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Salinity tolerance in barley during germination—homologs and potential genes

大麦芽期耐盐相关的同源和候选基因

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Abstract

Salinity affects more than 6% of the world’s total land area, causing massive losses in crop yield. Salinity inhibits plant growth and development through osmotic and ionic stresses; however, some plants exhibit adaptations through osmotic regulation, exclusion, and translocation of accumulated Na+ or Cl-. Currently, there are no practical, economically viable methods for managing salinity, so the best practice is to grow crops with improved tolerance. Germination is the stage in a plant’s life cycle most adversely affected by salinity. Barley, the fourth most important cereal crop in the world, has outstanding salinity tolerance, relative to other cereal crops. Here, we review the genetics of salinity tolerance in barley during germination by summarizing reported quantitative trait loci (QTLs) and functional genes. The homologs of candidate genes for salinity tolerance in Arabidopsis, soybean, maize, wheat, and rice have been blasted and mapped on the barley reference genome. The genetic diversity of three reported functional gene families for salt tolerance during barley germination, namely dehydration-responsive element-binding (DREB) protein, somatic embryogenesis receptor-like kinase and aquaporin genes, is discussed. While all three gene families show great diversity in most plant species, the DREB gene family is more diverse in barley than in wheat and rice. Further to this review, a convenient method for screening for salinity tolerance at germination is needed, and the mechanisms of action of the genes involved in salt tolerance need to be identified, validated, and transferred to commercial cultivars for field production in saline soil.

概 要

土壤盐害影响了全球 6%以上的陆地面积, 并导致了大量的农作物减产. 盐害主要通过渗透和离子胁迫抑制植物的生长和发育, 而植物相应地通过渗透调节、 转移或外排积累的钠和氯离子以增强适应性. 目前, 生产上尚未有实用、 经济的方法治理盐害, 因而最为可行的途径是增强植物自身的耐盐性. 盐胁迫严重抑制种子萌发, 而作为全球第四大禾谷类作物的大麦与其他谷物相比耐盐性更强. 本文综述了大麦芽期耐盐性的遗传机制, 总结了已报道的相关数量性状位点和功能基因, 比对了拟南芥、 大豆、 玉米、 小麦和水稻中耐盐候选基因在大麦中的同源基因并映射到参考基因组. 此外, 本文还讨论了三个耐盐功能基因家族的遗传多样性, 包括脱水应答元件结合蛋白 (DREB)、 类体细胞胚胎发生受体激酶和水通道蛋白. 上述三个基因家族在植物中都存在丰富的多样性, 但 DREB 家族在大麦中的多样性高于水稻和小麦. 后续研究中, 芽期耐盐性的简便筛选方法仍有待开发, 耐盐基因及相关机理机制仍需鉴定、 验证, 并整合到栽培品种中, 以实现盐土上作物的生产.

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References

  1. Abido WAE, Allem A, Zsombic L, et al, 2019. Effect of gibberellic acid on germination of six wheat cultivars under salinity stress levels. Asian J Biol Sci, 12(1): 51–60. https://doi.org/10.3923/ajbs.2019.51.60

  2. Abrol IP, Yadav JSP, Massoud FI, 1988. Salt-Affected Soils and Their Management. FAO Soils Bulletin 39, Food and Agriculture Organization of the United Nations, Rome.

  3. Agarwal PK, Jha B, 2010. Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant, 54(2):20–22. https://doi.org/10.1007/s10535-010-0038-7

  4. Agarwal PK, Agarwal P, Reddy MK, et al, 2006. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep, 25(12): 1263–1274. https://doi.org/10.1007/s00299-006-0204-8

  5. Agarwal PK, ShuklaPS, Gupta K, et al.,2013. Bioengineering for salinity tolerance in plants: state of the art. Mol Bio-technol, 54(1): 102–123. https://doi.org/10.1007/s12033-012-9538-3

  6. Ahmed IM, Cao FB, Zhang M, et al., 2013a. Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE, 8(10):e77869. https://doi.org/10.1371/journal.pone.0077869

  7. Ahmed IM, Dai HX, Zheng WT, et al., 2013b. Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol Biochem, 63:49–60. https://doi.org/10.1016/j.plaphy.2012.11.004

  8. Alavilli H, Awasthi JP, Rout GR, et al., 2016. Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants. Front Plant Sci, 1:1566. https://doi.org/10.3389/fpls.2016.01566

  9. Albrecht C, Russinova E, Kemmerling B, et al., 2008. Ara-bidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways. Plant Physiol, 148(1): 611–619. https://doi.org/10.1104/pp.108.123216

  10. Alexander R, Alamillo JM, Salamini F, et al, 1994. A novel embryo-specific barley cDNA clone encodes a protein with homologies to bacterial glucose and ribitol dehydrogenase. Planta, 192(4): 519–525. https://doi.org/10.1007/BF00203590

  11. Alhasnawi AN, 2019. Role of proline in plant stress tolerance: a mini review. Res Crops, 20(1):223–229. https://doi.org/10.31830/2348-7542.2019.032

  12. Ali E, Hussain N, Shamsi IH, et al., 2018. Role of jasmonic acid in improving tolerance of rapeseed (Brassica napus L.) to Cd toxicity. J Zhejiang Univ-Sci B (Biomed & Bi-otechnol), 19(2):130–146. https://doi.org/10.1631/jzus.B1700191

  13. al-Karaki GN, 2001. Germination, sodium, and potassium concentrations of barley seeds as influenced by salinity. J Plant Nutr, 2A(3):5–522. https://doi.org/10.1081/PLN-100104976

  14. Alsheikh MK, Heyen BJ, Randall SK, 2003. Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem, 278(42):40882–40889. https://doi.org/10.1074/jbc.M307151200

  15. Al-Yassin A, Khademian R, 2015. Allelic variation of salinity tolerance genes in barley ecotypes (natural populations) using EcoTILLING: a review article. Am Eur J Agric Environ Sci, 15(4):563–572. https://doi.org/10.5829/idosi.aejaes.2015.15.4.12579

  16. Angessa TT, Zhang XQ, Zhou GF, et al., 2017. Early growth stages salinity stress tolerance in CM72xGairdner doubled haploid barley population. PLoS ONE, 12(6):e0179715. https://doi.org/10.1371/journal.pone.0179715

  17. Anosheh HP, Sadeghi H, Emam Y, 2011. Chemical priming with urea and KN03 enhances maize hybrids (Zea mays L.) seed viability under abiotic stress. J Crop Sci Biotechnol, 14(4):289–295. https://doi.org/10.1007/s12892-011-0039-x

  18. Anuradha S, Rao SSR, 2001. Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regul, 33(2):151–153. https://doi.org/10.1023/A:1017590108484

  19. Arora A, 2005. Ethylene receptors and molecular mechanism of ethylene sensitivity in plants. Curr Sci, 89 (8): 1348–1361.

  20. Ashraf M, 2009. Biotechnological approach of improving plant salt tolerance using antioxidants as markers. BiotechnolAdv, 27(1): 84–93. https://doi.org/10.1016/j.biotechadv.2008.09.003

  21. Ashraf M, Harris PJC, 2004. Potential biochemical indicators of salinity tolerance in plants. PlantSci, 166(1):3–16. https://doi.org/10.1016/j.plantsci.2003.10.024

  22. Ashraf M, Harris PJC, 2005. Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches. Haworth Press, New York, USA.

  23. Ashraf M, Akram NA, Arteca RN, et al, 2010. The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev Plant Sci, 29(3): 162–190. https://doi.org/10.1080/07352689.2010.483580

  24. Assaha DVM, Ueda A, Saneoka H, et al, 2017. The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol, 1:509. https://doi.org/10.3389/fphys.2017.00509

  25. Bajguz A, Hayat S, 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem, https://doi.org/10.1016/j.plaphy.2008.10.002

  26. Battels D, Nelson D, 1994. Approaches to improve stress tolerance using molecular genetics. Plant Cell Environ, 17(5):659–667. https://doi.org/10.1111/j.1365-3040.1994.tb00157.x

  27. Baskin CC, Baskin JM, 2001. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. Academic Press, San Diego, USA. https://doi.org/10.1016/B978-0-12-080260-9.X5000-3

  28. Batistic O, Rehers M, Akerman A, et al., 2012. S-acylationdependent association of the calcium sensor CBL2 with the vacuolar membrane is essential for proper abscisic acid responses. Cell Res, 22(7): 1155–1168. https://doi.org/10.1038/cr.2012.71

  29. Baudino S, Hansen S, Brettschneider R, et al., 2001. Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta, 213(1):1–10. https://doi.org/10.1007/s004250000471

  30. Belin C, Lopez-Molina L, 2008. Arabidopsis seed germination responses to osmotic stress involve the chromatin modifier PICKLE. Plant Signal Behav, 3(7):478–479. https://doi.org/10.4161/psb.3.7.5679

  31. Benson DA, Cavanaugh M, Clark K, et al, 2013. GenBank. Nucleic Acids Res, 41 (D1): D36–D42. https://doi.org/10.1093/nar/gks1195

  32. Bentsink L, Koornneef M, 2008. Seed dormancy and germination. Arabidopsis Book, 6:e0119. https://doi.org/10.1199/tab.0119

  33. Bernstein L, 1963. Osmotic adjustment of plants to saline media. II. Dynamic phase. Am JBot, 50(4):360–370. https://doi.org/10.1002/j.1537-2197.1963.tb07204.x

  34. Bewley JD, 1997. Seed germination and dormancy. Plant Cell, 9(7): 1055–1066. https://doi.org/10.1105/tpc.9.7.1055

  35. Bewley JD, Bradford KJ, Hilhorst HWM, et al, 2013. Seeds: Physiology of Development, Germination and Dormancy, 3rd Ed. Springer, New York, USA. https://doi.org/10.1007/978-1-4614-4693-4

  36. Blackman SA, Wettlaufer SH, Obendorf RL, et al, 1991. Maturation proteins associated with desiccation tolerance in soybean. Plant Physiol, 96(3):868–874. https://doi.org/10.1104/pp.96.3.868

  37. Bliss RD, Platt-Aloia KA, Thomson WW, 1986. Osmotic sensitivity in relation to salt sensitivity in germinating barley seeds. Plant Cell Environ, 9(9):721–725. https://doi.org/10.1111/j.1365-3040.1986.tb02104.x

  38. Bordi A, 2010. The influence of salt stress on seed germination, growth and yield of canola cultivars. Not Bot Hort Ag-robotCluj, 38(1): 128–133. https://doi.org/10.15835/nbha3813572

  39. Brini F, Hanin M, Lumbreras V, et al., 2007. Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep, 26(11): 2017–2026. https://doi.org/10.1007/s00299-007-0412-x

  40. Brini F, Yamamoto A, Jlaiel L, et al., 2011. Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis. Plant Cell Physiol, 52(4):676–688. https://doi.org/10.1093/pcp/pcr030

  41. Calestani C, Moses MS, Maestri E, et al., 2015. Constitutive expression of the barley dehydrin gene aba2 enhances Arabidopsis germination in response to salt stress. Int J Plant Biol, 6(1):5826. https://doi.org/10.4081/pb.2015.5826

  42. Capiati DA, Pais SM, Tellez-Inon MT, 2006. Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling. JExpBot, 57(10):2391–2400. https://doi.org/10.1093/jxb/erj212

  43. Chen M, Wang QY, Cheng XG, et al., 2007. GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Bio-chem BiophysRes Commun, 353(2):299–305. https://doi.org/10.1016/j.bbrc.2006.12.027

  44. Chen ZH, Cuin TA, Zhou MX, et al, 2007. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot, 58(15-16):4245–4255. https://doi.org/10.1093/jxb/erm284

  45. Cheng C, Zhang Y, Chen XG, et al., 2018. Co-expression of AtNHXl and TsVP improves the salt tolerance of transgenic cotton and increases seed cotton yield in a saline field. Mol Breeding, 38(2): 19. https://doi.org/10.1007/s1l032-018-0774-5

  46. Cheng CH, Li CM, Wang DD, et al., 2018. The soybean GmNARK affects ABA and salt responses in transgenic Arabidopsis thaliana. Front Plant Sci, 1:514. https://doi.org/10.3389/fpls.2018.00514

  47. Cheng ZQ, Targolli J, Huang XQ, et al., 2002. Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.). Mol Breed, 10(1–2):71–82. https://doi.org/10.1023/A:1020329401191

  48. Cheong YH, Sung SJ, Kim BG, et al, 2010. Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. Mol Cells, 29(2):59–65. https://doi.org/10.1007/s10059-010-0025-z

  49. Chinnusamy V, Jagendorf A, Zhu JK, 2005. Understanding and improving salt tolerance in plants. Crop Sci, 45(2): 437–448. https://doi.org/10.2135/cropsci2005.0437

  50. Chinnusamy V, Zhu JH, Zhu JK, 2006. Gene regulation during cold acclimation in plants. Physiol Plant, 126(1): 52–61. https://doi.org/10.1111/j.1399-3054.2006.00596.x

  51. Chiwocha SDS, Cutler AJ, Abrams SR, et al, 2005. The etrl-2 mutation mArabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J, 42(1):35–48. https://doi.org/10.1111/j.1365-313X.2005.02359.x

  52. Colmsee C, Beier S, Himmelbach A, et al., 2015. BARLEX the barley draft genome explorer. Mol Plant, 8(6):964–966. https://doi.org/10.1016/j.molp.2015.03.009

  53. Corpas FJ, Barroso JB, Sandalio LM, et al, 1998. A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes. Biochem J, 330(2):777–784. https://doi.org/10.1042/bj3300777

  54. Dai XY, Xu YY, Ma QB, et al., 2007. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol, 143(4): 1739–1751. https://doi.org/10.1104/pp.106.094532

  55. Debez A, Slimen IDB, Bousselmi S, et al., 2019. Comparative analysis of salt impact on sea barley from semi-arid habitats in Tunisia and cultivated barley with special emphasis on reserve mobilization and stress recovery aptitude. Plant Biosyst, published online. https://doi.org/10.1080/11263504.2019.1651777

  56. Deng XM, Hu W, Wei SY, et al, 2013. TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS ONE, 8(7): e69881. https://doi.org/10.1371/journal.pone.0069881

  57. Diaz-Mendoza M, Diaz I, Martinez M, 2019. Insights on the proteases involved in barley and wheat grain germination. Int J Mol Sci, 20(9):2087. https://doi.org/10.3390/ijms20092087

  58. Diedhiou CJ, Popova OV, Dietz KJ, et al, 2008. The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol, 1:49. https://doi.org/10.1186/1471-2229-8-49

  59. Dodd GL, Donovan LA, 1999. Water potential and ionic effects on germination and seedling growth of two cold desert shrubs. Am J Bot, 86(8): 1146–1153. https://doi.org/10.2307/2656978

  60. Dong W, Wang MC, Xu F, et al., 2013. Wheat oxophy-todienoate reductase gene TaOPRl confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiol, 161(3): 1217–1228. https://doi.org/10.1104/pp.112.211854

  61. Dubouzet JG, Sakuma Y, Ito Y, et al, 2003. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J, 33(4):751–763. https://doi.org/10.1046/j.1365-313X.2003.01661.x

  62. el-Mashad AAA, Mohamed HI, 2012. Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma, 249(3):625–635. https://doi.org/10.1007/s00709-011-0300-7

  63. Emam Y, Hosseini E, Rafiei N, et al., 2013. Response of early growth and sodium and potassium concentration in ten barley (Hordeum vulgare L.) cultivars under salt stress conditions. Crop Physiol J, 19:5–15.

  64. Fedoroff NV, 2002. Cross-talk in abscisic acid signaling. Sci STKE, 10(140):re10. https://doi.org/10.1126/stke.2002.140.rel0

  65. Figueras M, Pujal J, Saleh A, et al, 2004. Maize Rabl7 over-expression mArabidopsis plants promotes osmotic stress tolerance. Ann Appl Biol, 144(3):251–257. https://doi.org/10.1111/j.1744-7348.2004.tb00341.x

  66. Finch-Savage WE, Leubner-Metzger G, 2006. Seed dormancy and the control of germination. NewPhytol, 171(3):501–523. https://doi.org/10.1111/j.1469-8137.2006.01787.x

  67. Flowers TJ, Hajibagheri MA, 2001. Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cul-tivars differing in salt tolerance. Plant Soil, 231(1): 1–9. https://doi.org/10.1023/A:1010372213938

  68. Fu LB, Shen QF, Kuang LH, et al., 2018. Metabolite profiling and gene expression of Na/K transporter analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Plant Physiol Biochem, 130:248–257. https://doi.org/10.1016/j.plaphy.2018.07.013

  69. Gao S, Song JB, Wang Y, et al., 2017. An F-box E3 ubiquitin ligase-coding gene AtDIFl is involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. Environ Exp Bot, 138:21–35. https://doi.org/10.1016/j.envexpbot.2017.02.013

  70. Ghassemi F, Jakeman AJ, Nix HA, 1995. Salinisation of Land and Water Resources: Human Causes, Extent, Management and Case Studies. CAB International, Wallingford, UK.

  71. Giri J, Vij S, Dansana PK, et al, 2011. Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol, 191(3):721–732. https://doi.org/10.1111/j.1469-8137.2011.03740.x

  72. Glenn EP, Brown JJ, Blumwald E, 1999. Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci, 18(2): 227–255. https://doi.org/10.1080/07352689991309207

  73. Gouiaa S, Khoudi H, Leidi EO, et al., 2012. Expression of wheat Na+/H+ antiporter TNHXS1 and H+-pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance. Plant Mol Biol, 79(1–2): 137–155. https://doi.org/10.1007/s1ll03-012-9901-6

  74. Graeber K, Linkies A, Miiller K, et al., 2010. Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol, 73(1–2): 67–87. https://doi.org/10.1007/s1ll03-009-9583-x

  75. Greenway H, Munns R, 1980. Mechanisms of salt tolerance in nonhalophytes. Ann Rev Plant Physiol, 31:149–190. https://doi.org/10.1146/annurev.pp.31.060180.001053

  76. Grotewold E, 2008. Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Bio-technol, 19(2): 138–144. https://doi.org/10.1016/j.copbio.2OO8.O2.OO2

  77. Guo WL, Chen TL, Hussain N, et al., 2016. Characterization of salinity tolerance of transgenic rice lines harboring HsCBL8 of wild barley (Hordeum spontanum) line from Qinghai-Tibet Plateau. Front Plant Sci, 1:1678. https://doi.org/10.3389/fpls.2016.01678

  78. Gupta B, Huang BR, 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics, 1:701596. https://doi.org/10.1155/2014/701596

  79. Giirel F, Oztiirk ZN, Ucarh C, et al., 2016. Barley genes as tools to confer abiotic stress tolerance in crops. Front Plant Sci, 1:1137. https://doi.org/10.3389/fpls.2016.01137

  80. Gutterson N, Reuber TL, 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol, 7(4):465–471. https://doi.org/10.1016/j.pbi.2004.04.007

  81. Hampson CR, Simpson GM, 1990. Effects of temperature, salt, and osmotic potential on early growth of wheat (Triticum aestivum). I. Germination. Can J Bot, 68(3):524–528. https://doi.org/10.1139/b90-072

  82. Han B, Hughes DW, Galau GA, et al., 1997. Changes in late-embryogenesis-abundant (LEA) messenger RNAs and dehydrins during maturation and premature drying of Ricinus communis L. seeds. Planta, 201(1):27–35. https://doi.org/10.1007/BF01258677

  83. Han Y, Yin SY, Huang L, 2015. Towards plant salinity tolerance-implications from ion transporters and biochemical regulation. Plant Growth Regul, 76(1): 13–23. https://doi.org/10.1007/s10725-014-9997-6

  84. Han Y, Yin SY, Huang L, et al., 2018. A sodium transporter HvHKTl;l confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant Cell Physiol, 59(10): 1976–1989. https://doi. org/10.1093/pcp/pcy 116

  85. Hanin M, Ebel C, Ngom M, et al., 2016. New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci, 1:1787. https://doi.org/10.3389/fpls.2016.01787

  86. Hara M, 2010. The multifunctionality of dehydrins: an overview. Plant Signal Behav, 5(5):503–508. https://doi.org/10.4161/psb.11085

  87. Harlan JR, 1995. The Living Fields: Our Agricultural Heritage. Cambridge University Press, Cambridge, UK.

  88. Hasegawa PM, Bressan RA, Zhu JK, et al., 2000. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol, 51:463–499. https://doi.org/10.1146/annurev.arplant.51.1.463

  89. Hauvermale AL, Ariizumi T, Steber CM, 2012. Gibberellin signaling: a theme and variations on DELLA repression. PlantPhysiol, 160(1):83–92. https://doi.org/10.1104/pp.112.200956

  90. Hazzouri KM, Khraiwesh B, Amiri KMA, et al, 2018. Mapping of HKT1;5 gene in barley using GWAS approach and its implication in salt tolerance mechanism. Front Plant Sci, 1:156. https://doi.org/10.3389/fpls.2018.00156

  91. He XL, Hou XN, Shen YZ, et al, 2011. TaSRG, a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis. FEBS Lett, 585(8): 1231–1237. https://doi.org/10.1016/j.febslet.2011.03.055

  92. Hecht V, Vielle-Calzada JP, Hartog MV, et al., 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol, 127(3):803–816. https://doi.org/10.1104/pp.010324

  93. Hentrich M, Bottcher C, Diichting P, et al., 2013. The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J, 74(4): 626–637. https://doi.org/10.1111/tpj.12152

  94. Hernandez JA, Ferrer MA, Jimenez A, et al., 2001. Antioxidant systems and 02~/H202 production in the apoplast of pea leaves, its relation with salt-induced necrotic lesions in minor veins. Plant Physiol, 127(3):817–831. https://doi.org/10.1104/pp.010188

  95. Hou FY, Huang J, Yu SL, et al., 2007. The 6-phosphogluconate dehydrogenase genes are responsive to abiotic stresses in rice. J Integr Plant Biol, 49(5):655–663. https://doi.org/10.1111/j.1744-7909.2007.00460.X

  96. Hou XN, Liang YZ, He XL, et al., 2013. A novel ABA-responsive TaSRHP gene from wheat contributes to enhanced resistance to salt stress in Arabidopsis thaliana. PlantMol Biol Rep, 31(4): 791–801. https://doi.org/10.1007/s1ll05-012-0549-9

  97. Hoyle GL, Steadman KJ, Good RB, et al, 2015. Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Front Plant Sci, 1:731. https://doi.org/10.3389/fpls.2015.00731

  98. Hu H, Xiong L, Yang Y, 2005. Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta, 222(1): 107–117. https://doi.org/10.1007/s00425-005-1534-4

  99. Hu W, Yuan QQ, Wang Y, et al., 2012. Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol, 53(12): 2127–2141. https://doi.org/10.1093/pcp/pcsl54

  100. Huang J, Zhang HS, Wang JF, et al., 2003. Molecular cloning and characterization of rice 6-phosphogluconate dehydrogenase gene that is up-regulated by salt stress. Mol Biol Rep, 30(4):223–227. https://doi.org/10.1023/A:1026392422995

  101. Huang L, Kuang LH, Li X, et al., 2018. Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare. Environ Exp Bot, 156:48–61. https://doi.org/10.1016/j.envexpbot.2018.08.019

  102. Huang L, Kuang LH, Wu LY, et al., 2019. Comparisons in functions of HKT1;5 transporters between Hordeum marinum and Hordeum vulgare in responses to salt stress. Plant Growth Regul, 89:309–319. https://doi.org/10.1007/s10725-019-00538-7

  103. Huang QJ, Wang Y, 2016. Overexpression of TaNAC2D displays opposite responses to abiotic stresses between seedling and mature stage of transgenic Arabidopsis. Front Plant Sci, 7.1754. https://doi.org/10.3389/fpls.2016.01754

  104. Huang QJ, Wang Y, Li B, et al., 2015. TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol, 1:268. https://doi.org/10.1186/s12870-015-0644-9

  105. Huang X, Zhang Y, Jiao B, et al., 2012. Overexpression of the wheat salt tolerance-related gene TaSC enhances salt tolerance in Arabidopsis. J Exp Bot, 63(15):5463–5473. https://doi.org/10.1093/jxb/ersl98

  106. Hwang YS, Bethke PC, Cheong YH, et al., 2005. A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol, 138(3): 1347–1358. https://doi.org/10.1104/pp.105.062703

  107. Isayenkov SV, 2019. Genetic sources for the development of salt tolerance in crops. Plant Growth Regul, 89(1): 1–17. https://doi.org/10.1007/s10725-019-00519-w

  108. Ishikawa T, Shabala S, 2019. Control of xylem Na+ loading and transport to the shoot in rice and barley as a determinant of differential salinity stress tolerance. Physiol Plant, 165(3):619–631. https://doi.org/10.1111/pp1.12758

  109. Jahn TP, Mailer ALB, Zeuthen T, et al., 2004. Aquaporin homologues in plants and mammals transport ammonia. FEES Lett, 574(1–3):31–36. https://doi.org/10.1016/j.febslet.2004.08.004

  110. Jalili F, Khavazi K, Pazira E, et al., 2009. Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol, 166(6): 667–674. https://doi.org/10.1016/jjplph.2008.08.004

  111. Jamil A, Riaz S, Ashraf M, et al., 2011. Gene expression profiling of plants under salt stress. Crit Rev Plant Sci, 30(5):435–458. https://doi.org/10.1080/07352689.2011.605739

  112. Jaschke WD, Peuke AD, Pate JS, et al., 1997. Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. J Exp Bot, 48(9): 1737–1747. https://doi.org/10.1093/jxb/48.9.1737

  113. Javot H, Lauvergeat V, Santoni V, et al., 2003. Role of a single aquaporin isoform in root water uptake. Plant Cell, 15(2): 509–522. https://doi.org/10.1105/tpc.008888

  114. Jayakannan M, Bose J, Babourina O, et al., 2013. Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot, 64(8):2255–2268. https://doi.org/10.1093/jxb/ert085

  115. Jeong MJ, Lee SK, Kim BG, et al, 2006. A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell Tissue Organ Cult, 85(2):151–160. https://doi.org/10.1007/s11240-005-9064-0

  116. Jia FJ, Wang CY, Huang JG, et al., 2015. SCF E3 ligase PP2-B11 plays a positive role in response to salt stress in Arabidopsis. J Exp Bot, 66(15):4683–4697. https://doi.org/10.1093/jxb/erv245

  117. Jiang QY, Hu Z, Zhang H, et al., 2014. Overexpression of GmDREBl improves salt tolerance in transgenic wheat and leaf protein response to high salinity. Crop J, 2(2–3): 120–131. https://doi.org/10.1016/j.cj.2014.02.003

  118. Jornvall H, von Bahr-Lindstrom H, Jany KD, et al., 1984. Extended superfamily of short alcoholpolyol-sugar dehydrogenases: structural similarities between glucose and ribitol dehydrogenases. FEES Lett, 165(2): 190–196. https://doi.org/10.1016/0014-5793(84)80167-2

  119. Joshi R, Wani SH, Singh B, et al, 2016. Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci, 1:1029. https://doi.org/10.3389/fpls.2016.01029

  120. Jung J, Won SY, Suh SC, et al, 2007. The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta, 225(3):575–588. https://doi.org/10.1007/s00425-006-0373-2

  121. Jung YJ, Lee IH, Han KH, et al., 2010. Expression analysis and characterization of rice oligopeptide transport gene (OsOPTIO) that contributes to salt stress tolerance. J Plant Biotechnol, 37(4):483–493. https://doi.org/10.5010/JPB.2010.37.4.483

  122. Kanneganti V, Gupta AK, 2008. Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol, 66(5):445–462. https://doi.org/10.1007/s1ll03-007-9284-2

  123. Kavas M, Baloglu MC, Yiicel AM, et al, 2016. Enhanced salt tolerance of transgenic tobacco expressing a wheat salt tolerance gene. Turk J Biol, 40:727–735. https://doi.org/10.3906/biy-1506-36

  124. Kazan K, Manners JM, 2012. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci, 17(1):22–31. https://doi.org/10.1016/j.tplants.2011.10.006

  125. Keskin BC, Sarikaya AT, Yiiksel B, et al., 2010. Abscisic acid regulated gene expression in bread wheat (Triticum aes-tivum L.). AustJ Crop Sci, 4(8):617–625.

  126. Kleist TJ, Spencley AL, Luan S, 2014. Comparative phylo-genomics of the CBL-CIPK calcium-decoding network in the moss Physcomitrella, Arabidopsis, and other green lineages. Front Plant Sci, 1:187. https://doi.org/10.3389/fpls.2014.00187

  127. Koag MC, Fenton RD, Wilkens S, et al., 2003. The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol, 131(1):309–316. https://doi.org/10.1104/pp.011171

  128. Koag MC, Wilkens S, Fenton RD, et al, 2009. The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol, 150(3):1503–1514. https://doi.org/10.1104/pp.109.136697

  129. Kong DJ, Li MJ, Dong ZH, et al., 2015. Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses. Plant Cell Rep, 34(3):395–410. https://doi.org/10.1007/s00299-014-1717-l

  130. Kong XP, Pan JW, Zhang MY, et al., 2011. ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ, 34(8):1291–1303. https://doi.org/10.1111/j.1365-3040.2011.02329.x

  131. Koornneef M, Bentsink L, Hilhorst H, 2002. Seed dormancy and germination. Curr Opin Plant Biol, 5(1):33–36. https://doi.org/10.1016/S1369-5266(01)00219-9

  132. Krishnaswamy S, Verma S, Rahman MH, et al., 2011. Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol, 75(1–2): 107–127. https://doi.org/10.1007/s11103-010-9711-7

  133. Kriiger C, Berkowitz O, Stephan UW, et al., 2002. A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. J Biol Chem, 277(28):25062–25069. https://doi.org/10.1074/jbc.M201896200

  134. Kuang LH, Shen QF, Wu LY, et al., 2019. Identification of microRNAs responding to salt stress in barley by high-throughput sequencing and degradome analysis. Environ Exp Bot, 160:59–70. https://doi.org/10.1016/j.envexpbot.2019.01.006

  135. Kumar S, Stecher G, Li M, et al., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

  136. Kumari N, Malik K, Rani B, et al, 2019. Insights in the physiological, biochemical and molecular basis of salt stress tolerance in plants. In: Giri B, Varma A (Eds.), Microorganisms in Saline Environments: Strategies and Functions. Springer, Cham, p.353–374. https://doi.org/10.1007/978-3-030-18975-4_15

  137. Lai S, Gulyani V, Khurana P, 2008. Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res, 17(4): 651–663. https://doi.org/10.1007/s11248-007-9145-4

  138. Lauchli A, Grattan SR, 2007. Plant growth and development under salinity stress. In: Jenks MA, Hasegawa PM, Jain SM (Eds.), Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. Springer, Dordrecht, p.1–32. https://doi.org/10.1007/978-1-4020-5578-2_1

  139. Lauchli AE, Epstein E, 1990. Plant responses to saline and sodic conditions. In: Tanji KK (Ed.), Agricultural Salinity Assessment and Management. ASCE, New York, p.113–137.

  140. Lee JH, Hong JP, Oh SK, et al., 2004. The ethylene-responsive factor like protein 1 (CaERFLPl) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLPl in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol, 55(1):61–81. https://doi.org/10.1007/s11103-004-0417-6

  141. Li DD, Xia XL, Yin WL, et al., 2013. Two poplar calcineurin B-like proteins confer enhanced tolerance to abiotic stresses in transgenic Arabidopsis thaliana. Biol Plant, 57(1):70–78. https://doi.org/10.1007/s10535-012-0251-7

  142. Li J, 2010. Multi-tasking of somatic embryogenesis receptorlike protein kinases. Curr Opin Plant Biol, 13(5):509–514. https://doi.org/10.1016/j.pbi.2010.09.004

  143. Li SO, Xu CH, Yang YA, et al., 2010. Functional analysis of TaDH9A, a salt-responsive gene in wheat. Plant Cell Environ, 33(1): 117–129. https://doi.org/10.1111/j.1365-3040.2009.02063.x

  144. Li YB, Liu CH, Guo GM, et al., 2016. Expression analysis of three SERK-like genes in barley under abiotic and biotic stresses. J Plant Interact, 12(1):279–285. https://doi.org/10.1080/17429145.2017.1339836

  145. Li YY, Chen QZ, Nan HY, et al, 2017. Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean. PLoS ONE, 12(6):e0179554. https://doi.org/10.1371/journal.pone.0179554

  146. Li ZY, Xu ZS, Chen Y, et al, 2013. A novel role for Arabidopsis CBL1 in affecting plant responses to glucose and gibberellin during germination and seedling development. PLoS OAE, 8(2):e56412. https://doi.org/10.1371/journal.pone.0056412

  147. Liang WJ, Ma XL, Wan P, et al, 2018. Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun, 495(1):286–291. https://doi.org/10.1016/j.bbrc.2017.11.043

  148. Liao Y, Zou HF, Wang HW, et al, 2008. Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants. Cell Res, 18(10): 1047–1060. https://doi.org/10.1038/cr.2008.280

  149. Liu JP, Zhu JK, 1998. A calcium sensor homolog required for plant salt tolerance. Science, 280(5371): 1943–1945. https://doi.org/10.1126/science.280.5371.1943

  150. Liu JP, Ishitani M, Halfter U, et al, 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA, 97(7): 3730–3734. https://doi.org/10.1073/pnas.97.7.3730

  151. Liu P, Xu ZS, Lu PP, et al, 2013. A wheat PI4K gene whose product possesses threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis. J ExpBot, 64(10):2915–2927. https://doi.org/10.1093/jxb/ert133

  152. Liu PP, Montgomery TA, Fahlgren N, et al., 2007. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J, 52(1):133–146. https://doi.org/10.1111/j.1365-313X.2007.03218.x

  153. Liu Q, Kasuga M, Sakuma Y, et al., 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 10(8):1391–1406. https://doi.org/10.1105/tpc.10.8.1391

  154. Liu RR, Wang L, Tanveer M, et al, 2018. Seed hetero-morphism: an important adaptation of halophytes for habitat heterogeneity. Front Plant Sci, 1:1515. https://doi.org/10.3389/fpls.2018.01515

  155. Liu SW, Lv ZY, Liu YH, et al., 2018. Network analysis of ABA-dependent and ABA-independent drought responsive genes mArabidopsis thaliana. Genet Mol Biol, 41(3): 624–637. https://doi.org/10.1590/1678-4685-gmb-2017-0229

  156. Lopez-Molina L, Mongrand S, Chua NH, 2001. A postger-mination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA, 98(8):4782–4787. https://doi.org/10.1073/pnas.081594298

  157. Lopez-Molina L, Mongrand S, McLachlin DT, et al., 2002. ABI5 acts downstream of ABB to execute an ABA-dependent growth arrest during germination. Plant J, 32(3):317–328. https://doi.org/10.1046/j.1365-313X.2002.01430.x

  158. Luan ZH, Xiao MX, Zhou DW, et al, 2014. Effects of salinity, temperature, and polyethylene glycol on the seed germination of sunflower (Helianthus annuus L.). Sci World J, 1:170418. https://doi.org/10.1155/2014/170418

  159. Ma XY, Zhu XL, Li CL, et al., 2015. Overexpression of wheat NF-YA10 gene regulates the salinity stress response in Arabidopsis thaliana. Plant Physiol Biochem, 86:34–43. https://doi.org/10.1016/j.plaphy.2014.11.011

  160. Ma ZG, Bykova NV, Igamberdiev AU, 2017. Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds. Crop J, 5(6):459–477. https://doi.org/10.1016/jxj.2017.08.007

  161. Machado RMA, Serralheiro RP, 2017. Soil salinity: effect on vegetable crop growth, management practices to prevent and mitigate soil salinization. Horticulturae, 3(2): 30. https://doi.org/10.3390/horticulturae3020030

  162. Majeed A, Muhammad Z, 2019. Salinity: a major agricultural problem-causes, impacts on crop productivity and management strategies. In: Hasanuzzaman M, Hakeem KR, Nahar K, et al. (Eds.), Plant Abiotic Stress Tolerance. Springer, Cham, p.83–99. https://doi.org/10.1007/978-3-030-06118-0_3

  163. Manchanda G, Garg N, 2008. Salinity and its effects on the functional biology of legumes. Acta Physiol Plant, 30(5): 595–618. https://doi.org/10.1007/s1l738-008-0173-3

  164. Mangano S, Silberstein S, Santa-Maria GE, 2008. Point mutations in the barley HvHAKl potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress. FEES Lett, 582(28): 3922–3928. https://doi.org/10.1016/j.febslet.2008.10.036

  165. Mano Y, Takeda K, 1997. Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica, 94(3):263–272. https://doi.org/10.1023/A:1002968207362

  166. Mano Y, Nakazumi H, Takeda K, 1996. Varietal variation in and effects of some major genes on salt tolerance at the germination stage in barley. BreedSci, 46:227–233.

  167. Mansour MMF, Ali EF, 2017. Evaluation of proline functions in saline conditions. Phytochemistry, 140:52–68. https://doi.org/10.1016/j.phytochem.2017.04.016

  168. MAPK Group, Ichimura K, Shinozaki K, et al., 2002. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci, 7(7):301–308. https://doi.org/10.1016/S1360-1385(02)02302-6

  169. Marrs KA, 1996. The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant MolBiol, 47:127–158. https://doi.org/10.1146/annurev.arplant.47.1.127

  170. Mascher M, Gundlach H, Himmelbach A, et al., 2017. A chromosome conformation capture ordered sequence of the barley genome. Nature, 544(7651):427–433. https://doi.org/10.1038/nature22043

  171. Matilla A J, 2000. Ethylene in seed formation and germination. SeedSciRes, 10(2): 111–126. https://doi.org/10.1017/S096025850000012X

  172. Maurel C, Verdoucq L, Luu DT, et al., 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol, 59:595–624. https://doi.org/10.1146/annurev.arplant.59.032607.092734

  173. Maurel C, Boursiac Y, Luu DT, et al., 2015. Aquaporins in plants. Physiol Rev, 95(4): 1321–1358. https://doi.org/10.1152/physrev.00008.2015

  174. Mekawy AMM, Assaha DVM, Yahagi H, et al., 2015. Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress. Plant Physiol Biochem, 87:17–25. https://doi.org/10.1016/j.plaphy.2014.12.007

  175. Mian A, Oomen RJFJ, Isayenkov S, et al., 2011. Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J, 68(3):468–479. https://doi.org/10.1111/j.1365-313X.2011.04701.x

  176. Miransari M, Smith DL, 2014. Plant hormones and seed germination. Environ Exp Bot, 99:110–121. https://doi.org/10.1016/j.envexpbot.2013.11.005

  177. Miransari M, Smith D, 2019. Sustainable wheat (Triticum aestivum L.) production in saline fields: a review. Crit RevBiotechnol, 39(8):999–1014. https://doi.org/10.1080/07388551.2019.1654973

  178. Mishra S, Jha AB, Dubey RS, 2011. Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma, 248(3):565–577. https://doi.org/10.1007/s00709-010-0210-0

  179. Moon H, Lee B, Choi G, et al., 2003. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA, 100(1): 358–363. https://doi.org/10.1073/pnas.252641899

  180. Mu JY, Tan HL, Hong SL, et al., 2013. Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development. Mol Plant, 6(1): 188–201. https://doi.org/10.1093/mp/sss061

  181. Mukhopadhyay A, Vij S, Tyagi AK, 2004. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA, 101(16):6309–6314. https://doi.org/10.1073/pnas.0401572101

  182. Munns R, Tester M, 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol, 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911

  183. Munns R, Gardner PA, Tonnet ML, et al, 1988. Growth and development in NaCl-treated plants. II. Do Na+ or Cl-concentrations in dividing or expanding tissues determine growth in barley? AustJPlant Physiol, 15(4): 529–540. https://doi.org/10.1071/PP9880529

  184. Munns R, James RA, Xu B, et al., 2012. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol, 30(4):360–364. https://doi.org/10.1038/nbt.2120

  185. Nakashima K, Yamaguchi-Shinozaki K, 2006. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant, 126(1): 62–71. https://doi.org/10.1111/j.1399-3054.2005.00592.x

  186. Nalousi AM, Ahmadiyan S, Hatamzadeh A, et al., 2012. Protective role of exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper (Capsicum annum L.). Am Eur J Agric Environ Sci, 12(8): 1085–1090. https://doi.org/10.5829/idosi.aejaes.2012.12.08.1938

  187. Narsing Rao MP, Dong ZY, Xiao M, et al, 2019. Effect of salt stress on plants and role of microbes in promoting plant growth under salt stress. In: Giri B, Varma A (Eds.), Microorganisms in Saline Environments: Strategies and Functions. Springer, Cham, p.423–435. https://doi.org/10.1007/978-3-030-18975-4_18

  188. Nawaz K, 2007. Alleviation of the Adverse Effects of Salinity Stress on Maize (Zea mays L.) by Exogenous Application of Glycine Betaine. PhD Dissemination, Faculty of Sciences, University of Agriculture, Faisalabad, Pakistan.

  189. Negrao S, Schmockel SM, Tester M, 2017. Evaluating physiological responses of plants to salinity stress. Ann Bot, 119(1):1–11. https://doi.org/10.1093/aob/mcw191

  190. Nguyen TH, To HTM, Lebrun M, et al, 2019. Jasmonates-the master regulator of rice development, adaptation and defense. Plants, 8(9):339. https://doi.org/10.3390/plants8090339

  191. Nolan KE, Irwanto RR, Rose RJ, 2003. Auxin up-regulates MtSERKl expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol, 133(1): 218–230. https://doi.org/10.1104/pp.103.020917

  192. Oh SJ, Kwon CW, Choi DW, et al., 2007. Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. PlantBiotechnolJ, 5(5):646–656. https://doi.org/10.1111/j.1467-7652.2007.00272.X

  193. Pandey DK, Chaudhary B, 2014. Oxidative stress responsive SERK1 gene directs the progression of somatic embryo-genesis in cotton (Gossypium hirsutum L. cv. Coker 310). AmJPlantSci, 5(1):80–102. https://doi.org/10.4236/ajps.2014.51012

  194. Pandey GK, Grant JJ, Cheong YH, et al., 2008. Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant, 1(2):238–248. https://doi.org/10.1093/mp/ssn003

  195. Pardo JM, Reddy MP, Yang SL, et al., 1998. Stress signaling through Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc Natl AcadSci USA, 95(16):9681–9686. https://doi.org/10.1073/pnas.95.16.9681

  196. Parihar P, Singh S, Singh R, et al., 2015. Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res, 22(6):4056–4075. https://doi.org/10.1007/s1l356-014-3739-l

  197. Peleg Z, Blumwald E, 2011. Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol, 14(3):290–295. https://doi.org/10.1016/j.pbi.2011.02.001

  198. Pennazio S, Roggero P, 1991. Effects of exogenous salicylate on basal and stress-induced ethylene formation in soybean. Biol Plant, 33(1):58–65. https://doi.org/10.1007/BF02873789

  199. Petruzzelli L, Coraggio I, Leubner-Metzger G, 2000. Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase. Planta, 211(1): 144–149. https://doi.org/10.1007/s004250000274

  200. Pimentel D, Berger B, Filiberto D, etal.,2004. Water resources: agricultural and environmental issues. BioScience, 54(10): 909–918. https://doi.org/10.1641/0006-3568(2004)054[0909:WRA AEI]2.0.CO;2

  201. Pirasteh-Anosheh H, Ranjbar G, Pakniyat H, et al., 2016. Physiological mechanisms of salt stress tolerance in plants: an overview. In: Azooz MM, Ahmad P (Eds.), Plant-Environment Interaction: Responses and Approaches to Mitigate Stress. John Wiley & Sons, Ltd., Chichester, UK, p. 141–160. https://doi.org/10.1002/9781119081005.ch8

  202. Polash MAS, Sakil A, Hossain A, 2019. Plants responses and their physiological and biochemical defense mechanisms against salinity: a review. Trop Plant Res, 6(2):250–274. https://doi.org/10.22271/tpr.2019.v6.i2.035

  203. Popko J, Hansen R, Mendel RR, et al., 2010. The role of ab-scisic acid and auxin in the response of poplar to abiotic stress. Plant Biol, 12(2):242–258. https://doi.org/10.1111/j.1438-8677.2009.00305.x

  204. Popova LP, Stoinova ZG, Maslenkova LT, 1995. Involvement of abscisic acid in photo synthetic process in Hordeum vulgare L. during salinity stress. J Plant Growth Regul, 14(4):211–218. https://doi.org/10.1007/BF00204914

  205. Postaire O, Tournaire-Roux C, Grondin A, et al., 2010. A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. PlantPhysiol, 152(3): 1418–1430. https://doi.org/10.1104/pp.109.145326

  206. Prochazka P, Stranc P, Kupka I, et al., 2015. Forest seed treatment with brassinosteroids to increase their germination under stress conditions. J For Sci, 61(7):291–296. https://doi.org/10.17221/2/2015-JFS

  207. Qiu L, Wu DZ, Ali S, et al, 2011. Evaluation of salinity tolerance and analysis of allelic function of HvHKTl and HvHKT2 in Tibetan wild barley. Theor Appl Genet, 122(4):695–703. https://doi.org/10.1007/s00122-010-1479-2

  208. Rajjou L, Duval M, Gallardo K, et al., 2012. Seed germination and vigor. Annu Rev Plant Biol, 63:507–533. https://doi.org/10.1146/annurev-arplant-042811-105550

  209. Reddy VS, Reddy ASN, 2004. Proteomics of calcium-signaling components in plants. Phytochemistry, 65(12): 1745–1776. https://doi.org/10.1016/j.phytochem.2004.04.033

  210. Redillas MCFR, Jeong JS, Kim YS, et al., 2012. The overex-pression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant BiotechnolJ, 10(7): 792–805. https://doi.org/10.1111/j.1467-7652.2012.00697.x

  211. Rengasamy P, 2002. Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric, 42(3):351–361. https://doi.org/10.1071/EA01111

  212. Rengasamy P, 2006. World salinization with emphasis on Australia. JExpBot, 57(5): 1017–1023. https://doi.org/10.1093/jxb/erjl08

  213. Riechmann JL, Heard J, Martin G, et al., 2000. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290(5499):2105–2110. https://doi.org/10.1126/science.290.5499.2105

  214. Rinaldi LMR, 2000. Germination of seeds of olive (Olea europaea L.) and ethylene production: effects of harvesting time and thidiazuron treatment. J Hortic Sci Biotechnol, 75(6):727–732. https://doi.org/10.1080/14620316.2000.11511314

  215. Rivandi J, Miyazaki J, Hrmova M, et al, 2011. A SOS3 hom-ologue maps to HvNax4, a barley locus controlling an environmentally sensitive Na+ exclusion trait. J Exp Bot, 62(3):1201–1216. https://doi.org/10.1093/jxb/erq346

  216. Romo JT, Haferkamp MR, 1987. Effects of osmotic potential, potassium chloride, and sodium chloride on germination of greasewood (Sarcobatus vermiculatus). Great Basin Ata, 47(1):110–116.

  217. Rong W, Qi L, Wang AY, et al., 2014. The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant BiotechnolJ, 12(4):468–479. https://doi.org/10.1111/pbi.12153

  218. Sabagh AEL, Hossain A, Islam S, et al, 2019. Drought and salinity stresses in barley: consequences and mitigation strategies. Aust J Crop Sci, 13(6):810–820.

  219. Safdar H, Amin A, Shafiq Y, et al., 2019. A review: impact of salinity on plant growth. Nat Sci, 17:34–40.

  220. Sakuma Y, Liu Q, Dubouzet JG, et al., 2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun, 290(3):998–1009. https://doi.org/10.1006/BBRC.2001.6299URL

  221. Sayar R, Bchini H, Mosbahi M, et al, 2010. Effects of salt and drought stresses on germination, emergence and seedling growth of durum wheat (Triticum durum Desf). J Agric Res, 5(15):2008–2016. https://doi.org/10.5897/AJAR09.707

  222. Schmidt EDL, Guzzo F, Toonen MAJ, et al, 1997. A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development, 124(10):2049–2062.

  223. Schulte D, Close TJ, Graner A, et al., 2009. The international barley sequencing consortium-at the threshold of efficient access to the barley genome. Plant Physiol, 149(1): 142–147. https://doi.org/10.1104/pp.108.128967

  224. Seo PJ, Lee AK, Xiang FN, et al, 2008. Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol, 49(3):334–344. https://doi.org/10.1093/pcp/pcn011

  225. Shabala S, Shabala S, Cuin TA, et al., 2010. Xylem ionic relations and salinity tolerance in barley. Plant J, 61(5): 839–853. https://doi.org/10.1111/j.1365-313X.2009.04110.x

  226. Sharma R, Sahoo A, Devendran R, et al., 2014. Over-expression of a rice tau class glutathione S-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS ONE, 9(3):e92900. https://doi.org/10.1371/journal.pone.0092900

  227. Shen QF, Yu JH, Fu LB, et al., 2018. Ionomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in Tibetan wild barley. Plant Physiol Biochem, 123:319–330. https://doi.org/10.1016/j.plaphy.2017.12.032

  228. Shi HZ, Ishitani M, Kim C, et al., 2000. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/Pf antiporter. Proc Natl Acad Sci USA, 97(12):6896–6901. https://doi.org/10.1073/pnas.120170197

  229. Shinozaki K, Yamaguchi-Shinozaki K, 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol, 3(3):217–223. https://doi.org/10.1016/S1369-5266(00)80068-0

  230. Shinozaki K, Yamaguchi-Shinozaki K, 2007. Gene networks involved in drought stress response and tolerance. J Exp Bot, 58(2):221–227. https://doi.org/10.1093/jxb/erll64

  231. Shiu SH, Shih MC, Li WH, 2005. Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol, 139(1): 18–26. https://doi.org/10.1104/pp.105.065110

  232. Shrivastava P, Kumar R, 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci, 22(2): 123–131. https://doi.org/10.1016/j.sjbs.2014.12.001

  233. Shu S, Guo SR, Yuan LY, 2012. A review: polyamines and photosynthesis. In: Najafpour M (Ed.), Advances in Photosynthesis-Fundamental Aspects. Intech Open, Ri-jeka, Croatia, p.439–464. https://doi.org/10.5772/26875

  234. Singla B, Khurana JP, Khurana P, 2008. Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum. Plant CellRep, 27(5):833–843. https://doi.org/10.1007/s00299-008-0505-1

  235. Singla B, Khurana JP, Khurana P, 2009. Structural characterization and expression analysis of the SERK/SERL gene family in rice (Oryza sativa). Int J Plant Genomics, 2009: 539402. https://doi.org/10.1155/2009/539402

  236. Skriver K, Mundy J, 1990. Gene expression in response to abscisic acid and osmotic stress. Plant Cell, 2(6):503–52. https://doi.org/10.1105/tpc.2.6.503

  237. Somleva MN, Schmidt EDL, de Vries SC, 2000. Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Rep, 19(7):718–726. https://doi.org/10.1007/s002999900169

  238. Subbiah V, Reddy KJ, 2010. Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci, 35(3):451–458. https://doi.org/10.1007/s12038-010-0050-2

  239. Sun SJ, Guo SQ, Yang X, et al., 2010. Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. JExpBot, 61(10):2807–2818. https://doi.org/10.1093/jxb/erql20

  240. Sun TP, Gubler F, 2004. Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol, 55:197–223. https://doi.org/10.1146/annurev.arplant.55.031903.141753

  241. Teige M, Scheikl E, Eulgem T, et al, 2004. The MKK2 pathway mediates cold and salt stress signaling in Ara-bidopsis. Mol Cell, 15(1): 141–152. https://doi.org/10.1016/j.molcel.2004.06.023

  242. The International Barley Genome Sequencing Consortium, 2012. A physical, genetic and functional sequence assembly of the barley genome. Nature, 491(7426):711–716. https://doi.org/10.1038/naturel1543

  243. Tunnacliffe A, Wise MJ, 2007. The continuing conundrum of the LEA proteins. Naturwissenschaften, 94(10):791–812. https://doi.org/10.1007/s00114-007-0254-y

  244. Turan S, Cornish K, Kumar S, 2012. Salinity tolerance in plants: breeding and genetic engineering. AustJ Crop Sci, 6(9): 1337–1348.

  245. Uehlein N, Lovisolo C, Siefritz F, et al., 2003. The tobacco aquaporin NtAQPl is a membrane C02 pore with physiological functions. Nature, 425(6959):734–737. https://doi.org/10.1038/nature02027

  246. Valderrama R, Corpas FJ, Carreras A, et al., 2006. The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ, 29(7):449–459. https://doi.org/10.1111/j.1365-3040.2006.01530.x

  247. Vazquez MN, Guerrero YR, de la Noval WT, et al, 2019. Advances on exogenous applications of brassinosteroids and their analogs to enhance plant tolerance to salinity: a review. AustJ Crop Sci, 13(1): 115–121. https://doi.org/10.21475/ajcs.19.13.01.pl404

  248. Visioni A, al-Abdallat A, Elenien JA, et al., 2019. Genomics and molecular breeding for improving tolerance to abiotic stress in barley (Hordeum vulgare L.). In: Rajpal VR, Sehgal D, Kumar A, et al. (Eds.), Genomics Assisted Breeding of Crops for Abiotic Stress Tolerance, Vol. II. Springer, Cham, p.49–68. https://doi.org/10.1007/978-3-319-99573-1_4

  249. Volkmar KM, Hu Y, Steppuhn H, 1998. Physiological responses of plants to salinity: a review. Can J Plant Sci, 78(1): 19–27. https://doi.org/10.4141/P97-020

  250. Walia H, Wilson C, Wahid A, et al., 2006. Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genomics, 6(2): 143–156. https://doi.org/10.1007/s10142-005-0013-0

  251. Walters C, Ried JL, Walker-Simmons MK, 1997. Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties. Seed Sci Res, 7(2): 125–134. https://doi.org/10.1017/S0960258500003469

  252. Wang C, Deng PY, Chen LL, et al., 2013. A wheat WRKY transcription factor TaWRKYlO confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS ONE, 8(6):e65120. https://doi.org/10.1371/journal.pone.0065120

  253. Wang JB, Ding B, Guo YL, et al., 2014. Overexpression of a wheat phospholipase D gene, TaPLDa, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana. Planta, 240(1): 103–115. https://doi.org/10.1007/s00425-014-2066-6

  254. Wang L, He XL, Zhao YJ, et al, 2011. Wheat vacuolar Pf-ATPase subunit B cloning and its involvement in salt tolerance. Planta, 234(1):1–7. https://doi.org/10.1007/s00425-011-1383-2

  255. Wang MY, Gu D, Liu TS, et al., 2007. Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol, 65(6):733–746. https://doi.org/10.1007/s11103-007-9238-8

  256. Wang X, Shi GX, Xu QS, et al., 2007. Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J Plant Physiol, 164(8): 1062–1070. https://doi.org/10.1016/jjplph.2006.06.003

  257. Wang X, Hou C, Zheng K, et al., 2017. Overexpression of ERF96, a small ethylene response factor gene, enhances salt tolerance in Arabidopsis. Biol Plant, 61(4): 693–701. https://doi.org/10.1007/s10535-017-0734-7

  258. Wang XT, Zeng J, Li Y, et al, 2015. Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances. Front Plant Sci, 1:615. https://doi.org/10.3389/fpls.2015.00615

  259. Weitbrecht K, Muller K, Leubner-Metzger G, 2011. First off the mark: early seed germination. JExpBot, 62(10):3289–3309. https://doi.org/10.1093/jxb/err030

  260. Weyers JDB, Paterson NW, 2001. Plant hormones and the control of physiological processes. New Phytol, 152(3): 375–407. https://doi.org/10.1046/j.0028-646X.2001.00281.x

  261. Widodo, Patterson JH, Newbigin E, et al, 2009. Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. JExpBot, 60(14):4089–4103. https://doi.org/10.1093/jxb/erp243

  262. Witzel K, Weidner A, Surabhi GK, et al, 2010. Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant Cell Environ, 33(2):211–222. https://doi.org/10.1111/j.1365-3040.2009.02071.x

  263. Wu DZ, Qiu L, Xu LL, et al., 2011. Genetic variation of HVCBF genes and their association with salinity tolerance in Tibetan annual wild barley. PLoS ONE, 6(7): e22938. https://doi.org/10.1371/journal.pone.0022938

  264. Wu HH, Shabala L, Zhou MX, et al., 2019. Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance. Plant J, 100(1):55–67. https://doi.org/10.1111/tpj.14424

  265. Wurzinger B, Mair A, Pfister B, et al, 2011. Cross-talk of calcium-dependent protein kinase and MAP kinase signaling. Plant Signal Behav, 6(1):8–12. https://doi.org/10.4161/psb.6.1.14012

  266. Xiang Y, Lu YH, Song M, et al., 2015. Overexpression of a Triticum aestivum calreticulin gene (TaCRTl) improves salinity tolerance in tobacco. PLoS ONE, 10(10): e0140591. https://doi.org/10.1371/journal.pone.0140591

  267. Xiong HY, Li JJ, Liu PL, et al., 2014. Overexpression of OsMYB48-l, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE, 9(3):e92913. https://doi.org/10.1371/journal.pone.0092913

  268. Xiong LM, Zhu JK, 2001. Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant, 112(2):152–166. https://doi.org/10.1034/j.1399-3054.2001.1120202.x

  269. Xiong LZ, Yang YN, 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell, 15(3):745–759. https://doi.org/10.1105/tpc.008714

  270. Xu Q, Truong TT, Barrero JM, et al, 2016. A role for jasmonates in the release of dormancy by cold stratification in wheat. J Exp Bot, 67(ll):3497-3508. https://doi.org/10.1093/jxb/erwl72

  271. Xu ZS, Ni ZY, Liu L, et al., 2008a. Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat. Mol Genet Genomics, 280(6):497–508. https://doi.org/10.1007/s00438-008-0382-x

  272. Xu ZS, Chen M, Li LC, et al, 2008b. Functions of the ERF transcription factor family in plants. Botany, 86(9): 969–977. https://doi.org/10.1139/B08-041

  273. Xu ZS, Ni ZY, Li ZY, et al., 2009. Isolation and functional characterization of HvDREB1-a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare. J Plant Res, 122(1): 121–130. https://doi.org/10.1007/s10265-008-0195-3

  274. Xue DW, Huang YZ, Zhang XQ, et al, 2009. Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica, 169(2): 187–196. https://doi.org/10.1007/s10681-009-9919-2

  275. Xue GP, Loveridge CW, 2004. HvDRFl is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J, 37(3): 326–339. https://doi.org/10.1046/j.1365-313X.2003.01963.x

  276. Xue ZY, Zhi DY, Xue GP, et al, 2004. Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/FI+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci, 167(4):849–859. https://doi.org/10.1016/j.plantsci.2004.05.034

  277. Yadav D, Ahmed I, Shukla P, et al., 2016. Overexpression of Arabidopsis AnnAt8 alleviates abiotic stress in transgenic Arabidopsis and tobacco. Plants, 5(2): 18. https://doi.org/10.3390/plants5020018

  278. Yang C, Zhao TJ, Yu DY, et al., 2011. Isolation and functional characterization of a SERK gene from soybean Glycine max (L.) Merr.). Plant Mol Biol Rep, 29(2): 334–344. https://doi.org/10.1007/s1ll05-010-0235-8

  279. Yang SF, Hoffman NE, 1984. Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol, 35: 155–189. https://doi.org/10.1146/annurev.pp.35.060184.001103

  280. Yarra R, 2019. The wheat NHX gene family: potential role in improving salinity stress tolerance of plants. Plant Gene, 1:100178. https://doi.org/10.1016/j.plgene.2019.100178

  281. Yarra R, Kirti PB, 2019. Expressing class I wheat NHX (TaNHX2) gene in eggplant (Solanum melongena L.) improves plant performance under saline condition. Fund Integr Genomics, 19(4):541–554. https://doi.org/10.1007/s10142-019-00656-5

  282. Yen HE, Wu SM, Hung YH, et al., 2000. Isolation of 3 salt-induced low-abundance cDNAs from light-grown callus of Mesembryanthemum crystallinum by suppression subtractive hybridization. Physiol Plant, 110(3):402–409. https://doi.org/10.1111/j.1399-3054.2000.1100315.x

  283. Yi SY, Kim JH, Joung YH, et al., 2004. The pepper transcription factor CaPFl confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol, 136(1):2862–2874. https://doi.org/10.1104/pp.104.042903

  284. Yin SY, Han Y, Huang L, et al., 2018. Overexpression of HvCBF7 and HvCBF9 changes salt and drought tolerance in Arabidopsis. Plant Growth Regul, 85(2):281–292. https://doi.org/10.1007/s10725-018-0394-4

  285. Yin XY, Yang AF, Zhang KW, et al., 2004. Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene. Acta Bot Sin-Engl erf, 46(7):854–861.

  286. Yousefirad S, Soltanloo H, Ramezanpour SS, et al., 2018. Salt oversensitivity derived from mutation breeding improves salinity tolerance in barley via ion homeostasis. Biol Plant, 62(4):775–785. https://doi.org/10.1007/s10535-018-0823-2

  287. Zang DD, Li HY, Xu HY, et al., 2016. An Arabidopsis zinc finger protein increases abiotic stress tolerance by regulating sodium and potassium homeostasis, reactive oxygen species scavenging and osmotic potential. Front Plant Sci, 1:1272. https://doi.org/10.3389/fpls.2016.01272

  288. Zardoya R, Ding XD, Kitagawa Y, et al., 2002. Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci USA, 99(23): 14893–14896. https://doi.org/10.1073/pnas.192573799

  289. Zhang D, Jiang S, Pan J, et al., 2014. The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol, 16(3):558–570. https://doi.org/10.1111/p1b.12084

  290. Zhang GQ, Zhang M, Zhao ZX, et al., 2017. Wheat TaPUBl modulates plant drought stress resistance by improving antioxidant capability. Sci Rep, 1:7549. https://doi.org/10.1038/s41598-017-08181-w

  291. Zhang HW, Huang ZJ, Xie BY, et al., 2004. The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta, 220(2):262–270. https://doi.org/10.1007/s00425-004-1347-x

  292. Zhang HX, Irving LJ, McGill C, et al., 2010. The effects of salinity and osmotic stress on barley germination rate: sodium as an osmotic regulator. Ann Bot, 106(6): 1027–1035. https://doi.org/10.1093/aob/mcq204

  293. Zhang X, Ju HW, Chung MS, et al, 2011. The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol, 52(1): 138–148. https://doi.org/10.1093/pcp/pcq180

  294. Zhang XX, Liu SK, Takano T, 2008. Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. PlantMolBiol, 68(1–2): 131–143. https://doi.org/10.1007/s1ll03-008-9357-x

  295. Zhang XX, Tang YJ, Ma QB, et al, 2013. OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean. PLoS ONE, 8(12):e83011. https://doi.org/10.1371/journal.pone.0083011

  296. Zhang Y, Chen C, Jin XF, et al., 2009. Expression of a rice DREB1 gene, OsDREBID, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Rep, 42(8): 486–492. https://doi.org/10.5483/bmbrep.2009.42.8.486

  297. Zhang YY, Wang LL, Liu YL, et al., 2006. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta, 224(3):545–555. https://doi.org/10.1007/s00425-006-0242-z

  298. Zhao LQ, Zhang F, Guo JK, et al., 2004. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol, 134(2): 849–857. https://doi.org/10.1104/pp.103.030023

  299. Zhao Y, Tian XJ, Li YY, et al., 2017. Molecular and functional characterization of wheat ARGOS genes influencing plant growth and stress tolerance. Front Plant Sci, 1:170. https://doi.org/10.3389/fpls.2017.00170

  300. Zhu JH, Shi HZ, Lee BH, et al., 2004. An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci USA, 101(26):9873–9878. https://doi.org/10.1073/pnas.0403166101

  301. Zhu JH, Verslues PE, Zheng XW, et al, 2005. HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci USA, 102(28): 9966–9971. https://doi.org/10.1073/pnas.0503960102

  302. Zhu JK, 2001. Plant salt tolerance. Trends Plant Sci, 6(2): 66–71. https://doi.org/10.1016/S1360-1385(00)01838-0

  303. Zhu JK, 2002. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329

  304. Zhu JK, 2003. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol, 6(5):441–445. https://doi.org/10.1016/S1369-5266(03)00085-2

  305. Zhu JK, Hasegawa PM, Bressan RA, et al, 1997. Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci, 16(3):253–277. https://doi.org/10.1080/07352689709701950

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Acknowledgments

The authors would like to appreciate the expertise assistance from the institution and staff of Murdoch University, Western Barley Genetics Alliance, Western Australian State Agricultural Biotechnology Centre and the Department of Primary Industries and Regional Development (Australia). We are grateful to Peng-hao WANG and Yong JIA (Murdoch University, Australia) for their input during information analysis and cherish Le XU (Yangtze University, China) for comments on the manuscript and discussion.

Author information

Edward MWANDO performed literature search, data analysis, interpretation of information, and drafting the manuscript. Tefera Tolera ANGESSA and Yong HAN gave guidance on relevant literature search, information and data interpretation. Chengdao LI conceived the projects idea. All authors revised the paper and approved the final version to be published.

Correspondence to Chengdao Li.

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Edward MWANDO, Tefera Tolera ANGESSA, Yong HAN, and Chengdao LI declare that they have no conflict of interest.

This article does not contain any studies with human or animal subjects performed by any of the authors.

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Mwando, E., Angessa, T.T., Han, Y. et al. Salinity tolerance in barley during germination—homologs and potential genes. J. Zhejiang Univ. Sci. B (2020). https://doi.org/10.1631/jzus.B1900400

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Keywords

  • Genetics
  • Barley
  • Quantitative trait locus (QTL)
  • Germination
  • Salinity tolerance
  • Homologous gene
  • Diversity

关键词

  • 遗传
  • 大麦
  • 数量性状位点
  • 发芽
  • 耐盐性
  • 同源基因
  • 多样性

CLC number

  • S512.3
  • Q943.2