Hamada,H., Yamanaka,T., Iida,K., Nakagawa,Y., Saji, H., et al. (2012a). Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca²⁺ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol. 12: 11.

[108] Kurusu,T., Yamanaka, T., Nakano,M., Takiguchi,A., Ogasawara, Y., Hayashi,T., Iida,K., Hanamata, S., Shinozaki,K., Iida,H., et al. (2012b). Involvement of the putative Ca²⁺-permeable mechanosensitive channels, NtMCA1 and NtMCA2, in Ca²⁺ uptake, Ca²⁺-dependent cell proliferation and mechanical stress-induced gene expression in tobacco (Nicotiana tabacum) BY-2 cells. J. Plant Res. 125: 555-568.

[109] Lagarde,D., Basset, M., Lepetit,M., Conejero,G., Gaymard, F., Astruc,S., and Grignon,C. (1996). Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K⁺ nutrition. Plant J. 9: 195-203.

[110] Laohavisit,A., Richards, S.L., Shabala,L., Chen,C., Colaço, R.D., Swarbreck,S.M., Shaw,E., Dark,A., Shabala,S., Shang, Z., et al. (2013). Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin1. Plant Physiol. 163: 253-262.

[111] Laplante,M., and Sabatini, D.M. (2012). mTOR signaling in growth control and disease. Cell 149: 274-293.

[112] Lei,L., Cao,L., Ding,G., Zhou, J., Luo,Y., Bai,L., Xia,T., Chen,L., Wang, J., Liu,K., et al. (2023). OsBBX11 on qSTS4 links to salt tolerance at the seeding stage in Oryza sativa L. ssp. Japonica. Front. Plant Sci. 14: 1139961.

[113] Leshem,Y., Melamed-Book, N., Cagnac,O., Ronen,G., Nishri, Y., Solomon,M., Cohen,G., and Levine, A. (2006). Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H₂O₂-containing vesicles with tonoplast and increased salt tolerance. Proc. Natl. Acad. Sci. U.S.A. 103: 18008-18013.

[114] Li,B., Byrt,C., Qiu,J., Baumann, U., Hrmova,M., Evrard,A., Johnson, A.A., Birnbaum,K.D., Mayo,G.M., Jha,D., et al. (2016). Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiol. 170: 1014-1029.

[115] Li,B., Qiu,J., Jayakannan,M., Xu,B., Li,Y., Mayo,G.M., Tester, M., Gilliham,M., and Roy,S.J. (2017a). AtNPF2.5 modulates chloride (Cl⁻) efflux from roots of Arabidopsis thaliana. Front. Plant Sci. 7: 2013.

[116] Li,B., Tester, M., and Gilliham,M. (2017b). Chloride on the move. Trends Plant Sci. 22: 236-248.

[117] Li,C., Lu,H., Li,W., Yuan, M., and Fu,Y. (2017). A ROP2-RIC1 pathway fine-tunes microtubule reorganization for salt tolerance in Arabidopsis. Plant Cell Environ. 40: 1127-1142.

[118] Li,C., Wang,G., Zhao,J., Zhang, L., Ai,L., Han,Y., Sun,D., Zhang,S., and Sun, Y. (2014). The receptor-like kinase SIT1 mediates salt sensitivity by sctivating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell 26: 2538-2553.

[119] Li,J., Shen,L., Han,X., He, G., Fan,W., Li,Y., Yang,S., Zhang,Z., Yang, Y., Jin,W., et al. (2023a). Phosphatidic acid-regulated SOS2 controls sodium and potassium homeostasis in Arabidopsis under salt stress. EMBO J. 42: e112401.

[120] Li,J., Zhou,H., Zhang,Y., Li, Z., Yang,Y., and Guo,Y. (2020a). The GSK3-like kinase BIN2 is a molecular switch between the salt stress response and growth recovery in Arabidopsis thaliana. Dev. Cell 55: 367-380.e366.

[121] Li,J., Zhou,X., Wang,Y., Song, S., Ma,L., He,Q., Lu,M., Zhang,K., Yang, Y., Zhao,Q., et al. (2023b). Inhibition of the maize salt overly sensitive pathway by ZmSK3 and ZmSK4. J. Genet. Genomics 50: 960-970.

[122] Li,Q., Xu,F., Chen,Z., Teng, Z., Sun,K., Li,X., Yu,J., Zhang,G., Liang, Y., Huang,X., et al. (2021). Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nat. Plants 7: 1108-1118.

[123] Li,S., Tian,Y.H., Wu,K., Ye, Y.F., Yu,J.P., Zhang,J.Q., Liu,Q., Hu,M.Y., Li, H., Tong,Y.P., et al. (2018a). Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560: 595-600.

[124] Li,S., Wang,N., Ji,D., Zhang, W., Wang,Y., Yu,Y., Zhao,S., Lyu,M., You, J., Zhang,Y., et al. (2019). A GmSIN1/GmNCED3s/GmRbohBs feed-forward loop acts as a signal amplifier that regulates root growth in soybean exposed to salt stress. Plant Cell 31: 2107-2130.

[125] Li,X., Zheng,H., Wu,W., Liu, H., Wang,J., Jia,Y., Li,J., Yang,L., Lei, L., Zou,D., et al. (2020b). QTL mapping and candidate gene analysis for alkali tolerance in Japonica rice at the bud stage based on linkage mapping and genome-wide association study. Rice 13: 48.

[126] Li,Y., Chu,Z., Luo,J., Zhou, Y., Cai,Y., Lu,Y., Xia,J., Kuang,H., Ye, Z., and Ouyang,B. (2018b). The C2H2 zinc-finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B. Plant Biotechnol. J. 16: 1201-1213.

[127] Li,Z., Zhong,F., Guo,J., Chen, Z., Song,J., and Zhang,Y. (2022). Improving wheat salt tolerance for saline agriculture. J. Agric. Food Chem. 70: 14989-15006.

[128] Liang,X., Liu,S., Wang,T., Li, F., Cheng,J., Lai,J., Qin,F., Li,Z., Wang, X., and Jiang,C. (2021a). Metabolomics-driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize. New Phytol. 230: 2355-2370.

[129] Liang,Y., Liu,H.J., Yan,J., and Tian, F. (2021b). Natural variation in crops: Realized understanding, continuing promise. Annu. Rev. Plant Biol. 72: 357-385.

[130] Liao,H., Tang,R., Zhang,X., Luan, S., and Yu,F. (2017). FERONIA receptor kinase at the crossroads of hormone signaling and stress responses. Plant Cell Physiol. 58: 1143-1150.

[131] Lin,H., Du,W., Yang,Y., Schumaker, K.S., and Guo,Y. (2014). A calcium-independent activation of the Arabidopsis SOS2-like protein kinase24 by its interacting SOS3-like calcium binding protein1. Plant Physiol. 164: 2197-2206.

[132] Lin,H., Zhu,M., Yano,M., Gao, J., Liang,Z., Su,W.A., Hu,X., Ren,Z., and Chao, D. (2003). QTLs for Na⁺ and K⁺ uptake of the shoots and roots controlling rice salt tolerance. Theor. Appl. Genet. 108: 253-260.

[133] Lin,Z., Li,Y., Wang,Y., Liu, X., Ma,L., Zhang,Z., Mu,C., Zhang,Y., Peng, L., Xie,S., et al. (2021). Initiation and amplification of SnRK2 activation in abscisic acid signaling. Nat. Commun. 12: 2456.

[134] Lin,Z., Li,Y., Zhang,Z., Liu, X., Hsu,C.C., Du,Y., Sang,T., Zhu,C., Wang, Y., Satheesh,V., et al. (2020). A RAF-SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat. Commun. 11: 613.

[135] Lindsay,M.P., Lagudah, E.S., Hare,R.A., and Munns,R. (2004). A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct. Plant Biol. 31: 1105-1114.

[136] Linh,L.H., Linh,T.H., Xuan,T.D., Ham, L.H., Ismail,A.M., and Khanh,T.D. (2012). Molecular breeding to improve salt tolerance of rice (Oryza sativa L.) in the Red River delta of Vietnam. Int. J. Plant Genomics 2012: 1-9.

[137] Lister,R., O'Malley, R.C., Tonti-Filippini,J., Gregory,B.D., Berry,C.C., Millar,A.H., and Ecker, J.R. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523-536.

[138] Liu,G., Jiang,W., Tian,L., Fu, Y., Tan,L., Zhu,Z., Sun,C., and Liu,F. (2022a). Polyamine oxidase 3 is involved in salt tolerance at the germination stage in rice. J. Genet. Genomics 49: 458-468.

[139] Liu,J., Ishitani, M., Halfter,U., Kim,C.S., and Zhu, J.K. (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. U.S.A. 97: 3730-3734.

[140] Liu,J., and Zhu, J.K. (1997). An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc. Natl. Acad. Sci. U.S.A. 94: 14960-14964.

[141] Liu,J., and Zhu, J.K. (1998). A calcium sensor homolog required for plant salt tolerance. Science 280: 1943-1945.

[142] Liu,L., Song,W., Huang,S., Jiang, K., Moriwaki,Y., Wang,Y., Men,Y., Zhang,D., Wen, X., Han,Z., et al. (2022b). Extracellular pH sensing by plant cell-surface peptide-receptor complexes. Cell 185: 3341-3355.

[143] Liu,Q., Liu,W., Niu,Y., Wang, T., and Dong,J. (2023a). Liquid-liquid phase separation in plants: Advances and perspectives from model species to crops. Plant Commun. 5: 100663.

[144] Liu,S., Liu,S., Wang,M., Wei, T., Meng,C., Wang,M., and Xia, G. (2014). A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell 26: 164-180.

[145] Liu,X., Jiang,W., Li,Y., Nie, H., Cui,L., Li,R., Tan,L., Peng,L., Li, C., Luo,J., et al. (2023b). FERONIA coordinates plant growth and salt tolerance via the phosphorylation of phyB. Nat. Plants 9: 645-660.

[146] Liu,X., Yu,X., Shi,Y., Ma, L., Fu,Y., and Guo,Y. (2023c). Phosphorylation of RhoGDI1, a Rho GDP dissociation inhibitor, regulates root hair development in Arabidopsis under salt stress. Proc. Natl. Acad. Sci. U.S.A. 120: e2217957120.

[147] Liu,Y., Li,M., Yu,J., Ma, A., Wang,J., Yun,D., and Xu, Z. (2023d). Plasma membrane-localized Hsp40/DNAJ chaperone protein facilitates OsSUVH7-OsBAG4-OsMYB106 transcriptional complex formation for OsHKT1;5 activation. J. Integr. Plant Biol. 65: 265-279.

[148] Livanos,P., Galatis, B., Gaitanaki,C., and Apostolakos,P. (2014). Phosphorylation of a p38-like MAPK is involved in sensing cellular redox state and drives atypical tubulin polymer assembly in angiosperms. Plant Cell Environ. 37: 1130-1143.

[149] Lou,L., Yu,F., Tian,M., Liu, G., Wu,Y., Wu,Y., Xia,R., Pardo,J.M., Guo, Y., and Xie,Q. (2020). ESCRT-I component VPS23A sustains salt tolerance by strengthening the SOS module in Arabidopsis. Mol. Plant 13: 1134-1148.

[150] Luo,M., Zhang,Y., Li,J., Zhang, P., Chen,K., Song,W., Wang,X., Yang,J., Lu, X., Lu,B., et al. (2021). Molecular dissection of maize seedling salt tolerance using a genome-wide association analysis method. Plant Biotechnol. J. 19: 1937-1951.

[151] Lu,K., Song,R., Guo,J., Zhang, Y., Zuo,J., Chen,H., Liao,C., Hu,X., Ren, F., Lu,Y., et al. (2023). CycC1;1-WRKY75 complex-mediated transcriptional regulation of SOS1 controls salt stress tolerance in Arabidopsis. Plant Cell 35: 2570-2591.

[152] Lutts,S., Kinet,J.M., and Bouharmont,J. (1995). Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J. Exp. Bot. 46: 1843-1852.

[153] Ma,J., Li,C., Sun,L., Ma, X., Qiao,H., Zhao,W., Yang,R., Song,S., Wang, S., and Huang,H. (2023a). The SlWRKY57-SlVQ21/SlVQ16 module regulates salt stress in tomato. J. Integr. Plant Biol. 65: 2437-2455.

[154] Ma,L., Han,R., Yang,Y., Liu, X., Li,H., Zhao,X., Li,J., Fu,H., Huo, Y., Sun,L., et al. (2023b). Phytochromes enhance SOS2-mediated PIF1 and PIF3 phosphorylation and degradation to promote Arabidopsis salt tolerance. Plant Cell 35: 2997-3020.

[155] Ma,L., Ye,J., Yang,Y., Lin, H., Yue,L., Luo,J., Long,Y., Fu,H., Liu, X., Zhang,Y., et al. (2019). The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev. Cell 48: 697-709.e695.

[156] Ma,Y., Szostkiewicz, I., Korte,A., Moes,D., Yang,Y., Christmann,A., and Grill,E. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.

[157] Mahfouz,M.M., Kim,S., Delauney,A.J., and Verma,D.P. (2006). Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18: 477-490.

[158] Mann,A., Lata,C., Kumar,N., Kumar, A., Kumar,A., and Sheoran,P. (2023). Halophytes as new model plant species for salt tolerance strategies. Front. Plant Sci. 14: 1137211.

[159] Mansour,M.M.F., and Ali, E.F. (2017). Evaluation of proline functions in saline conditions. Phytochemistry 140: 52-68.

[160] Mao,H., Sun,S., Yao,J., Wang, C., Yu,S., Xu,C., Li,X., and Zhang,Q. (2010). Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc. Natl. Acad. Sci. U.S.A. 107: 19579-19584.

[161] Martínez-Atienza,J., Jiang,X., Garciadeblas, B., Mendoza,I., Zhu,J.K., Pardo,J.M., and Quintero,F.J. (2007). Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 143: 1001-1012.

[162] Mazel,A., Leshem, Y., Tiwari,B.S., and Levine,A. (2004). Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol. 134: 118-128.

[163] Mian,A., Oomen,R.J., Isayenkov,S., Sentenac,H., Maathuis, F.J., and Véry,A.A. (2011). Over-expression of an Na⁺-and K⁺-permeable HKT transporter in barley improves salt tolerance. Plant J. 68: 468-479.

[164] Miao,Y., Lv,D., Wang,P., Wang, X.C., Chen,J., Miao,C., and Song, C.P. (2006). An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18: 2749-2766.

[165] Miller,G., and Mittler, R. (2006). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98: 279-288.

[166] Miller,G., Suzuki, N., Ciftci-Yilmaz,S., and Mittler,R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33: 453-467.

[167] Munns,R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25: 239-250.

[168] Munns,R. (2005). Genes and salt tolerance: Bringing them together. New Phytol. 167: 645-663.

[169] Munns,R., and Gilliham, M. (2015). Salinity tolerance of crops—What is the cost? New Phytol. 208: 668-673.

[170] Munns,R., James,R.A., Xu,B., Athman, A., Conn,S.J., Jordans,C., Byrt,C.S., Hare,R.A., Tyerman, S.D., Tester,M., et al. (2012). Wheat grain yield on saline soils is improved by an ancestral Na⁺ transporter gene. Nat. Biotechnol. 30: 360-364.

[171] Munns,R., Passioura, J.B., Colmer,T.D., and Byrt,C.S. (2020). Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol. 225: 1091-1096.

[172] Munns,R., Rebetzke, G.J., Husain,S., James,R.A., and Hare, R.A. (2003). Genetic control of sodium exclusion in durum wheat. Aust. J. Agric. Res. 54: 627-635.

[173] Munns,R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681.

[174] Negi,J., Matsuda, O., Nagasawa,T., Oba,Y., Takahashi, H., Kawai-Yamada,M., Uchimiya,H., Hashimoto, M., and Iba,K. (2008). CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452: 483-486.

[175] Nguyen,C.T., Agorio, A., Jossier,M., DepréS., Thomine, S., and Filleur,S. (2016). Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol. 57: 764-775.

[176] Noctor,G., and Foyer, C.H. (1998). ASCORBATE AND GLUTATHIONE: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249-279.

[177] Oda,Y., Kobayashi, N.I., Tanoi,K., Ma,J.F., Itou,Y., Katsuhara,M., Itou,T., and Horie, T. (2018). T-DNA tagging-based gain-of-function of OsHKT1;4 reinforces na exclusion from leaves and stems but triggers Na toxicity in roots of rice under salt stress. Int. J. Mol. Sci. 19: 235.

[178] Ogasawara,Y., Kaya,H., Hiraoka,G., Yumoto, F., Kimura,S., Kadota,Y., Hishinuma, H., Senzaki,E., Yamagoe,S., Nagata, K., et al. (2008). Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca²⁺ and phosphorylation. J. Biol. Chem. 283: 8885-8892.

[179] Ogawa-Ohnishi,M., Yamashita, T., Kakita,M., Nakayama,T., Ohkubo, Y., Hayashi,Y., Yamashita,Y., Nomura, T., Noda,S., Shinohara,H., et al. (2022). Peptide ligand-mediated trade-off between plant growth and stress response. Science 378: 175-180.

[180] Pabuayon,I.C.M., Jiang,J., Qian,H., Chung, J.S., and Shi,H. (2021). Gain-of-function mutations of AtNHX1 suppress sos1 salt sensitivity and improve salt tolerance in Arabidopsis. Stress Biol. 1: 14.

[181] Panuccio,M.R., Chaabani, S., Roula,R., and Muscolo,A. (2018). Bio-priming mitigates detrimental effects of salinity on maize improving antioxidant defense and preserving photosynthetic efficiency. Plant Physiol. Biochem. 132: 465-474.

[182] Park,H.J., Gámez-Arjona, F.M., Lindahl,M., Aman,R., Villalta, I., Cha,J.Y., Carranco,R., Lim,C.J., García,E., Bressan,R.A., et al. (2023). S-acylated and nucleus-localized SALT OVERLY SENSITIVE3/CALCINEURIN B-LIKE4 stabilizes GIGANTEA to regulate Arabidopsis flowering time under salt stress. Plant Cell 35: 298-317.

[183] Park,S.Y., Fung,P., Nishimura,N., Jensen,D.R., Fujii,H., Zhao,Y., Lumba, S., Santiago,J., Rodrigues,A., Chow,T.F., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.

[184] Park,Y.C., Lim,S.D., Moon,J.C., and Jang, C.S. (2019). A rice really interesting new gene H2-type E3 ligase, OsSIRH2-14, enhances salinity tolerance via ubiquitin/26S proteasome-mediated degradation of salt-related proteins. Plant Cell Environ. 42: 3061-3076.

[185] Peng,L., Xiao,H., Li,R., Zeng, Y., Gu,M., Moran,N., Yu,L., and Xu,G. (2023). Potassium transporter OsHAK18 mediates potassium and sodium circulation and sugar translocation in rice. Plant Physiol. 193: 2003-2020.

[186] Pommerrenig,B., Papini-Terzi, F.S., and Sauer,N. (2007). Differential regulation of sorbitol and sucrose loading into the phloem of Plantago major in response to salt stress. Plant Physiol. 144: 1029-1038.

[187] Qin,R., Hu,Y., Chen,H., Du, Q., Yang,J., and Li,W.X. (2023). MicroRNA408 negatively regulates salt tolerance by affecting secondary cell wall development in maize. Plant Physiol. 192: 1569-1583.

[188] Qiu,Q.S., Guo,Y., Dietrich,M.A., Schumaker,K.S., and Zhu, J.K. (2002). Regulation of SOS1, a plasma membrane Na⁺/H⁺ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U.S.A. 99: 8436-8441.

[189] Qiu,Q.S., Guo,Y., Quintero,F.J., Pardo,J.M., Schumaker, K.S., and Zhu,J.K. (2004). Regulation of vacuolar Na⁺/H⁺ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J. Biol. Chem. 279: 207-215.

[190] Qu,Y., Guan,R., Bose,J., Henderson, S.W., Wege,S., Qiu,L., and Gilliham, M. (2021). Soybean CHX-type ion transport protein GmSALT3 confers leaf Na⁺ exclusion via a root derived mechanism, and Cl⁻ exclusion via a shoot derived process. Plant Cell Environ. 44: 856-869.

[191] Quan,R., Lin,H., Mendoza,I., Zhang, Y., Cao,W., Yang,Y., Shang,M., Chen,S., Pardo, J.M., and Guo,Y. (2007). SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19: 1415-1431.

[192] Quintero,F.J., Martinez-Atienza, J., Villalta,I., Jiang,X., Kim,W.Y., Ali,Z., Fujii, H., Mendoza,I., Yun,D.J., Zhu,J.K., et al. (2011). Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 108: 2611-2616.

[193] Ragel,P., Ródenas, R., García-Martín, E., Andrés,Z., Villalta,I., Nieves-Cordones, M., Rivero,R.M., Martínez,V., Pardo, J.M., Quintero,F.J., et al. (2015). The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K⁺ uptake in Arabidopsis roots. Plant Physiol. 169: 2863-2873.

[194] Rao,K.P., Richa,T., Kumar,K., Raghuram, B., and Sinha,A.K. (2010). In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res. 17: 139-153.

[195] Rawat,N., Wungrampha, S., Singla-Pareek,S.L., Yu,M., Shabala, S., and Pareek,A. (2022). Rewilding staple crops for the lost halophytism: Toward sustainability and profitability of agricultural production systems. Mol. Plant 15: 45-64.

[196] Ren,Z., Bai,F., Xu,J., Wang, L., Wang,X., Zhang,Q., Feng,C., Niu,Q., Zhang, L., Song,J., et al. (2021). A chloride efflux transporter, BIG RICE GRAIN 1, is involved in mediating grain size and salt tolerance in rice. J. Integr. Plant Biol. 63: 2150-2163.

[197] Ren,Z.H., Gao,J.P., Li,L.G., Cai, X.L., Huang,W., Chao,D.Y., Zhu,M.Z., Wang,Z.Y., Luan, S., and Lin,H.X. (2005). A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37: 1141-1146.

[198] Ryu,J.Y., Lee,H.J., Seo,P.J., Jung, J.H., Ahn,J.H., and Park,C.M. (2014). The Arabidopsis floral repressor BFT delays flowering by competing with FT for FD binding under high salinity. Mol. Plant 7: 377-387.

[199] Ryu,K.H., Huang,L., Kang,H.M., and Schiefelbein, J. (2019). Single-Cell RNA sequencing resolves molecular relationships among individual plant cells. Plant Physiol. 179: 1444-1456.

[200] Sakuraba,Y., Kim,E.Y., Han,S.H., Piao, W., An,G., Todaka,D., Yamaguchi-Shinozaki, K., and Paek,N.C. (2017). Rice Phytochrome-Interacting Factor-Like1 (OsPIL1) is involved in the promotion of chlorophyll biosynthesis through feed-forward regulatory loops. J. Exp. Bot. 68: 4103-4114.

[201] Saneoka,H., Nagasaka, C., Hahn,D.T., Yang,W.J., Premachandra, G.S., Joly,R.J., and Rhodes,D. (1995). Salt tolerance of glycinebetaine-deficient and -containing maize lines. Plant Physiol. 107: 631-638.

[202] Schmutz,J., Cannon, S.B., Schlueter,J., Ma,J., Mitros, T., Nelson,W., Hyten,D.L., Song,Q., Thelen,J.J., Cheng, J., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.

[203] Schnable,P.S., Ware,D., and Fulton,R.S. (2009). The B73 maize genome: Complexity, diversity, and dynamics. Science 326: 1112-1115.

[204] Shabala,L., Zhang,J., Pottosin,I., Bose, J., Zhu,M., Fuglsang,A.T., Velarde-Buendia, A., Massart,A., Hill,C.B., Roessner, U., et al. (2016). Cell-type-specific H⁺-ATPase activity in root tissues enables K⁺ retention and mediates acclimation of barley (Hordeum vulgare) to salinity stress. Plant Physiol. 172: 2445-2458.

[205] Shi,H., Ishitani, M., Kim,C., and Zhu,J.K. (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na⁺/H⁺ antiporter. Proc. Natl. Acad. Sci. U.S.A. 97: 6896-6901.

[206] Shi,H., Quintero, F.J., Pardo,J.M., and Zhu,J.K. (2002). The putative plasma membrane Na⁺/H⁺antiporter SOS1 controls long-distance Na⁺ transport in plants. Plant Cell 14: 465-477.

[207] Song,T., Shi,Y., Shen,L., Cao, C., Shen,Y., Jing,W., Tian,Q., Lin,F., Li, W., and Zhang,W. (2021). An endoplasmic reticulum-localized cytochrome b5 regulates high-affinity K⁺ transport in response to salt stress in rice. Proc. Natl. Acad. Sci. U.S.A. 118: e211434711.

[208] Steinhorst,L., He,G., Moore,L.K., Schültke, S., Schmitz-Thom,I., Cao,Y., Hashimoto, K., Andrés,Z., Piepenburg,K., Ragel,P., et al. (2022). A Ca²⁺-sensor switch for tolerance to elevated salt stress in Arabidopsis. Dev. Cell 57: 2081-2094.e2087.

[209] Stephan,A.B., Kunz,H.H., Yang,E., and Schroeder, J.I. (2016). Rapid hyperosmotic-induced Ca²⁺ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters. Proc. Natl. Acad. Sci. U.S.A. 113: E5242-E5249.

[210] Sun,F., Zhang,W., Hu,H., Li, B., Wang,Y., Zhao,Y., Li,K., Liu,M., and Li, X. (2008). Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol. 146: 178-188.

[211] Sun,W., Zhang,H., Yang,S., Liu, L., Xie,P., Li,J., Zhu,Y., Ouyang,Y., Xie, Q., Zhang,H., et al. (2023). Genetic modification of Gγ subunit AT1 enhances salt-alkali tolerance in main graminaceous crops. Natl. Sci. Rev. 10: nwad075.

[212] Takahashi,F., Suzuki, T., Osakabe,Y., Betsuyaku,S., Kondo,Y., Dohmae,N., Fukuda, H., Yamaguchi-Shinozaki,K., and Shinozaki,K. (2018). A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556: 235-238.

[213] Takahashi,Y., Zhang,J., Hsu,P.K., Ceciliato, P.H.O., Zhang,L., Dubeaux,G., Munemasa, S., Ge,C., Zhao,Y., Hauser, F., et al. (2020). MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat. Commun. 11: 12.

[214] Takeno,K. (2016). Stress-induced flowering: The third category of flowering response. J. Exp. Bot. 67: 4925-4934.

[215] Teakle,N.L., and Tyerman, S.D. (2010). Mechanisms of Cl⁻ transport contributing to salt tolerance. Plant Cell Environ. 33: 566-589.

[216] Tester,M., and Davenport, R. (2003). Na⁺ tolerance and Na⁺ transport in higher plants. Ann. Bot. 91: 503-527.

[217] Thalmann,M., Pazmino, D., Seung,D., Horrer,D., Nigro,A., Meier,T., Kölling, K., Pfeifhofer,H.W., Zeeman,S.C., and Santelia, D. (2016). Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. Plant Cell 28: 1860-1878.

[218] Thomson,M.J., de Ocampo, M., Egdane,J., Rahman,M.A., Sajise, A.G., Adorada,D.L., Tumimbang-Raiz,E., Blumwald, E., Seraj,Z.I., Singh,R.K., et al. (2010). Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3: 148-160.

[219] Tian J,W.C., Xia,J., Wu,L., Xu, G., Wu,W., Li,D., Qin,W., Han,X., Chen, Q., Jin,W., et al. (2019). Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 16: 658-664.

[220] Uozumi,N., Kim,E.J., Rubio,F., Yamaguchi, T., Muto,S., Tsuboi,A., Bakker, E.P., Nakamura,T., and Schroeder,J.I. (2000). The Arabidopsis HKT1 gene homolog mediates inward Na⁺ currents in xenopus laevis oocytes and Na⁺ uptake in Saccharomyces cerevisiae. Plant Physiol. 122: 1249-1259.

[221] van Zelm,E., Zhang,Y., and Testerink,C. (2020). Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71: 403-433.

[222] Véry,A.A., Nieves-Cordones, M., Daly,M., Khan,I., Fizames, C., and Sentenac,H. (2014). Molecular biology of K⁺ transport across the plant cell membrane: What do we learn from comparison between plant species? J. Plant Physiol. 171: 748-769.

[223] Vlad,F., Rubio,S., Rodrigues,A., Sirichandra,C., Belin,C., Robert,N., Leung, J., Rodriguez,P.L., Laurière,C., and Merlot, S. (2009). Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21: 3170-3184.

[224] Walkowiak,S., Gao,L., Monat,C., et al. (2020). Multiple wheat genomes reveal global variation in modern breeding. Nature 588: 277-283.

[225] Wang,B., Zhang,H., Huai,J., Peng, F., Wu,J., Lin,R., and Fang, X. (2022a). Condensation of SEUSS promotes hyperosmotic stress tolerance in Arabidopsis. Nat. Chem. Biol. 18: 1361-1369.

[226] Wang,C., Zhang,L., and Huang,R. (2011). Cytoskeleton and plant salt stress tolerance. Plant Signal. Behav. 6: 29-31.

[227] Wang,J., Li,D., Peng,Y., Cai, M., Liang,Z., Yuan,Z., Du,X., Wang,J., Schnable, P.S., Gu,R., et al. (2022b). The anthocyanin accumulation related ZmBZ1, facilitates seedling salinity stress tolerance via ROS scavenging. Int. J. Mol. Sci. 23: 16123.

[228] Wang,J., Nan,N., Li,N., Liu, Y., Wang,T.J., Hwang,I., Liu,B., and Xu,Z.Y. (2020a). A DNA methylation reader-chaperone regulator-transcription factor complex activates OsHKT1;5 expression during salinity stress. Plant Cell 32: 3535-3558.

[229] Wang,M., Wang,M., Zhao,M., Wang, M., Liu,S., Tian,Y., Moon,B., Liang,C., Li, C., Shi,W., et al. (2022c). TaSRO1 plays a dual role in suppressing TaSIP1 to fine tune mitochondrial retrograde signalling and enhance salinity stress tolerance. New Phytol. 236: 495-511.

[230] Wang,M., Yuan,J., Qin,L., Shi, W., Xia,G., and Liu,S. (2019). TaCYP81D5, one member in a wheat cytochrome P450 gene cluster, confers salinity tolerance via reactive oxygen species scavenging. Plant Biotechnol. J. 18: 791-804.

[231] Wang,P., Zhao,Y., Li,Z., Hsu, C.C., Liu,X., Fu,L., Hou,Y.J., Du,Y., Xie, S., Zhang,C., et al. (2018a). Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol. Cell 69: 100-112.

[232] Wang,W., Mauleon, R., Hu,Z., Chebotarov,D., Tai,S., Wu,Z., Li, M., Zheng,T., Fuentes,R.R., Zhang,F., et al. (2018b). Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557: 43-49.

[233] Wang,W., Wang,W., Wu,Y., Li, Q., Zhang,G., Shi,R., Yang,J., Wang,Y., and Wang, W. (2020b). The involvement of wheat U-box E3 ubiquitin ligase TaPUB1 in salt stress tolerance. J. Integr. Plant Biol. 62: 631-651.

[234] Wang,X., Devaiah, S.P., Zhang,W., and Welti,R. (2006). Signaling functions of phosphatidic acid. Prog. Lipid Res. 45: 250-278.

[235] Wang,Y., Cao,Y., Liang,X., Zhuang, J., Wang,X., Qin,F., and Jiang, C. (2022d). A dirigent family protein confers variation of Casparian strip thickness and salt tolerance in maize. Nat. Commun. 13: 2222.

[236] Wang,Z., Hong,Y., Li,Y., Shi, H., Yao,J., Liu,X., Wang,F., Huang,S., Zhu, G., and Zhu,J.K. (2021). Natural variations in SlSOS1 contribute to the loss of salt tolerance during tomato domestication. Plant Biotechnol. J. 19: 20-22.

[237] Wang,Z., Hong,Y., Zhu,G., Li, Y., Niu,Q., Yao,J., Hua,K., Bai,J., Zhu, Y., Shi,H., et al. (2020c). Loss of salt tolerance during tomato domestication conferred by variation in a Na⁺/K⁺ transporter. EMBO J. 39: e103256.

[238] Wei,H., Wang,X., He,Y., Xu, H., and Wang,L. (2021). Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. EMBO J. 40: e105086.

[239] Wei,P., Wang,L., Liu,A., Yu, B., and Lam,H.M. (2016). GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front. Plant Sci. 7: 1082.

[240] Wei,W., Lu,L., Bian,X., Li, Q., Han,J., Tao,J., Yin,C., Lai,Y., Li, W., Bi,Y., et al. (2023). Zinc-finger protein GmZF351 improves both salt and drought stress tolerance in soybean. J. Integr. Plant Biol. 65: 1636-1650.

[241] Wu,F., Chi,Y., Jiang,Z., Xu, Y., Xie,L., Huang,F., Wan,D., Ni,J., Yuan, F., Wu,X., et al. (2020a). Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578: 577-581.

[242] Wu,F., Yang,J., Yu,D., and Xu, P. (2020b). Identification and validation a major QTL from “Sea Rice 86” seedlings conferred salt tolerance. Agronomy 10: 410.

[243] Wu,K., Wang,S.S., Song,W.Z., Zhang, J.Q., Wang,Y., Liu,Q., Yu,J.P., Ye,Y.F., Li, S., Chen,J.F., et al. (2020c). Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367: eaaz2046.

[244] Wu,S.J., Ding,L., and Zhu,J.K. (1996). SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617-627.

[245] Xia,G., and Chen, H. (1996). Plant regeneration from intergeneric somatic hybridization between Triticum aestivum L. and Leymus chinensis (Trin.) Tzvel. Plant Sci. 120: 197-203.

[246] Xiang,Y.H., Yu,J.J., Liao,B., Shan, J.X., Ye,W.W., Dong,N.Q., Guo,T., Kan,Y., Zhang, H., Yang,Y.B., et al. (2022). An α/β hydrolase family member negatively regulates salt tolerance but promotes flowering through three distinct functions in rice. Mol. Plant 15: 1908-1930.

[247] Xiao,S., Song,W., Xing,J., Su, A., Zhao,Y., Li,C., Shi,Z., Li,Z., Wang, S., Zhang,R., et al. (2023). ORF355 confers enhanced salinity stress adaptability to S-type cytoplasmic male sterility maize by modulating the mitochondrial metabolic homeostasis. J. Integr. Plant Biol. 65: 656-673.

[248] Xing,L., Zhu,M., Luan,M., Zhang, M., Jin,L., Liu,Y., Zou,J., Wang,L., and Xu, M. (2022). miR169q and NUCLEAR FACTOR YA8 enhance salt tolerance by activating PEROXIDASE1 expression in response to ROS. Plant Physiol. 188: 608-623.

[249] Xiong,Y., McCormack, M., Li,L., Hall,Q., Xiang,C., and Sheen,J. (2013). Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496: 181-186.

[250] Xu,J., Li,H.D., Chen,L.Q., Wang, Y., Liu,L.L., He,L., and Wu, W.H. (2006). A protein kinase, interacting with two calcineurin B-like proteins, regulates K⁺ transporter AKT1 in Arabidopsis. Cell 125: 1347-1360.

[251] Xu,S.L., Rahman, A., Baskin,T.I., and Kieber,J.J. (2008). Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20: 3065-3079.

[252] Yan,J., Liu,Y., Yan,J., Liu, Z., Lou,H., and Wu,J. (2023). The salt-activated CBF1/CBF2/CBF3-GALS1 module fine-tunes galactan-induced salt hypersensitivity in Arabidopsis. J. Integr. Plant Biol. 65: 1904-1917.

[253] Yan,J., Liu,Y., Yang,L., He, H., Huang,Y., Fang,L., Scheller, H., Jiang,M., and Zhang,A. (2021). Cell wall β-1,4-galactan regulated by the BPC1/BPC2-GALS1 module aggravates salt sensitivity in Arabidopsis thaliana. Mol. Plant 14: 411-425.

[254] Yan,J., and Wang, X. (2023). Machine learning bridges omics sciences and plant breeding. Trends Plant Sci. 28: 199-210.

[255] Yang,C., Ma,B., He,S.J., Xiong, Q., Duan,K.X., Yin,C.C., Chen,H., Lu,X., Chen, S.Y., and Zhang,J.S. (2015). MAOHUZI6/ETHYLENE INSENSITIVE3-LIKE1 and ETHYLENE INSENSITIVE3-LIKE2 regulate ethylene response of roots and coleoptiles and negatively affect salt tolerance in rice. Plant Physiol. 169: 148-165.

[256] Yang,J., Qu,X., Li,T., Gao, Y., Du,H., Zheng,L., Ji,M., Zhang,P., Zhang, Y., Hu,J., et al. (2023a). HY5-HDA9 orchestrates the transcription of HsfA2 to modulate salt stress response in Arabidopsis. J. Integr. Plant Biol. 65: 45-63.

[257] Yang,P., Jin,J., Zhang,J., Wang, D., Bai,X., Xie,W., Hu,T., Zhao,X., Mao, T., and Qin,T. (2022). MDP25 mediates the fine-tuning of microtubule organization in response to salt stress. J. Integr. Plant Biol. 64: 1181-1195.

[258] Yang,Y., and Guo, Y. (2018a). Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol. 217: 523-539.

[259] Yang,Y., and Guo, Y. (2018b). Unraveling salt stress signaling in plants. J. Integr. Plant Biol. 60: 796-804.

[260] Yang,Y., Han,X., Ma,L., Wu, Y., Liu,X., Fu,H., Liu,G., Lei,X., and Guo, Y. (2021). Dynamic changes of phosphatidylinositol and phosphatidylinositol 4-phosphate levels modulate H⁺-ATPase and Na⁺/H⁺ antiporter activities to maintain ion homeostasis in Arabidopsis under salt stress. Mol. Plant 14: 2000-2014.

[261] Yang,Y., Qin,Y., Xie,C., Zhao, F., Zhao,J., Liu,D., Chen,S., Fuglsang,A.T., Palmgren,M.G., Schumaker, K.S., et al. (2010). The Arabidopsis chaperone J3 regulates the plasma membrane H⁺-ATPase through interaction with the PKS5 kinase. Plant Cell 22: 1313-1332.

[262] Yang,Y., Wu,Y., Ma,L., Yang, Z., Dong,Q., Li,Q., Ni,X., Kudla,J., Song, C., and Guo,Y. (2019a). The Ca²⁺ sensor SCaBP3/CBL7 modulates plasma membrane H⁺-ATPase activity and promotes alkali tolerance in Arabidopsis. Plant Cell 31: 1367-1384.

[263] Yang,Y., Zhang,C., Tang,R.J., Xu, H.X., Lan,W.Z., Zhao,F., and Luan, S. (2019b). Calcineurin B-like proteins CBL4 and CBL10 mediate two independent salt tolerance pathways in Arabidopsis. Int. J. Mol. Sci. 20: 2421.

[264] Yang,Z., Cao,Y., Shi,Y., Qin, F., Jiang,C., and Yang,S. (2023b). Genetic and molecular exploration of maize environmental stress resilience: Towards sustainable agriculture. Mol. Plant 16: 1496-1517.

[265] Yang,Z., Wang,C., Xue,Y., Liu, X., Chen,S., Song,C., Yang,Y., and Guo,Y. (2019c). Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat. Commun. 10: 1199.

[266] Yao,H.Y., and Xue, H.W. (2018). Phosphatidic acid plays key roles regulating plant development and stress responses. J. Integr. Plant Biol. 60: 851-863.

[267] Yin,P., Liang,X., Zhao,H., Xu, Z., Chen,L., Yang,X., Qin,F., Zhang,J., and Jiang, C. (2023). Cytokinin signaling promotes salt tolerance by modulating shoot chloride exclusion in maize. Mol. Plant 16: 1031-1047.

[268] Yin,W., Xiao,Y., Niu,M., Meng, W., Li,L., Zhang,X., Liu,D., Zhang,G., Qian, Y., Sun,Z., et al. (2020a). ARGONAUTE2 enhances grain length and salt tolerance by activating BIG GRAIN3 to modulate cytokinin distribution in rice. Plant Cell 32: 2292-2306.

[269] Yin,X., Xia,Y., Xie,Q., Cao, Y., Wang,Z., Hao,G., Song,J., Zhou,Y., and Jiang, X. (2020b). The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance. J. Exp. Bot. 71: 1801-1814.

[270] Yu,B., Zheng,W., Xing,L., Zhu, J.K., Persson,S., and Zhao,Y. (2022). Root twisting drives halotropism via stress-induced microtubule reorientation. Dev. Cell 57: 2412-2425.

[271] Yu,J., Hu,S., Wang,J., Wong, G.K., Li,S., Liu,B., Deng,Y., Dai,L., Zhou, Y., Zhang,X., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79-92.

[272] Yu,J., Zhu,C., Xuan,W., An, H., Tian,Y., Wang,B., Chi,W., Chen,G., Ge, Y., Li,J., et al. (2023). Genome-wide association studies identify OsWRKY53 as a key regulator of salt tolerance in rice. Nat. Commun. 14: 3550.

[273] Yu,L., Nie,J., Cao,C., Jin, Y., Yan,M., Wang,F., Liu,J., Xiao,Y., Liang, Y., and Zhang,W. (2010). Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188: 762-773.

[274] Yu,Z., Duan,X., Luo,L., Dai, S., Ding,Z., and Xia,G. (2020). How plant hormones mediate salt stress responses. Trends Plant Sci. 25: 1117-1130.

[275] Yuan,F., Yang,H., Xue,Y., Kong, D., Ye,R., Li,C., Zhang,J., Theprungsirikul,L., Shrift,T., Krichilsky, B., et al. (2014). OSCA1 mediates osmotic-stress-evoked Ca²⁺ increases vital for osmosensing in Arabidopsis. Nature 514: 367-371.

[276] Zagotta,M.T., Hicks,K.A., Jacobs,C.I., Young, J.C., Hangarter,R.P., and Meeks-Wagner,D.R. (1996). The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 10: 691-702.

[277] Zepeda-Jazo,I., Velarde-Buendía, A.M., Enríquez-Figueroa, R., Bose,J., Shabala,S., Muñiz-Murguía, J., and Pottosin,I.I. (2011). Polyamines interact with hydroxyl radicals in activating Ca²⁺ and K⁺ transport across the root epidermal plasma membranes. Plant Physiol. 157: 2167-2180.

[278] Zhang,D., Jiang,S., Pan,J., Kong, X., Zhou,Y., Liu,Y., and Li, D. (2014a). The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol. 16: 558-570.

[279] Zhang,F., Li,L., Jiao,Z., Chen, Y., Liu,H., Chen,X., Fu,J., Wang,G., and Zheng, J. (2016a). Characterization of the calcineurin B-Like (CBL) gene family in maize and functional analysis of ZmCBL9 under abscisic acid and abiotic stress treatments. Plant Sci. 253: 118-129.

[280] Zhang,G., Zhang,M., Zhao,Z., Ren, Y., Li,Q., and Wang,W. (2017a). Wheat TaPUB1 modulates plant drought stress resistance by improving antioxidant capability. Sci. Rep. 7: 7549.

[281] Zhang,H., Yu,F., Xie,P., Sun, S., Qiao,X., Tang,S., Chen,C., Yang,S., Mei, C., Yang,D., et al. (2023a). A Gγ protein regulates alkaline sensitivity in crops. Science 379: eade8.

[282] Zhang,H., Zhao,F.G., Tang,R.J., Yu, Y., Song,J., Wang,Y., Li,L., and Luan,S. (2017b). Two tonoplast MATE proteins function as turgor-regulating chloride channels in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114: e2036-e2045.

[283] Zhang,H., Zhu,H., Pan,Y., Yu, Y., Luan,S., and Li,L. (2014b). A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol. Plant 7: 1522-1532.

[284] Zhang,K., Xu,X., Wu,R., Shi, J., and Guo,L. (2006). Dought- and salttolerant wheat cultivar. Shanrong No.3 and its cultivation techniques. Shandong Agric. Sci. 2: 86-87.

[285] Zhang,L., Sun,X., Li,Y., Luo, X., Song,S., Chen,Y., Wang,X., Mao,D., Chen, L., and Luan,S. (2021). Rice Na⁺-permeable transporter OsHAK12 mediates shoots Na⁺ exclusion in response to salt stress. Front. Plant Sci. 12: 771746.

[286] Zhang,M., Cao,J., Zhang,T., Xu, T., Yang,L., Li,X., Ji,F., Gao,Y., Ali, S., Zhang,Q., et al. (2022). A putative plasma membrane Na⁺/H⁺ antiporter GmSOS1 is critical for salt stress tolerance in Glycine max. Front. Plant Sci. 13: 870695.

[287] Zhang,M., Cao,Y., Wang,Z., Wang, Z.Q., Shi,J., Liang,X., Song,W., Chen,Q., Lai, J., and Jiang,C. (2018). A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na⁺ exclusion and salt tolerance in maize. New Phytol. 217: 1161-1176.

[288] Zhang,M., Li,Y., Liang,X., Lu, M., Lai,J., Song,W., and Jiang, C. (2023b). A teosinte-derived allele of an HKT1 family sodium transporter improves salt tolerance in maize. Plant Biotechnol. J. 21: 97-108.

[289] Zhang,M., Liang,X., Wang,L., Cao, Y., Song,W., Shi,J., Lai,J., and Jiang,C. (2019a). A HAK family Na⁺ transporter confers natural variation of salt tolerance in maize. Nat. Plants 5: 1297-1308.

[290] Zhang,M., Smith,J.A., Harberd,N.P., and Jiang,C. (2016b). The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol. Biol. 91: 651-659.

[291] Zhang,Q., Lin,F., Mao,T., Nie, J., Yan,M., Yuan,M., and Zhang, W. (2012a). Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24: 4555-4576.

[292] Zhang,S., Sun,L., Dong,X., Lu, S., Tian,W., and Liu,J. (2016). Cellulose synthesis genes CESA6 and CSI1 are important for salt stress tolerance in Arabidopsis. J. Integr. Plant Biol. 58: 623-626.

[293] Zhang,W., Liao,X., Cui,Y., Ma, W., Zhang,X., Du,H., Ma,Y., Ning,L., Wang, H., Huang,F., et al. (2019b). A cation diffusion facilitator, GmCDF1, negatively regulates salt tolerance in soybean. PLoS Genet. 15: e1007798.

[294] Zhang,X., Tang,L., Nie,J., Zhang, C., Han,X., Li,Q., Qin,L., Wang,M., Huang, X., Yu,F., et al. (2023c). Structure and activation mechanism of the rice Salt Overly Sensitive 1 (SOS1) Na⁺/H⁺ antiporter. Nat. Plants 9: 1924-1936.

[295] Zhang,Y., Tan,J., Guo,Z., Lu, S., He,S., Shu,W., and Zhou, B. (2009). Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis-epoxycarotenoid dioxygenase influence H₂O₂ and NO production and antioxidant defences. Plant Cell Environ. 32: 509-519.

[296] Zhang,Y., Zhou,J., Ni,X., Wang, Q., Jia,Y., Xu,X., Wu,H., Fu,P., Wen, H., Guo,Y., et al. (2023d). Structural basis for the activity regulation of Salt Overly Sensitive 1 in Arabidopsis salt tolerance. Nat. Plants 9: 1915-1923.

[297] Zhang,Z., Wang,J., Zhang,R., and Huang, R. (2012b). The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J. 71: 273-287.

[298] Zhao,C., Jiang,W., Zayed,O., Liu, X., Tang,K., Nie,W., Li,Y., Xie,S., Li, Y., Long,T., et al. (2020a). The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones. Natl. Sci. Rev. 8: nwaa149.

[299] Zhao,C., Zayed,O., Yu,Z., Jiang, W., Zhu,P., Hsu,C.C., Zhang,L., Tao,W.A., Lozano-Durán, R., and Zhu,J.K. (2018). Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 115: 13123-13128.

[300] Zhao,C., Zhang,H., Song,C., Zhu, J.K., and Shabala,S. (2020b). Mechanisms of plant responses and adaptation to soil salinity. Innovation 1: 100017.

[301] Zhao,X., Zhang,T., Bai,L., Zhao, S., Guo,Y., and Li,Z. (2023). CKL2 mediates the crosstalk between abscisic acid and brassinosteroid signaling to promote swift growth recovery after stress in Arabidopsis. J. Integr. Plant Biol. 65: 64-81.

[302] Zhao,Y., Wang,T., Zhang,W., and Li, X. (2011). SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol. 189: 1122-1134.

[303] Zhou,H., Lin,H., Chen,S., Becker, K., Yang,Y., Zhao,J., Kudla,J., Schumaker,K.S., and Guo,Y. (2014). Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26: 1166-1182.

[304] Zhou,H., Xiao,F., Zheng,Y., Liu, G., Zhuang,Y., Wang,Z., Zhang,Y., He,J., Fu, C., and Lin,H. (2022a). PAMP-INDUCED SECRETED PEPTIDE 3 modulates salt tolerance through RECEPTOR-LIKE KINASE 7 in plants. Plant Cell 34: 927-944.

[305] Zhou,X., Li,J., Wang,Y., Liang, X., Zhang,M., Lu,M., Guo,Y., Qin,F., and Jiang, C. (2022b). The classical SOS pathway confers natural variation of salt tolerance in maize. New Phytol. 236: 479-494.

[306] Zhou,Y.B., Liu,C., Tang,D.Y., Yan, L., Wang,D., Yang,Y.Z., Gui,J.S., Zhao,X.Y., Li, L.G., Tang,X.D., et al. (2018). The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H₂O₂ homeostasis and improving salt tolerance in rice. Plant Cell 30: 1100-1118.

[307] Zhou,Z., Jiang,Y., Wang,Z., Gou, Z., Lyu,J., Li,W., Yu,Y., Shu,L., Zhao, Y., Ma,Y., et al. (2015). Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat. Biotechnol. 33: 408-414.

[308] Zhu,J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53: 247-273.

[309] Zhu,J.K. (2016). Abiotic stress signaling and responses in plants. Cell 167: 313-324.

RIGHTS & PERMISSIONS

2023 Institute of Botany, Chinese Academy of Sciences.