1932

Abstract

Salt stress reduces land and water productivity and contributes to poverty and food insecurity. Increased salinization caused by human practices and climate change is progressively reducing agriculture productivity despite escalating calls for more food. Plant responses to salt stress are well understood, involving numerous critical processes that are each controlled by multiple genes. Knowledge of the critical mechanisms controlling salt uptake and exclusion from functioning tissues, signaling of salt stress, and the arsenal of protective metabolites is advancing. However, little progress has been made in developing salt-tolerant varieties of crop species using standard (but slow) breeding approaches. The genetic diversity available within cultivated crops and their wild relatives provides rich sources for trait and gene discovery that has yet to be sufficiently utilized. Transforming this knowledge into modern approaches using genomics and molecular tools for precision breeding will accelerate the development of tolerant cultivars and help sustain food production.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042916-040936
2017-04-28
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/arplant/68/1/annurev-arplant-042916-040936.html?itemId=/content/journals/10.1146/annurev-arplant-042916-040936&mimeType=html&fmt=ahah

Literature Cited

  1. Amtmann A, Sanders D. 1.  1999. Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res. 29:75–112 [Google Scholar]
  2. Apse MP, Aharon GS, Snedden WA, Blumwald E. 2.  1999. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–58 [Google Scholar]
  3. Apse MP, Sottosanto JB, Blumwald E. 3.  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. 36:229–39 [Google Scholar]
  4. Ashraf M, Foolad MR. 4.  2013. Crop breeding for salt tolerance in the era of molecular marker-assisted selection. Plant Breed 132:10–20 [Google Scholar]
  5. Atwell B, Wang H, Scafaro AP. 5.  2014. Could abiotic stress tolerance in wild relatives of rice be used to improve Oryza sativa?. Plant Sci 215:48–58 [Google Scholar]
  6. Awlia M, Nigro A, Fajkus J, Schmoeckel SM, Negrão S. 6.  et al. 2016. High-throughput non-destructive phenotyping of traits that contribute to salinity tolerance in Arabidopsis thaliana. Front. Plant Sci. 7:1414 [Google Scholar]
  7. Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A. 7.  et al. 2012. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–42 [Google Scholar]
  8. Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z. 8.  et al. 2011. The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224–39 [Google Scholar]
  9. Bassil E, Tajima H, Liang YC, Ohto MA, Ushijima K. 9.  et al. 2011. The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23:3482–97 [Google Scholar]
  10. Baxter A, Mittler R, Suzuki N. 10.  2014. ROS as key players in plant stress signaling. J. Exp. Bot. 65:1229–40 [Google Scholar]
  11. Begum H, Spindel JE, Lalusin A, Borromeo T, Gregorio G. 11.  et al. 2015. Genome wide association mapping for yield and other agronomic traits in an elite breeding population of tropical rice (Oryza sativa). PLOS ONE 10:e0119873 [Google Scholar]
  12. Berthomieu P, Conéjéro G, Nublat A, Brackenbury WJ, Lambert C. 12.  et al. 2003. Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 22:2004–14 [Google Scholar]
  13. Bimpong IK, Manneh B, Sock M, Diaw F, Amoah NKA. 13.  et al. 2016. Improving salt tolerance of lowland rice cultivar “Rassi” through marker-aided backcross breeding in West Africa. Plant Sci 242:288–99 [Google Scholar]
  14. Blumwald E, Aharon GS, Apse MP. 14.  2000. Sodium transport in plant cells. Biochim. Biophys. Acta 1465:140–51 [Google Scholar]
  15. Boscari A, Clément M, Volkov V, Colldack D, Hybiak J. 15.  et al. 2009. Potassium channels in barley: cloning, functional characterization and expression analyses in relation to leaf growth and development. Plant Cell Environ 32:1761–77 [Google Scholar]
  16. Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES. 16.  et al. 2007. HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol. 143:1918–28 [Google Scholar]
  17. Byrt CS, Xu B, Krishnan M, Lightfoot DJ, Athman A. 17.  et al. 2014. The Na+ transporter, TaHKT1;5-D, limits shoot Na+ accumulation in bread wheat. Plant J 80:516–26 [Google Scholar]
  18. Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW. 18.  et al. 2017. Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ In press. https://doi.org/10.1111/pce.12832 [Google Scholar]
  19. Campbell MT, Knecht AC, Berger B, Brien CJ, Wang D, Walia H. 19.  2015. Integrating image-based phenomics and association analysis to dissect the genetic architecture of temporal salinity responses in rice. Plant Physiol 168:1476–89 [Google Scholar]
  20. Chen G, Hu Q, Luo L, Yang T, Zhang S. 20.  et al. 2015. Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell Environ 38:2747–65 [Google Scholar]
  21. Chen H, He H, Zou Y, Chen W, Yu R. 21.  et al. 2011. Development and application of a set of breeder-friendly SNP markers for genetic analyses and molecular breeding of rice (Oryza sativa L.). Theor. Appl. Genet. 123:869–79 [Google Scholar]
  22. Chen ZC, Yamaji N, Fujii-Kashino M, Ma JF. 22.  2016. A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice. Plant Physiol 171:494–507 [Google Scholar]
  23. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi HZ. 23.  2008. Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J. 53:554–65 [Google Scholar]
  24. Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ. 24.  et al. 2007. Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278–92 [Google Scholar]
  25. Colmer TD, Flowers TJ, Munns R. 25.  2006. Use of wild relatives to improve salt tolerance in wheat. J. Exp. Bot. 57:1059–78 [Google Scholar]
  26. Colmer TD, Munns R, Flowers TJ. 26.  2005. Improving salt tolerance of wheat and barley: future prospects. Aust. J. Exp. Agric. 45:1425–43 [Google Scholar]
  27. Coskun D, Dev T, Britto DT, Jean Y-K, Kabir I. 27.  et al. 2013. K+ efflux and retention in response to NaCl stress do not predict salt tolerance in contrasting genotypes of rice (Oryza sativa L.). PLOS ONE 8:e57767 [Google Scholar]
  28. Cotsaftis O, Plett D, Shirley N, Tester M, Hrmova M. 28.  2012. A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLOS ONE 7:e39865 [Google Scholar]
  29. Cuin TA, Bose J, Stefano G, Jha D, Tester M. 29.  et al. 2011. Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–61 [Google Scholar]
  30. Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M. 30.  2007. The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ. 30:497–507 [Google Scholar]
  31. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI. 31.  2014. Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–79 [Google Scholar]
  32. Demidchik V.32.  2014. Mechanisms and physiological roles of K+ efflux from root cells. J. Plant Physiol. 171:696–707 [Google Scholar]
  33. Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA. 33.  et al. 2002. Arabidopsis thaliana root nonselective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808 [Google Scholar]
  34. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ. 34.  et al. 2010. Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J. Cell Sci. 123:1468–79 [Google Scholar]
  35. Demidchik V, Maathuis FJM. 35.  2007. Physiological roles of nonselective cation channels in plants: from salt stress to signaling and development. New Phytol 175:387–404 [Google Scholar]
  36. Demidchik V, Tester MA. 36.  2002. Sodium fluxes through nonselective cation channels in the plant plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol 128:379–87 [Google Scholar]
  37. Dubcovsky J, Maria SG, Epstein E, Luo MC, Dvořák J. 37.  1996. Mapping of the K+/Na+ discrimination locus Kna1 in wheat. Theor. Appl. Genet. 2:448–54 [Google Scholar]
  38. Essah PA, Davenport R, Tester M. 38.  2003. Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–18 [Google Scholar]
  39. Feki K, Quintero FJ, Khoudi H, Leidi EO, Masmoudi K. 39.  et al. 2014. A constitutively active form of a durum wheat Na+/H+ antiporter SOS1 confers high salt tolerance to transgenic Arabidopsis. Plant Cell Rep. 33:277–88 [Google Scholar]
  40. Feki K, Quintero FJ, Pardo JM, Masmoudi K. 40.  2011. Regulation of durum wheat Na+/H+ exchanger TdSOS1 by phosphorylation. Plant Mol. Biol. 76:545–56 [Google Scholar]
  41. Flowers TJ, Colmer TD. 41.  2008. Salinity tolerance in halophytes. New Phytol 179:945–63 [Google Scholar]
  42. Flowers TJ, Flowers SA, Hajibagheri MA, Yeo AR. 42.  1990. Salt tolerance in the halophytic wild rice, Porteresia Coarctata Tateoka. New Phytol 114:675–84 [Google Scholar]
  43. Flowers TJ, Yeo AR. 43.  1981. Variability in the resistance of sodium chloride salinity within rice (Oryza sativa L.) varieties. New Phytol 88:363–73 [Google Scholar]
  44. Foolad MR.44.  2004. Recent advances in genetics of salt tolerance in tomato. Plant Cell Tissue Organ Cult 76:101–19 [Google Scholar]
  45. Francois LE, Maas EV, Donovan TJ, Youngs VL. 45.  1986. Effect of salinity on grain yield and quality, vegetative growth, and germination of semi-dwarf and durum wheat. Agron. J. 78:1053–58 [Google Scholar]
  46. Ganal MW, Altmann T, Röder MS. 46.  2009. SNP identification in crop plants. Curr. Opin. Plant Biol. 12:211–17 [Google Scholar]
  47. Gao J, Sun J, Cao P, Ren L, Liu C. 47.  et al. 2016. Variation in tissue Na+ content and the activity of SOS1 genes among two species and two related genera of Chrysanthemum. BMC Plant Biol. 16:98 [Google Scholar]
  48. Garg R, Verma M, Agrawal S, Shankar R, Majee M, Jain M. 48.  2013. Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors. DNA Res 21:69–84 [Google Scholar]
  49. Gaxiola RA, Sanchez CA, Paez-Valencia J, Ayre BG, Elser JJ. 49.  2012. Genetic manipulation of a “vacuolar” H+-PPase: from salt tolerance to yield enhancement under phosphorus-deficient soils. Plant Physiol 159:3–11 [Google Scholar]
  50. Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D. 50.  et al. 1998. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–55 [Google Scholar]
  51. Gong H, Blackmore D, Clingeleffer P, Sykes S, Jha D. 51.  et al. 2011. Contrast in chloride exclusion between two grapevine genotypes and its variation in their hybrid progeny. J. Exp. Bot. 62:989–99 [Google Scholar]
  52. Gorham J.52.  1990. Salt tolerance in the Triticeae: K/Na discrimination in synthetic hexaploid wheat. J. Exp. Bot. 41:623–27 [Google Scholar]
  53. Grattan SR, Zeng L, Shannon MC, Roberts SR. 53.  2002. Rice is more sensitive to salinity than previously thought. Calif. Agric. 56:189–95 [Google Scholar]
  54. Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ. 54.  2002. Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Res 76:91–101 [Google Scholar]
  55. Guan R, Qu Y, Guo Y, Yu L, Liu Y. 55.  et al. 2014. Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J. 80:937–50 [Google Scholar]
  56. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. 56.  2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:463–99 [Google Scholar]
  57. Hauser F, Horie T. 57.  2010. A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–65 [Google Scholar]
  58. He Y, Fu J, Yu C, Wang X, Jiang Q. 58.  et al. 2015. Increasing cyclic electron flow is related to Na+ sequestration into vacuoles for salt tolerance in soybean. J. Exp. Bot. 66:6877–89 [Google Scholar]
  59. Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR. 59.  et al. 2015. Grapevine and Arabidopsis cation-chloride cotransporters localize to the Golgi and trans-Golgi network and indirectly influence long-distance ion transport and plant salt tolerance. Plant Physiol 169:2215–29 [Google Scholar]
  60. Horie T, Hauser F, Schroeder JI. 60.  2009. HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–68 [Google Scholar]
  61. Hossain H, Rahman MA, Alam MS, Singh RK. 61.  2015. Mapping of quantitative trait loci associated with reproductive-stage salt tolerance in rice. J. Agron. Crop Sci. 201:17–31 [Google Scholar]
  62. Hou C, Tian W, Kleist T, He K, Garcia V. 62.  et al. 2014. DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res 24:632–35 [Google Scholar]
  63. Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD. 63.  et al. 2006. A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142:1718–27 [Google Scholar]
  64. Huang X, Wei X, Sang T, Zhao Q, Feng Q. 64.  et al. 2010. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42:961–67 [Google Scholar]
  65. Huertas R, Rubio L, Cagnac O, García-Sánchez MJ, Alché JD. 65.  et al. 2013. The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato. Plant Cell Environ 36:2135–49 [Google Scholar]
  66. Islam MR, Salam MA, Bhuiyan MAR, Rahman MA, Yasmeen R. 66.  et al. 2008. BRRI Dhan 47: a salt tolerant rice variety for Boro season isolated through participatory variety selection. Int. J. BioRes. 5:1–6 [Google Scholar]
  67. Islam MR, Sarker MRA, Sharma N, Rahman MA, Collard BCY. 67.  et al. 2015. Assessment of adaptability of recently released salt tolerant rice varieties in coastal regions of South Bangladesh. Field Crops. Res. 190:34–43 [Google Scholar]
  68. Ismail AM, Heuer S, Thomson MJ, Wissuwa M. 68.  2007. Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol. Biol. 65:547–70 [Google Scholar]
  69. Ismail AM, Tuong TP. 69.  2009. Brackish water coastal zones of the monsoon tropics: challenges and opportunities. Natural Resource Management for Poverty Reduction and Environmental Sustainability in Fragile Rice-Based Systems. SM Haefele, AM Ismail 113–21 Los Baños, Philipp.: Int. Rice Res. Inst.
  70. Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL. 70.  et al. 2009. Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955–71 [Google Scholar]
  71. James RA, Blake C, Byrt CS, Munns R. 71.  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. 62:2939–47 [Google Scholar]
  72. James RA, Davenport RJ, Munns R. 72.  2006. Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol. 142:1537–47 [Google Scholar]
  73. Jaradat AA, Shahid M, Al-Maskri A. 73.  2004. Genetic diversity in the Batini barley landrace from Oman: II. Response to salinity stress. Crop Sci 44:997–1007 [Google Scholar]
  74. Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J. 74.  et al. 2012. ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31:4359–70 [Google Scholar]
  75. Khan MS, Ahmad D, Khan MA. 75.  2015. Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnol. Biotechnol. Equip. 29:815–25 [Google Scholar]
  76. Khatodia S, Bhatotia K, Passricha N, Khurana SM, Tuteja N. 76.  2016. The CRISPR/Cas genome-editing tool: application in improvement of crops. Front. Plant Sci. 7:506 [Google Scholar]
  77. Leidi EO, Barraga V, Rubio L, El-Hamdaoui A, Ruiz MT. 77.  et al. 2010. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J 61:495–506 [Google Scholar]
  78. Li B, Byrt C, Qiu J, Baumann U, Hrmova M. 78.  et al. 2016. Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiol 170:1014–29 [Google Scholar]
  79. Lindsay MP, Lagudah ES, Hare RA, Munns R. 79.  2004. A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct. Plant Biol. 31:1105–14 [Google Scholar]
  80. Linh LH, Linh TH, Xuan TD, Ham LH, Ismail AM, Khanh TD. 80.  2012. Molecular breeding to improve salt tolerance of rice (Oryza sativa L.) in the Red River Delta of Vietnam. Int. J. Plant Genom. 2012:949038 [Google Scholar]
  81. Ma L, Zhang H, Sun L, Jiao Y, Zhang G. 81.  et al. 2012. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J. Exp. Bot. 63:305–17 [Google Scholar]
  82. Maas EV, Hoffman GJ. 82.  1977. Crop salt tolerance: evaluation of existing data. Managing Water for Irrigation: Proceedings of the International Salinity Conference HE Dregne 187–98 Lubbock: Tex. Tech. Univ. [Google Scholar]
  83. Maathuis FJM, Sanders D. 83.  2001. Sodium uptake in Arabidopsis thaliana roots is regulated by cyclic nucleotides. Plant Physiol 127:1617–25 [Google Scholar]
  84. Mano Y, Takeda K. 84.  1997. Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–72 [Google Scholar]
  85. Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu J-K. 85.  et al. 2007. Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–12 [Google Scholar]
  86. Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ. 86.  et al. 2002. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett. 531:157–61 [Google Scholar]
  87. Mason MG, Jha D, Salt DE, Tester M, Hill K. 87.  et al. 2010. Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots. Plant J 64:753–63 [Google Scholar]
  88. Meyer R, Choi JY, Sanches M, Plessis A, Flowers JM. 88.  et al. 2016. Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat. Genet. 48:1083–88 [Google Scholar]
  89. Mian A, Oomen RJFJ, Isayenkov S, Sentenac H, Maathuis FJM, Véry A-A. 89.  2011. Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–79 [Google Scholar]
  90. Michard E, Lima PT, Borges F, Silva AC, Portes MT. 90.  et al. 2011. Glutamate receptor–like genes form Ca2+ channels in pollen tubes and are regulated by pistil d-serine. Science 332:434–37 [Google Scholar]
  91. Mishra S, Singh B, Misra P, Rai V, Singh NK. 91.  2016. Haplotype distribution and association of candidate genes with salt tolerance in Indian wild rice germplasm. Plant Cell Rep 35:2295 [Google Scholar]
  92. Mishra S, Singh B, Panda K, Singh P, Singh N. 92.  et al. 2016. Association of SNP haplotypes of HKT family genes with salt tolerance in Indian wild rice germplasm. Rice 9:15 [Google Scholar]
  93. Mizrahi Y, Pasternak D. 93.  1985. Effect of salinity on quality of various agricultural crops. Plant Soil 89:301–7 [Google Scholar]
  94. Mohammadi R, Mendioro MS, Diaz GQ, Gregorio GB, Singh RK. 94.  2014. Genetic analyses of salt tolerance at seedling and reproductive stages in rice. Plant Breed 133:548–59 [Google Scholar]
  95. Møller IS, Gilliham M, Deepa J, Mayo GM, Roy SJ. 95.  et al. 2009. Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–78 [Google Scholar]
  96. Moradi F, Ismail AM. 96.  2007. Responses of photosynthesis, chlorophyll fluorescence and ROS scavenging system to salt stress during seedling and reproductive stages in rice. Ann. Bot. 99:1161–73 [Google Scholar]
  97. Moradi F, Ismail AM, Gregorio G, Egdane J. 97.  2003. Salinity tolerance of rice during reproductive development and association with tolerance at seedling stage. Ind. J. Plant Physiol. 8:105–16 [Google Scholar]
  98. Munns R, Gilliham M. 98.  2015. Salinity tolerance of crops—what is the cost?. New Phytol 208:668–73 [Google Scholar]
  99. Munns R, James RA, Läuchli A. 99.  2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57:1025–43 [Google Scholar]
  100. Munns R, James RA, Xu B, Athman A, Conn SJ. 100.  et al. 2012. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat. Biotechnol. 30:360–64 [Google Scholar]
  101. Munns R, Tester M. 101.  2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59:651–81 [Google Scholar]
  102. Negrão S, Courtois B, Ahmadi N, Abreu I, Saibo N, Oliveira MM. 102.  2011. Recent updates on salinity stress in rice: from physiological to molecular responses. Crit. Rev. Plant Sci. 30:329–77 [Google Scholar]
  103. Nutan KK, Kushwaha HR, Singla-Pareek SL, Pareek A. 103.  2017. Transcription dynamics of Saltol QTL localized genes encoding transcription factors, reveals their differential regulation in contrasting genotypes of rice. Funct. Integr. Genom. 17:69 [Google Scholar]
  104. Olías R, Eljakaoui Z, Li J, De Morales PA, Marín-Manzano MC. 104.  et al. 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 Environ 32:904–16 [Google Scholar]
  105. Panda BB, Badoghar AK, Sekhar S, Kariali E, Mohapatra PK, Shaw PB. 105.  2016. Biochemical and molecular characterization of salt-induced poor grain filling in a rice cultivar. Funct. Plant Biol. 43:266–77 [Google Scholar]
  106. Pardo JM, Cubero B, Leidi EO, Quintero FJ. 106.  2006. Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J. Exp. Bot. 57:1181–99 [Google Scholar]
  107. Platten JD, Egdane J, Ismail AM. 107.  2013. Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism?. BMC Plant Biol 13:32 [Google Scholar]
  108. Poland JA, Rife TW. 108.  2012. Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102 [Google Scholar]
  109. Qiu J, Henderson SW, Tester M, Roy SJ, Gilliham M. 109.  2016. SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl accumulation and salt tolerance in Arabidopsis thaliana. J. Exp. Bot. 67:4495–505 [Google Scholar]
  110. Rahman MA, Thomson MJ, Shah-E-Alam M, de Ocampo M, Egdane J, Ismail AM. 110.  2016. Exploring novel genetic sources of salinity tolerance in rice through molecular and physiological characterization. Ann. Bot. 117:1083–97 [Google Scholar]
  111. Rains DW, Epstein E. 111.  1967. Sodium absorption by barley roots: its mediation by mechanism 2 of alkali cation transport. Plant Physiol 42:319–23 [Google Scholar]
  112. Rao PS, Mishra B, Gupta SR. 112.  2013. Effects of soil salinity and alkalinity on grain quality of tolerant, semi-tolerant and sensitive rice genotypes. Rice Sci 20:284–91 [Google Scholar]
  113. Reguera M, Bassil E, Tajima H, Wimmer M, Chanoca A. 113.  et al. 2015. pH regulation by NHX-type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. Plant Cell 27:1200–17 [Google Scholar]
  114. Ren ZH, Gao JP, Li LG, Cai XL, Huang W. 114.  et al. 2005. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat. Genet. 37:1141–46 [Google Scholar]
  115. Rick CM, Chetelat RT. 115.  1995. Utilization of related wild species for tomato improvement. Acta Hortic 412:21–38 [Google Scholar]
  116. Rodríguez-Rosales MP, Galvez FJ, Huertas R, Aranda MN, Baghour M. 116.  et al. 2009. Plant NHX cation/proton antiporters. Plant Signal. Behav. 4:265–76 [Google Scholar]
  117. Roy SJ, Huang W, Wang XJ, Evrard A, Schmoeckel SM. 117.  et al. 2013. A novel protein kinase involved in Na+ exclusion revealed from positional cloning. Plant Cell Environ 36:553–68 [Google Scholar]
  118. Rubio F, Gassmann W, Schroeder JI. 118.  1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–63 [Google Scholar]
  119. Sako K, Kim JM, Matsui A, Nakamura K, Tanaka M. 119.  et al. 2016. Ky-2, a histone deacetylase inhibitor, enhances high-salinity stress tolerance in Arabidopsis thaliana. Plant Cell Physiol. 57:776–83 [Google Scholar]
  120. Salehi M, Arzani A. 120.  2013. Grain quality traits in triticale influenced by field salinity stress. Aust. J. Crop Sci. 7:580–87 [Google Scholar]
  121. Saranga Y, Cahaner A, Zamir D, Marani A, Rudich J. 121.  1992. Breeding tomatoes for salt tolerance: inheritance of salt tolerance and related traits in interspecific populations. Theor. Appl. Genet. 84:390–96 [Google Scholar]
  122. Sayed HI.122.  1985. Diversity of salt tolerance in a germplasm collection of wheat (Triticum spp.). Theor. Appl. Genet. 69:651–57 [Google Scholar]
  123. Sbei H, Sato K, Shehzad T, Harrabi M, Okuno K. 123.  2014. Detection of QTLs for salt tolerance in Asian barley (Hordeum vulgare L.). Breed. Sci 64378–88 [Google Scholar]
  124. Schachtman DP, Schroeder JI. 124.  1994. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–58 [Google Scholar]
  125. Shabala S.125.  2013. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot. 112:1209–21 [Google Scholar]
  126. Shabala S, Bose J, Hedrich R. 126.  2014. Salt bladders: Do they matter?. Trends Plant Sci 19:687–91 [Google Scholar]
  127. Shabala S, Cuin TA. 127.  2008. Potassium transport and plant salt tolerance. Physiol. Plant. 133:651–69 [Google Scholar]
  128. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ. 128.  et al. 2006. Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–65 [Google Scholar]
  129. Shahbaz M, Ashraf M. 129.  2013. Improving salinity tolerance in cereals. Crit. Rev. Plant Sci. 32:237–49 [Google Scholar]
  130. Shi HZ, Quintero FJ, Pardo JM, Zhu JK. 130.  2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–77 [Google Scholar]
  131. Singh YP, Mishra VK, Singh S, Sharma DK, Singh D. 131.  et al. 2016. Productivity of sodic soils can be enhanced through the use of salt tolerant rice varieties and proper agronomic practices. Field Crops Res 190:82–90 [Google Scholar]
  132. Smajgle A, Toan TQ, Nhan DK, Ward J, Trung NH. 132.  et al. 2015. Responding to rising sea levels in the Mekong Delta. Nat. Clim. Change 5:167–74 [Google Scholar]
  133. Sun J, Li LS, Liu MQ, Wang MJ, Ding MQ. 133.  et al. 2010. Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–15 [Google Scholar]
  134. Sunarpi Horie T, Motoda J, Kubo M, Yang H. 134.  et al. 2005. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–38 [Google Scholar]
  135. Surekha R, Mishra B, Gupta SR, Rathore A. 135.  2008. Reproductive stage tolerance to salinity and alkalinity stresses in rice genotypes. Plant Breed 127:256–61 [Google Scholar]
  136. Suzuki K, Yamaji M, Costa A, Okuma E, Kobayashi NI. 136.  et al. 2016. OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol 16:22 [Google Scholar]
  137. Takagi H, Tamiru M, Abe A, Yoshida K, Uemura A. 137.  et al. 2015. MutMap accelerates breeding of salt-tolerant rice cultivar. Nat. Biotechnol. 33:445–49 [Google Scholar]
  138. Tapken D, Anschütz U, Liu L-H, Huelsken T, Seebohm G. 138.  et al. 2013. A plant homolog of animal glutamate receptors is an ion channel gated by multiple hydrophobic amino acids. Sci. Signal. 6:ra47 [Google Scholar]
  139. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK. 139.  2011. Additive effects of Na+ and Cl ions on barley growth under salinity stress. J. Exp. Bot. 62:2189–203 [Google Scholar]
  140. Teakle NL, Tyerman SD. 140.  2010. Mechanisms of Cl transport contributing to salt tolerance. Plant Cell Environ 33:566–89 [Google Scholar]
  141. Thomson MJ, de Ocampo M, Egdane J, Rahman MR, Sajise AG. 141.  et al. 2010. Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3:148–60 [Google Scholar]
  142. Thomson MJ, Ismail AM, McCouch SR, Mackill MJ. 142.  2010. Marker assisted breeding. Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation A Pareek, SK Sopory, HJ Bohnert, Govindjee 451–69 Dordrecht, Neth.: Springer [Google Scholar]
  143. Thomson MJ, Zhao K, Wright M, McNally K, Rey J. 143.  et al. 2012. High-throughput single nucleotide polymorphism genotyping for breeding applications in rice using the BeadXpress platform. Mol. Breed. 29:875–86 [Google Scholar]
  144. Tiwari S, Krishnamurthy SL, Kumar V, Singh B, Rao AR. 144.  et al. 2016. Mapping QTLs for salt tolerance in rice (Oryza sativa L.) by bulk segregant analysis of recombinant inbred lines using SNP chip. PLOS ONE 11:e0153610 [Google Scholar]
  145. 145. Tomato Genome Consort 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–41 [Google Scholar]
  146. Tounsi S, Amar SB, Masmoudi K, Sentenac H, Brini F, Véry A-A. 146.  2016. Characterization of two HKT1;4 transporters from Triticum monococcum to elucidate the determinants of the wheat salt tolerance Nax1 QTL. Plant Cell Physiol. 57:2047–57 [Google Scholar]
  147. Tripathy BC, Oelmüller R. 147.  2012. Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7:1621–33 [Google Scholar]
  148. Tyerman SD, Skerrett M, Garrill A, Findlay GP, Leigh RA. 148.  1997. Pathways for the permeation of Na+ and Cl into protoplasts derived from the cortex of wheat roots. J. Exp. Bot. 48:459–80 [Google Scholar]
  149. Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S. 149.  et al. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol. 1221249–59
  150. Venema K, Quintero FJ, Pardo JM, Donaire JP. 150.  2002. The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J. Biol. Chem. 277:2413–18 [Google Scholar]
  151. Véry A-A, Sentenac H. 151.  2003. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54:575–603 [Google Scholar]
  152. Vincill ED, Bieck AM, Spalding EP. 152.  2012. Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159:40–46 [Google Scholar]
  153. Walia H, Wilson C, Condamine P, Liu X, Ismail AM. 153.  et al. 2005. Comparative transcriptional profiling of two contrasting rice (Oryza sativa L.) genotypes under salinity stress during vegetative growth stage. Plant Physiol 139:822–35 [Google Scholar]
  154. Wang R, Jing W, Xiao L, Jin Y, Shen L, Zhang W. 154.  2015. The rice High-Affinity Potassium Transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor. Plant Physiol 168:1076–90 [Google Scholar]
  155. Wang S, Su SZ, Wu Y, Li SP, Shan XH. 155.  et al. 2015. Overexpression of maize chloride channel gene ZmCLC-d in Arabidopsis thaliana improved its stress resistance. Biol. Plant. 59:55–64 [Google Scholar]
  156. Wei P, Wang L, Liu A, Yu B, Lam HM. 156.  2016. GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front. Plant Sci. 7:1082 [Google Scholar]
  157. Wei Q, Liu Y, Zhou G, Li Q, Yang C, Peng SA. 157.  2013. Overexpression of CsCLCc, a chloride channel gene from Poncirus trifoliata, enhances salt tolerance in Arabidopsis. Plant Mol. Biol. Rep. 31:1548–57 [Google Scholar]
  158. Wing RA, Ammiraju JSS, Luo M, Kim H, Yu Y. 158.  et al. 2005. The Oryza Map Alignment Project: the golden path to unlocking the genetic potential of wild rice species. Plant Mol. Biol. 59:56–62 [Google Scholar]
  159. Wong TH, Li MW, Yao XQ, Lam HM. 159.  2013. The GmCLC1 protein from soybean functions as a chloride ion transporter. J. Plant Physiol. 170:101–4 [Google Scholar]
  160. Wu H, Shabala L, Liu X, Azzarello E, Zhou M. 160.  et al. 2015. Linking salinity stress tolerance with tissue-specific Na+ sequestration in wheat roots. Front. Plant Sci. 6:71 [Google Scholar]
  161. Wu H, Shabala L, Zhou M, Shabala S. 161.  2014. Durum and bread wheat differ in their ability to retain potassium in leaf mesophyll: implications for salinity stress tolerance. Plant Cell Physiol 55:1749–62 [Google Scholar]
  162. Wu H, Zhu M, Shabala L, Zhou M, Shabala S. 162.  2015. K+ retention in leaf mesophyll, an overlooked component of salinity tolerance mechanism: a case study for barley. J. Integr. Plant Biol. 57:171–85 [Google Scholar]
  163. Xu HX, Jiang XY, Zhan KH, Cheng XY, Chen XJ. 163.  et al. 2008. Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Arch. Biochem. Biophys. 473:8–15 [Google Scholar]
  164. Xu Y, Zhou Y, Hong S, Xia Z, Cui D. 164.  et al. 2013. Functional characterization of a wheat NHX antiporter gene TaNHX2 that encodes a K+/H+ exchanger. PLOS ONE 8:e78098 [Google Scholar]
  165. Yamaguchi E, Blumwald E. 165.  2005. Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–20 [Google Scholar]
  166. Yang T, Zhang S, Hu Y, Wu F, Hu Q. 166.  et al. 2014. The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166:945–59 [Google Scholar]
  167. Yang Y, Yan CQ, Cao BH, Xu HX, Chen JP, Jiang DA. 167.  2007. Some photosynthetic responses to salinity resistance are transferred into the somatic hybrid descendants from the wild soybean Glycine cyrtoloba ACC547. Physiol. Plant. 129:658–69 [Google Scholar]
  168. Yeo AR, Flowers TJ. 168.  1986. Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Aust. J. Plant Physiol. 13:161–73 [Google Scholar]
  169. Yuan F, Yang H, Xue Y, Kong D, Ye R. 169.  et al. 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–71 [Google Scholar]
  170. Yuan HJ, Ma Q, Wu GQ, Wang P, Hu J, Wang SM. 170.  2015. ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Ann. Bot. 115:495–507 [Google Scholar]
  171. Zhang F, Wang YP, Yang YL, Wu H, Wang D, Liu JQ. 171.  2007. Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ. 30:775–85 [Google Scholar]
  172. Zhang YM, Zhang HM, Liu ZH, Li HC, Guo XL, Li GL. 172.  2015. The wheat NHX antiporter gene TaNHX2 confers salt tolerance in transgenic alfalfa by increasing the retention capacity of intracellular potassium. Plant Mol. Biol. 87:317–27 [Google Scholar]
  173. Zhou G, Johnson P, Ryan PR, Delhaize E, Zhou M. 173.  2012. Quantitative trait loci for salinity tolerance in barley (Hordeum vulgare L.). Mol. Breed. 29:427–36 [Google Scholar]
  174. Zhu JK, Liu JP, Xiong LM. 174.  1998. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–91 [Google Scholar]
  175. Zhu M, Shabala L, Cuin TA, Huang X, Zhou M. 175.  et al. 2016. Nax loci affect SOS1-like Na+/H+ exchanger expression and activity in wheat. J. Exp. Bot. 67:835–44 [Google Scholar]
  176. Zhu M, Zhou MX, Shabala L, Shabala S. 176.  2015. Linking osmotic adjustment and stomatal characteristics with salinity stress tolerance in contrasting barley accessions. Funct. Plant Biol. 42:252–63 [Google Scholar]
  177. Zhu M, Zhou MX, Shabala L, Shabala S. 177.  2017. Physiological and molecular mechanisms mediating xylem Na+ loading in barley in the context of salinity stress tolerance. Plant Cell Environ In press. https://doi.org/10.1111/pce.12727 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042916-040936
Loading
/content/journals/10.1146/annurev-arplant-042916-040936
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error