Learning from halophytes: Physiological basis and strategies to improve abiotic stress tolerance in crops

Annals of Botany

Volumn 112, Issue 7, 2013, Pages 1209-1221

  Shabala, Sergey ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Cytosolic potassium; Drought; Epidermal bladder; Membrane potential; Osmotic adjustment; Salinity; Sodium sequestration; Stomata; Trichome; Vacuole; Xylem loading

Indexed keywords

BIOTIC FACTOR; BREEDING; CROP; GENETIC ANALYSIS; HALOPHYTE; NUTRIENT CYCLING; OPTIMIZATION; PHYSIOLOGY; SALINITY TOLERANCE; WATER USE EFFICIENCY;

SODIUM CHLORIDE;

ADAPTATION; CELL VACUOLE; CYTOSOLIC POTASSIUM; DROUGHT; EPIDERMAL BLADDER; HALOPHYTE; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT OSMOTIC ADJUSTMENT; PLANT STOMA; REVIEW; SALINITY; SODIUM SEQUESTRATION; STOMATA; TRICHOME; XYLEM LOADING;

CYTOSOLIC POTASSIUM; DROUGHT; EPIDERMAL BLADDER; MEMBRANE POTENTIAL; OSMOTIC ADJUSTMENT; SALINITY; SODIUM SEQUESTRATION; STOMATA; TRICHOME; VACUOLE; XYLEM LOADING;

ADAPTATION, PHYSIOLOGICAL; PLANT STOMATA; SALT-TOLERANT PLANTS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; VACUOLES;

EID: 84889820022     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mct205     Document Type: Review

References (159)

1. Adams P, Nelson DE, Yamada S, et aL. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138: 171-190.
2. Adolf VI, Shabala S, Andersen MN, Razzaghi F, Jacobsen SE. 2012. Varietal differences of quinoa's tolerance to saline conditions. Plant and Soil 357: 117-129.
3. Agarwal PK, Shukla PS, Gupta K, Jha B. 2013. Bioengineering for salinity tolerance in plants: state of the art. Molecular Biotechnology 54: 102-123.
4. Amarasinghe V, Watson L. 1988. Comparative ultrastructure of microhairs in grasses. Botanical Journal of the Linnean Society 98: 303-319.
5. AndersonWP,WillcocksDA,Wright BJ. 1977. Electrophysiological measurements on root of Atriplex hastata. Journal of Experimental Botany 28: 894-901.
6. Apse MP, Aharon GS, Snedden WA, Blumwald E. 1999. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256-1258.
7. Apse MP, Blumwald E. 2007. Na+ transport in plants. FEBS Letters 581: 2247-2254.
8. Asad A. 2002. Growing Atriplex and Maireana species in saline sodic andwaterlogged soils. Communications in Soil Science and Plant Analysis 33: 973-989.
9. Ayala F, O'Leary JW, Schumaker KS. 1996. Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr. in response to NaCL. Journal of Experimental Botany 47: 25-32.
10. Balnokin YV, Myasoedov NA, Shamsutdinov ZS, Shamsutdinov NZ. 2005. Significance of Na+ and K+ for sustained hydration of organ tissues in ecologically distinct halophytes of the family Chenopodiaceae. Russian Journal of Plant Physiology 52: 779-787.
11. Balnokin YV, Kurkova EB, Khalilova LA, Myasoedov NA, Yusufov AG. 2007. Pinocytosis in the root cells of a salt-accumulating halophyte Suaeda altissima and its possible involvement in chloride transport. Russian Journal of Plant Physiology 54: 797-805.
12. Barkla BJ, Zingarelli L, Blumwald E, Smith JAC. 1995. Tonoplast Na+/H+ antiport activity and its energization by the vacuolarH+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiology 109: 549-556.
13. Barrett-Lennard EG. 2002. Restoration of saline land through revegetation. Agricultural Water Management 53: 213-226.
14. Barrett-Lennard EG, Setter TL. 2010. Developing saline agriculture: moving from traits and genes to systems. Functional Plant Biology 37: pIII-IV. Blume YB,KrasylenkoYA,Yemets AI. 2012. Effects of phytohormones on the cytoskeleton of the plant celL. Russian Journal of Plant Physiology 59: 515-529.
15. Blumwald E, Poole RJ. 1985. Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiology 78: 163-167.
16. Bonales-Alatorre E, Pottosin I, Shabala L, et aL. 2013a. Plasma and vacuolar membrane transporters conferring genotypic difference in salinity tolerance in a halophyte species, Chenopodium quinoa. International Journal of Molecular Science 14: 9267-9285.
17. Bonales-Alatorre E, Shabala S, Chen ZH, Pottosin I. 2013b. Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, quinoa. Plant Physiology 162: 940-952.
18. Bose J, Shabala L, Pottosin I, et aL. 2013. Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to ROS: physiological traits that differentiate salinity tolerance between pea and barley. Plant, Cell and Environment, in press. doi:10.1111/pce.12180.
19. BoughallebF, DendenM,Ben TibaB. 2009. PhotosystemII photochemistry and physiological parameters of three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea under salt stress. Acta Physiologiae Plantarum 31: 463-476.
20. Boyer JS,Wong SC,FarquharGD.1997.CO2 andwater vapor exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiology 114: 185-191.
21. Brown ME, Funk CC. 2008. Climate -food security under climate change. Science 319: 580-581.
22. Bruggemann LI, Pottosin II, Schonknecht G. 1999. Selectivity of the fast activating vacuolar cation channeL. Journal of Experimental Botany 50: 873-876.
23. Chaudhri II, Shah BH, Naqvi N, Mallick IA. 1964. Investigations on the role of Suaedafruticose Forsk in the reclamation of saline and alkaline soils inWest Pakistan plains. Plant and Soil 21: 1-7.
24. ChenZH,Pottosin II, CuinTA, et aL. 2007.Root plasmamembrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiology 145: 1714-1725.
25. Chien JC, Sussex IM. 1996. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L) Heynh. Plant Physiology 111: 1321-1328.
26. Churchman ML, Brown ML, Kato N, et aL. 2006. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. The Plant Cell 18: 3145-3157.
27. Clipson NJW, Flowers TJ. 1987. Salt tolerance in the halophyte Suaeda maritima (L) Dum -the effect of salinity on the concentration of sodium in the xylem. New Phytologist 105: 359-366.
28. Colmenero-Flores JM, Martinez G, et aL. 2007. Identification and functional characterization of cation-chloride cotransporters in plants. The Plant Journal 50: 278-292.
29. Colmer TD, Munns R, Flowers TJ. 2005. Improving salt tolerance of wheat and barley: future prospects.Australian Journal of Experimental Agriculture 45: 1425-1443.
30. Cosentino C, Fischer-Schliebs E, Bertl A, Thiel G,HomannU. 2010. Na+/H+ antiporters are differentially regulated in response to NaCl stress in leaves and roots of Mesembryanthemum crystallinum. New Phytologist 186: 669-680.
31. Cuin TA, Shabala S. 2007. Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant, Cell and Environment 30: 875-885.
32. Cuin TA, TianY, Betts SA, Chalmandrier R, Shabala S. 2009. Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions. Functional Plant Biology 36: 1110-1119.
33. CuinTA,Parsons D, Shabala S. 2010.Wheat cultivars can be screened for NaCl salinity tolerance by measuring leaf chlorophyll content and shoot sap potassium. Functional Plant Biology 37: 656-664.
34. De Boer AH, Volkov V. 2003. Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant, Cell and Environment 26: 87-101.
35. Delpire E, Mount DB. 2002. Human and murine phenotypes associated with defects in cation-chloride cotransport. Annual Review of Physiology 64: 803-843.
36. DemidchikV, CuinTA, Svistunenko D, et aL. 2010. Arabidopsis rootK+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123: 1468-1479.
37. Epstein E, Norlyn JD, RushDW, et aL. 1980. Saline culture of crops -a genetic approach. Science 210: 399-404.
38. Eshel A, Zilberstein A, Alekparov C, et aL. 2010. Biomass production by desert halophytes: Alleviating the pressure on food production. In:Recent advances in energy and environment. EE'10 Proceedings of the 5th IASME/WSEAS international conference on Energy & environment. Pp. 362-367.
39. Flowers TJ. 1985. Physiology of halophytes. Plant and Soil 89: 41-56.
40. Flowers TJ. 2004. Improving crop salt tolerance. Journal of Experimental Botany 55: 307-319.
41. Flowers TJ, Colmer TD. 2008. Salinity tolerance in halophytes. New Phytologist 179: 945-963.
42. Flowers TJ,Yeo AR. 1995. Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22: 875-884.
43. Flowers TJ, Troke PF, Yeo AR. 1977. Mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology and Plant Molecular Biology 28: 89-121.
44. Flowers TJ, Hajibagheri MA, Clipson NJW. 1986. Halophytes. Quarterly Review of Biology 61: 313-337.
45. Flowers TJ, Galal HK, Bromham L. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37: 604-612.
46. Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR. 1999. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences, USA 96: 1480-1485.
47. Ghnaya T, Nouairi I, Slama I, et aL. 2005. Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. Journal of Plant Physiology 162: 1133-1140.
48. GlennEP,CoatesWE,Riley JJ,KuehlRO, Swingle RS.1992. Salicornia bigelovii Torr -a seawater-irrigated forage for goats. Animal Feed Science and Technology 40: 21-30.
49. Glenn E, Miyamoto S, Moore D, Brown JJ, Thompson TL, Brown P. 1997. Water requirements for cultivating Salicornia bigelovii Torr. with seawater on sand in a coastal desert environment. Journal of Arid Environments 36: 711-730.
50. Glenn E, Tanner R, Miyamoto S, Fitzsimmons K, Boyer J. 1998.Water use, productivity and forage quality of the halophyte Atriplex nummularia grown on saline waste water in a desert environment. Journal of Arid Environments 38: 45-62.
51. Glenn EP, Brown JJ, Blumwald E. 1999. Salt tolerance and crop potential of halophytes. Critical Reviews in Plant Sciences 18: 227-255.
52. Glover BJ. 2000. Differentiation in plant epidermal cells. Journal of Experimental Botany 51: 497-505.
53. Grebe M. 2012. The patterning of epidermal hairs in Arabidopsis -updated. Current Opinion in Plant Biology 15: 31-37.
54. Greenboim-Wainberg Y, Maymon I, Borochov R, et aL. 2005. Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. The Plant Cell 17: 92-102.
55. Greenway H, Munns R. 1980. Mechanisms of salt tolerance in non-halophytes. Annual Review of Plant Physiology 31: 149-190.
56. Guimil S, Dunand C. 2007. Cell growth and differentiation in Arabidopsis epidermal cells. Journal of Experimental Botany 58: 3829-3840.
57. Guo SL, Yin HB, Zhang X, et aL. 2006. Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Molecular Biology 60: 41-50.
58. Haas M. 1989. Properties and diversity of (Na-K-Cl) cotransporters. Annual Review of Physiology 51: 443-457.
59. Harling H, Czaja I, Schell J, Walden R. 1997. A plant cation-chloride co-transporter promoting auxin-independent tobacco protoplast division. EMBO Journal 16: 5855-5866.
60. Hedrich R, Neher E. 1987. Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329: 833-836.
61. Hughes FM, Cidlowski JA. 1999. Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Advances in Enzyme Regulation 39: 157-171.
62. Ishida T, Kurata T, Okada K,Wada T. 2008. A genetic regulatory network in the development of trichomes and root hairs. Annual Review of Plant Biology 59: 365-386.
63. Jacobsen SE,Mujica A, Ortiz R. 2003.Theglobal potential for quinoa and other Andean crops. Food Reviews International 19: 139-148.
64. Jacobsen SE, Christiansen JL, Rasmussen J. 2010.Weed harrowing and interrowhoeing in organic grownquinoa (Chenopodium quinoaWilld.). Outlook on Agriculture 39: 223-227.
65. Jordan FL, Yoklic M, Morino K, Brown P, Seaman R, Glenn EP. 2009. Consumptive water use and stomatal conductance of Atriplex lentiformis irrigated with industrial brine in a desert irrigation district. Agricultural and Forest Meteorology 149: 899-912.
66. Karimi G, Ghorbanli M, Heidari H, Nejad RAK, Assareh MH. 2005. The effects of NaCl on growth, water relations, osmolytes and ion content in Kochia prostrata. Biologia Plantarum 49: 301-304.
67. Kemp PR, Cunningham GL. 1981. Light, temperature and salinity effects on growth, leaf anatomy and photosynthesis of Distichlis spicata (L) greene. American Journal of Botany 68: 507-516.
68. KhanMA, Ansari R, Ali H, Gul B, Nielsen BL. 2009. Panicum turgidum, a potentially sustainable cattle feed alternative to maize for saline areas. Agriculture Ecosystems and Environment 129: 542-546.
69. Kobayashi H,YanakaM, IkedaTM.2010. Exogenous methyl jasmonate alters trichome density on leaf surfaces of Rhodes Grass (Chloris gayana Kunth). Journal of Plant Growth Regulation 29: 506-511.
70. Koyro HW, Eisa SS. 2008. Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd. Plant and Soil 302: 79-90.
71. Krebs M, Beyhl D, Gorlich E, et aL. 2010. Arabidopsis V-ATPase activity at the tonoplast is required forefficient nutrient storage but not for sodiumaccumulation. Proceedings of the National Academy of Sciences, USA 107: 3251-3256.
72. LacombeB, Pilot G,GaymardF, Sentenac H, ThibaudJB. 2000.pHcontrol of the plant outwardly-rectifying potassium channelSKOR.FEBSLetters 466: 351-354.
73. Larkin JC, Young N, Prigge M, Marks MD. 1996. The control of trichome spacing and number in Arabidopsis. Development 122: 997-1005.
74. Lun'kov RV, Andreev IM, Myasoedov NA, Khailova GF, Kurkova EB, Balnokin YV. 2005. Functional identification of H+-ATPase and Na+/H+ antiporter in the plasma membrane isolated from the root cells of saltaccumulating halophyte Suaeda altissima. Russian Journal of Plant Physiology 52: 635-644.
75. Lutts S, Lefevre I, Delperee C, et aL. 2004. Heavy metal accumulation by the halophyte species Mediterranean saltbush. Journal of Environmental Quality 33: 1271-1279.
76. Maathuis FJM, Flowers TJ, Yeo AR. 1992. Sodium-chloride compartmentation in leaf vacuoles of the halophyte Suaeda maritima (L) dum and its relation to tonoplast permeability. Journal of Experimental Botany 43: 1219-1223.
77. MacRobbie EAC. 1998. Signal transduction and ion channels in guard cells. Philosophical Transactions of the Royal Society B: Biological Sciences 353: 1475-1488.
78. Malcolm CV. 1986. Production from salt affected soils. Reclamation and Revegetation Research 5: 343-361.
79. Manousaki E, Kalogerakis N. 2009. Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environmental Science and Pollution Research 16: 844-854.
80. Manousaki E, Kalogerakis N. 2011a. Halophytes present new opportunities in phytoremediation of heavy metals and saline soils. Industrial and Engineering Chemistry Research 50: 656-660.
81. Manousaki E, Kalogerakis N. 2011b. Halophytes -an emerging trend in phytoremediation. International Journal of Phytoremediation 13: 959-969.
82. Marcum KB, Murdoch CL. 1992. Salt tolerance of the coastal salt-marsh grass, Sporobolus virginicus (L) kunth. New Phytologist 120: 281-288.
83. Maricle BR, Koteyeva NK, Voznesenskaya EV, Thomasson JR, Edwards GE. 2009. Diversity in leaf anatomy, and stomatal distribution and conductance, between salt marsh and freshwater species in the C-4 genus Spartina (Poaceae). New Phytologist 184: 216-233.
84. Marschner H. 1995. Mineral nutrition of higher plants. London: Academic Press.
85. Martin C, Glover BJ. 2007.Functional aspects of cell patterning in aerial epidermis. Current Opinion in Plant Biology 10: 70-82.
86. Martinez JP, Kinet JM, Bajji M, Lutts S. 2005. NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. Journal of Experimental Botany 56: 2421-2431.
87. Mathur J, Chua NH. 2000. Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. The Plant Cell 12: 465-477.
88. Maughan PJ, Turner TB, Coleman CE, et aL. 2009. Characterization of Salt Overly Sensitive 1 (SOS 1) gene homoeologs in quinoa (Chenopodium quinoaWilid.). Genome 52: 647-657.
89. Millar J,Roots J. 2012. Changes in Australian agriculture and land use: implications for future food security. International Journal of Agricultural Sustainability 10: 25-39.
90. Munns R. 2002.Comparative physiology of salt andwater stress. Plant,Cell and Environment 25: 239-250.
91. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-681.
92. Naz N, Hameed M, Ashraf M, Al-Qurainy F, Arshad M. 2010. Relationships between gas-exchange characteristics and stomatal structural modifications in some desert grasses under high salinity. Photosynthetica 48: 446-456.
93. Norman HC, Masters DG,Wilmot MG, Rintoul AJ. 2008. Effect of supplementation with grain, hay or straw on the performance of weaner Merino sheep grazing old man (Atriplex nummularia) or river (Atriplex amnicola) saltbush. Grass and Forage Science 63: 179-192.
94. Norman HC, Masters DG, Barrett-Lennard EG. 2013. Halophytes as forages in saline landscapes: interactions between plant genotype and environment change their feeding value to ruminants. Environmental and Experimental Botany 92: 96-109.
95. Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ. 2010. Intracellular consequences of SOS1 deficiency during salt stress. Journal of Experimental Botany 61: 1205-1213.
96. O'Leary JW, Glenn EP, Watson MC. 1985. Agricultural production of halophytes irrigated with seawater. Plant and Soil 89: 311-321.
97. OmamiEN,Hammes PS,Robbertse PJ. 2006. Differences in salinity tolerance for growth and water-use efficiency in some amaranth (Amaranthus spp.) genotypes. New Zealand Journal of Crop and Horticultural Science 34: 11-22.
98. Orsini F, Accorsi M, Gianquinto G, et aL. 2011. Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Functional Plant Biology 38: 818-831.
99. Pantoja O, Dainty J, Blumwald E. 1989. Ion channels in vacuoles from halophytes and glycophytes. FEBS Letters 255: 92-96.
100. ParksGE,DietrichMA,Schumaker KS. 2002. Increased vacuolarNa+/H+exchange activity in Salicornia bigelovii Torr. in response to NaCL. Journal of Experimental Botany 53: 1055-1065.
101. Passardi F, Dobias J, Valerio L, Guimil S, Penel C, Dunand C. 2007. Morphological and physiological traits of three major Arabidopsis thaliana accessions. Journal of Plant Physiology 164: 980-992.
102. Perazza D, Vachon G, Herzog M. 1998. Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis. Plant Physiology 117: 375-383.
103. Perera L, Mansfield TA, Malloch AJC. 1994. Stomatal responses to sodium-ions in Aster tripolium -a new hypothesis to explain salinity regulation in aboveground tissues. Plant, Cell and Environment 17: 335-340.
104. Pesch M, Hulskamp M. 2009. One, two, three . . . models for trichome patterning in Arabidopsis? Current Opinion in Plant Biology 12: 587-592.
105. Pilot G, Gaymard F, Mouline K, Cherel I, Sentenac H. 2003. Regulated expression of Arabidopsis Shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Molecular Biology 51: 773-787.
106. Pottosin II, Tikhonova LI, Hedrich R, Schonknecht G. 1997. Slowly activating vacuolarchannels cannot mediateCa2+-inducedCa2+release.The Plant Journal 12: 1387-1398.
107. Pottosin II, Dobrovinskaya OR,Muniz J. 2001.Conduction of monovalent and divalent cations in the slowvacuolar channeL. Journal of Membrane Biology 181: 55-65.
108. Qadir M, Tubeileh A, Akhtar J, Larbi A, Minhas PS, Khan MA. 2008. Productivityenhancement of salt-affected environmentsthrough crop diversification. Land Degradation and Development 19: 429-453.
109. Ramadan T. 1998. Ecophysiology of salt excretion in the xero-halophyte Reaumuria hirtella. New Phytologist 139: 273-281.
110. Ramadan T, Flowers TJ. 2004. Effects of salinity and benzyl adenine on development and function of microhairs of Zea mays L. Planta 219: 639-648.
111. Raven JA. 1985. Regulation of pH and generation of osmolarity in vascular plants -a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytologist 101: 25-77.
112. Rea PA, Poole RJ. 1993. Vacuolar H+-translocating pyrophosphatase. Annual Review of Plant Physiology and Plant Molecular Biology 44: 157-180.
113. Redondo-Gomez S, Mateos-Naranjo E, Davy AJ, et aL. 2007. Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Annals of Botany 100: 555-563.
114. RengasamyP. 2002.Transient salinityand subsoil constraints to dryland farming in Australian sodic soils: An overview. Australian Journal of Experimental Agriculture 42: 351-361.
115. Rengasamy P. 2006.World salinization with emphasis on Australia. Journal of Experimental Botany 57: 1017-1023.
116. Repo-Carrasco R, Espinoza C, Jacobsen SE. 2003. Nutritional value and use of the Andean crops quinoa (Chenopodium quinoa) and kaniwa (Chenopodium pallidicaule). Food Reviews International 19: 179-189.
117. Riadh K,Wided M, Koyro H-W, Chedly A. 2010. Responses of halophytes to environmental stresses with special emphasis to salinity. Advances in Botanical Research 53: 117-145.
118. RobinsonMF.1996. Sodium-induced stomatal closure in the maritime halophyte Aster tripolium (L.). PhD Thesis, Lancaster University, UK.
119. Rodriguez-Rosales MP, Jiang XY, Galvez FJ, Aranda MN, Cubero B, Venema K. 2008. Overexpression of the tomato K+/H+ antiporter LeNHX2confers salt tolerance by improving potassium compartmentalization. New Phytologist 179: 366-377.
120. Rozema J,GudeH, BijlF,Wesselman H. 1981. Sodium concentration in xylem sap in relation to ion exclusion, accumulation and secretion in halophytes. Acta Botanica Neerlandica 30: 309-311.
121. Ruan CJ, da Silva JAT, Mopper S, Qin P, Lutts S. 2010. Halophyte improvement for a salinized world. Critical Reviews in Plant Sciences 29: 329-359.
122. Schwab B, Mathur J, Saedler RR, et aL. 2003. Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: Actin controls the spatial organization of microtubules. Molecular Genetics and Genomics 269: 350-360.
123. Serna L, Fenoll C. 1997. Stomata pattern in Arabidopsis is modulated by ethylene. Plant Physiology 114: 280-280.
124. Serna L, Fenoll C. 2000. Stomatal development and patterning in Arabidopsis leaves. Physiologia Plantarum 109: 351-358
125. Serna L. 2009. Cell fate transitions during stomatal development. Bioessays 31: 865-873.
126. Shabala S. 2012. Plant stress physiology.Wallingford, UK: CAB InternationaL.
127. Shabala S, Cuin TA. 2008. Potassium transport and plant salt tolerance. Physiologia Plantarum 133: 651-669.
128. Shabala S,Mackay A. 2011. Ion transport in halophytes. Advances in Botanical Research 57: 151-199.
129. Shabala S, Shabala L. 2011. Ion transport and osmotic adjustment in plants and bacteria. BioMolecular Concepts 2: 407-419.
130. Shabala S, Babourina O, Newman I. 2000. Ion-specific mechanisms of osmoregulation in bean mesophyll cells. Journal of Experimental Botany 51: 1243-1253.
131. Shabala S, Cuin TA, Prismall L, Nemchinov LG. 2007. Expression of animal CED-9anti-apoptotic gene in tobacco modifies plasmamembrane ion fluxes in response to salinity and oxidative stress. Planta 227: 189-197.
132. Shabala S, CuinTA,PangJY, et aL. 2010. Xylem ionic relations and salinity tolerance in barley. The Plant Journal 61: 839-853.
133. Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou DW, Shabala S. 2012. Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiologia Plantarum 146: 26-38.
134. Shabala S, HariadiY, Jacobsen S-E. 2013. Genotypic difference in salinity tolerance in quinoa (Chenopodium quinoa) is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology 170: 906-914.
135. ShiHZ,Quintero FJ,PardoJM,ZhuJK. 2002. Theputative plasmamembrane Na+/H+antiporterSOS1controls long-distanceNa+transport in plants. The Plant Cell 14: 465-477.
136. Soliz D, Glenn EP, Seaman R, Yoklic M, Nelson SG, Brown P. 2011. Water consumption, irrigation efficiency and nutritional value of Atriplex lentiformis grownon reverse osmosis brine in a desert irrigation district. Agriculture Ecosystems and Environment 140: 473-483.
137. Storey R, Wynjones RG. 1979. Responses of Atriplex spongiosa and Suaeda monoica to salinity. Plant Physiology 63: 156-162.
138. Storey R. 1995. Salt tolerance, ion relations and the effect of root medium on the response of citrus to salinity. Australian Journal of Plant Physiology 22: 101-114.
139. Sugimoto-Shirasu K, Roberts K. 2003. 'Big it up': endoreduplication and cellsize control in plants. Current Opinion in Plant Biology 6: 544-553.
140. Thomas JC, Malick FK, Endreszl C, Davies EC, Murray KS. 1998. Distinct responses to copper stress in the halophyte Mesembryanthemum crystallinum. Physiologia Plantarum, 102: 360-368.
141. ThomsonWW, Faraday CD, Oross JW. 1988. Salt glands. In: Baker DA, Hall JL. eds. Solute transport in plant cells and tissues. Harlow, UK: Longman, 498-537.
142. Tominaga-Wada R, Ishida T,Wada T. 2011. New insights into the mechanism of development of arabidopsis root hairs and trichomes. International Review of Cell and Molecular Biology 286: 67-106.
143. TrawMB,Bergelson J. 2003. Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology 133: 1367-1375.
144. Ueda A, Kanechi M, Uno Y, Inagaki N. 2003. Photosynthetic limitations of a halophyte sea aster (Aster tripolium L) under water stress and NaCl stress. Journal of Plant Research 116: 65-70.
145. Valentine J, Clifton-Brown J, Hastings A, Robson P, Allison G, Smith P. 2012. Food vs. fuel: the use of land for lignocellulosic 'next generation' energy crops that minimize competition with primary food production. Global Change Biology Bioenergy 4: 1-19.
146. Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O. 1999. Salt stress in Mesembryanthemum crystallinum L cell suspensions activates adaptive mechanisms similar to those observed in the whole plant. Planta 207: 426-435.
147. Vera-Estrella R, Barkla BJ, Garcia-Ramirez L, Pantoja O. 2005. Salt stress in Thellungiella halophila activates Na+ transport mechanisms required for salinity tolerance. Plant Physiology 139: 1507-1517.
148. Very AA, Robinson MF, Mansfield TA, Sanders D. 1998. Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. The Plant Journal 14: 509-521.
149. Wang BS, Luttge U, Ratajczak R. 2001. Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. Journal of Experimental Botany 52: 2355-2365.
150. Watson MC, O'Leary JW. 1993. Performance of Atriplex species in the San Joaquin valley, California, under irrigation and with mechanical harvests. Agriculture Ecosystems and Environment 43: 255-266.
151. Wegner LH, De Boer AH. 1997. Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and longdistance signaling. Plant Physiology 115: 1707-1719.
152. Wegner LH, Raschke K. 1994. Ion channels in the xylem parenchyma of barley roots -a procedure to isolate protoplasts from this tissue and a patch-clamp exploration of salt passageways into xylem vessels. Plant Physiology 105: 799-813.
153. Wegner LH, Stefano G, Shabala L, Rossi M, Mancuso S, Shabala S. 2011. Sequential depolarization of root cortical and stelar cells induced by an acute salt shock -implications for Na+ and K+ transport into xylem vessels. Plant, Cell and Environment 34: 859-869.
154. Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B. The SbSOS1 gene from the extremehalophyte Salicornia brachiata enhancesNa+loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biology 12: 188.
155. Zeiger E. 1983. The biology of stomatal guard cells. Annual Review of Plant Physiology 34: 441-473.
156. Zhang HX, Blumwald E. 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19: 765-768.
157. Zhang HX, Hodson JN, Williams JP, Blumwald E. 2001. Engineering salttolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proceedings of the National Academy of Sciences, USA 98: 12832-12836.
158. Zhao JS, Zhi DY, Xue ZY, Liu H, Xia GM. 2007. Enhanced salt tolerance of transgenic progeny of tall fescue (Festuca arundinacea) expressing a vacuolar Na+/H+ antiporter gene fromArabidopsis. Journal of Plant Physiology 164: 1377-1383.
159. Zhao KF. 1991. Desalinization of saline soils by Suaeda salsa. Plant and Soil 135: 303-305.