Deploying Mechanisms Adapted by Halophytes to Improve Salinity Tolerance in Crop Plants: Focus on Anatomical Features, Stomatal Attributes, and Water Use Efficiency

  • Ankanagari Srinivas
  • Guddimalli Rajasheker
  • Gandra Jawahar
  • Punita L. Devineni
  • Maheshwari Parveda
  • Somanaboina Anil Kumar
  • Polavarapu B. Kavi Kishor


Nearly 1200 million hectares of land is affected by salinity throughout the world, and it is increasing year after year. It is one of the major causes that threaten our crop productivity at a time when we need to meet our growing food demands with limited land and freshwater resources. This leaves us but to understand the complex salinity tolerance mechanisms adapted by halophytic species especially their stomatal conductance (gs), epidermal salt bladders, and water use efficiency (WUE) and to utilize the candidate genes associated with them in crop plants for better tolerance and crop productivity.


Bulliform or motor cells Cation channels Epidermal bladder cells Glycophytes Halophytes Lignified cells Salt bladders Salt hairs Salt secretion Secretory cells Stomatal attributes Stomatal patchiness Successive cambia Trichome patterning Water use efficiency 



Abscisic acid


Crassulacean acid metabolism


Cation-chloride cotransporter


Cyclic nucleotide-gated channels


Epidermal bladder cells




Stomatal conductance


High-affinity potassium transporter


Potassium-efflux antiporter


Potassium inward-rectifying channel


Potassium outward-rectifying channel


Potassium uptake


Nicotinamide adenine dinucleotide phosphate (reduced)


Nonselective cation channels


Plasma membrane intrinsic protein


Reactive oxygen species




Specific leaf area


Salt overly sensitive


Tonoplast intrinsic protein


Water use efficiency



The research activities in the laboratory of Dr. AS supported by DST-PURSE, DST-FIST, and UGC-CAS, New Delhi, are gratefully acknowledged. PBK gratefully acknowledges the CSIR, New Delhi, for providing the Emeritus Scientist Fellowship.


  1. Aasamaa K, Sober A (2001) Hydraulic conductance and stomatal sensitivity to changes of leaf water status in six deciduous tree species. Biologia Plant 44:65–73. CrossRefGoogle Scholar
  2. Abd Elhalim ME, Abo-Alatta OK, Habib SA, Abd Elbar Ola H (2016) The anatomical features of the desert halophytes Zygophyllum album L.F. and Nitraria retusa (Forssk.) Asch. Ann Agric Sci 61:97–104. Google Scholar
  3. Adolf VI, Shabala S, Andersen MN, Razzaghi F, Jacobsen SE (2012) Varietal differences of quinoa’s tolerance to saline conditions. Plant Soil 357:117–129. CrossRefGoogle Scholar
  4. Albert R, Popp M (1977) Chemical composition of halophytes from the Neusiedler Lake region in Austria. Ecologia (Berl) 27:157–170. CrossRefGoogle Scholar
  5. Aslam R, Bostan N, Amen N, Maria M, Safdar W (2011) A critical review on halophytes: salt tolerant plants. J Med Plants Res 5:7108–7118. Google Scholar
  6. Balnokin YV, Kurkova EB, Myasoedov NA, Bukhov NG (2004) Structural and functional state of thylakoids in a halophyte Suaeda altissima before and after disturbance of salt-water balance by extremely high concentrations of NaCl. Russ J Plant Physiol 51:815–821. CrossRefGoogle Scholar
  7. 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. Russ J Plant Physiol 52:779–787. CrossRefGoogle Scholar
  8. Barkla BJ, Vera-Estrella R (2015) Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum. Front Plant Sci.
  9. Barrett-Lennard EG, Setter TL (2010) Developing saline agriculture: moving from traits and genes to systems. Funct Plant Biol 37(7).
  10. Barton KA, Schattat MH, Jakob T, Hause G, Wilhelm C, Mckenna JF, Máthé C, Runions J, Van Damme D, Mathur J (2016) Epidermal pavement cells of Arabidopsis have chloroplasts. Plant Physiol 171:723–726. PubMedGoogle Scholar
  11. Benz BW, Martin CE (2006) Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). J Plant Physiol 163:648–656. CrossRefPubMedGoogle Scholar
  12. Beyschlag W, Eckstein J (2001) Towards a causal analysis of stomatal patchiness: the role of stomatal size variability and hydrological heterogeneity. Acta Oecologica-Int J Ecol 22:161–173. CrossRefGoogle Scholar
  13. Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendia A, Massart A, Poschenrieder C, Hariadi Y, Shbala S (2014) 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 Environ 37:589–600. CrossRefPubMedGoogle Scholar
  14. Boughalleb F, Denden M, Ben Tiba B (2009) Photosystem II photochemistry and physiological parameters of three fodder shrubs, Nitraria retusa, Atriplex halimus, and Medicago arborea under salt stress. Acta Physiol Plant 31:463–476. CrossRefGoogle Scholar
  15. Breckle SW (1990) Salinity tolerance of different halophyte types. In: Bassam NE, Dambroth M, Loughman BC (eds) Genetic aspects of plant mineral nutrition. Springer, Berlin, pp 167–175. CrossRefGoogle Scholar
  16. Breckle SW (1995) How do halophyte overcome salinity? Biology of salt tolerant plants. In: Khan MA, Ungar IA (eds) Chelsca, pp 199–213Google Scholar
  17. Bucur N, Dobrescu C, Turcu GH, Lixandru GH, Tesu C, Dumbrava I, Afusoaie (1957) Contributii la studiul halofiliei plantelor din pasuni si fanete de saratura din Depresiunea Jijia-Bahlui (parten a I-a). Stud. Si Cerc. (Biol. Si St. Agric.) Acad. R.P. Romane, filial Iasi 8:277–317Google Scholar
  18. Céccoli G, Ramos J, Pilatti V, Dellaferrera I, Tivano JC, Taleisnik E, Vegetti AC (2015) Salt glands in the Poaceae family and their relationship to salinity tolerance. Bot Rev 81:162–178. CrossRefGoogle Scholar
  19. Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H, Nasholm T (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1585. CrossRefPubMedGoogle Scholar
  20. Churchman ML, Brown ML, Kato N, Kirik V, Hulskamp M, Inze D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, Gwin T, Churchman J, Larkin JC (2006) SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18:3145–3157. PubMedCentralCrossRefPubMedGoogle Scholar
  21. Claudia T, Murray DR (2000) Effects of elevated atmospheric [CO2] in Panicum species of different photosynthetic modes (Poaceae: Panicoideae). In: Jacobs SWL, Everett J (eds) Grasses: systematics and evolution. CSIRO Publishing, Collingwood, pp 259–266Google Scholar
  22. Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45(11):1425.
  23. Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumos J, Talon M (2007) Identification and functional characterization of cation–chloride cotransporters in plants. Plant J 50:278–292. CrossRefPubMedGoogle Scholar
  24. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 414:758–769. Google Scholar
  25. Cutler DF, Botha T, Stevenson DW (2007) Plant Anatomy- An applied approach. Blackwell Publishing, Australia.
  26. Dang ZH, Zheng LL, Wang J, Gao Z, Wu SB, Qi Z, Qi Z, Wang YC (2013) Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna. BMC Genomics 14:29. PubMedCentralCrossRefPubMedGoogle Scholar
  27. Dang ZH, Qi Q, Zhang HR, Yu LH, Wu SB, Wang YC (2014) Identification of salt-stress-induced genes from the RNA-Seq data of Reaumuria trigyna using differential-display reverse transcription PCR. Int J Genomics 381501.
  28. Dassanayake M, Larkin JC (2017) Making plants break a sweat: the structure, function, and evolution of plant salt glands. Front Plant Sci 8:406. PubMedCentralPubMedGoogle Scholar
  29. Delgado D, Alonso-Blanco C, Fenoll C, Mena M (2011) Natural variation in stomatal abundance of Arabidopsis thaliana includes cryptic diversity for different developmental processes. Ann Bot 107:1247–1258. PubMedCentralCrossRefPubMedGoogle Scholar
  30. Delpire E, Mount DB (2002) Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu Rev Physiol 64:803–843. CrossRefPubMedGoogle Scholar
  31. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+ −efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479. CrossRefPubMedGoogle Scholar
  32. Deng Y, Feng Z, Yuan F, Guo J, Suo S, Wang B (2015) Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands. Plant Physiol Biochem 97:20–27. CrossRefPubMedGoogle Scholar
  33. Dickison WC (2000) Integrative plant anatomy. Harcourt Academic Press, New YorkGoogle Scholar
  34. Dschida W, Platt-Aloia K, Thomson W (1992) Epidermal peels of Avicennia germinans (L.) Stearn: a useful system to study the function of salt glands. Ann Bot 70:501–509. CrossRefGoogle Scholar
  35. Duval-Jouve J (1871) Sur quelques tissus de Joncées, de Cyperacées et de Graminées. Bull Soc Bot Fr 18:231–239CrossRefGoogle Scholar
  36. Edwards D, Kerp H, Hass H (1998) Stomata in early land plants: an anatomical and ecophysiological approach. J Exp Bot 49:255–278. CrossRefGoogle Scholar
  37. Ehleringer JR, Forseth I (1980) Solar tracking by plants. Science 210:1094–1098. CrossRefPubMedGoogle Scholar
  38. Ehleringer J, Björkman O, Mooney HA (1976) Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science 191:376–377. CrossRefGoogle Scholar
  39. Esau K (1965) Plant anatomy. Wiley, New YorkGoogle Scholar
  40. Feng Z, Sun Q, Deng Y, Sun S, Zhang J, Wang B (2014) Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor. Acta Physiol Plant 36:2729–2741. CrossRefGoogle Scholar
  41. Feng Z, Deng Y, Zhang S, Liang X, Yuan F, Hao J et al (2015) K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS. Plant Sci 238:286–296. CrossRefPubMedGoogle Scholar
  42. Flowers TJ (1985) Physiology of halophytes. Plant Soil 89:41–56. CrossRefGoogle Scholar
  43. Flowers TJ, Colmer TD (2008) Flooding tolerance in halophytes. New Phytol 179:964–974. CrossRefPubMedGoogle Scholar
  44. Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331. PubMedCentralCrossRefPubMedGoogle Scholar
  45. Flowers TJ, Troke P, Yeo A (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121. CrossRefGoogle Scholar
  46. Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37:604–612. CrossRefGoogle Scholar
  47. Gan Y, Kumimoto R, Liu C, Ratcliffe O, Yu H, Broun P (2006) Glabrous inflorescence stems modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18:1383–1395. PubMedCentralCrossRefPubMedGoogle Scholar
  48. Glover BJ (2000) Differentiation in plant epidermal cells. J Exp Bot 51:497–505. CrossRefPubMedGoogle Scholar
  49. Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Ann Rev Plant Physiol 31:149–190. CrossRefGoogle Scholar
  50. Grigore M (2008) Introducere în Halofitologie. Elemente de anatomie integrativ. Edit. Pim. Ia. pp 3–28Google Scholar
  51. Grigore MN, Toma C, Boscaiu M (2010) Ecological implications of bulliform cells on halophytes in salt and water stress natural conditions. An. Şt. Univ., Al. I. Cuza” Iaşi, s. II, a. (Biol. Veget.) 56:5–15Google Scholar
  52. Hou XY (1982) Botanical geography and chemical ingredients of dominant plant species in China. Science, Beijing. (in Chinese)Google Scholar
  53. Hughes FM Jr, Cidlowski JA (1999) Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Adv Enzyme Reg 39:157–171. CrossRefGoogle Scholar
  54. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Ann Rev Plant Biol 59:365–386. CrossRefGoogle Scholar
  55. Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258. CrossRefGoogle Scholar
  56. 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. Biol Plant 49:301–304. CrossRefGoogle Scholar
  57. Kemp PR, Cunningham GL (1981) Light, temperature and salinity effects on growth, leaf anatomy and photosynthesis of Distichlis spicata (L) green. Am J Bot 68:507–516. CrossRefGoogle Scholar
  58. Kobayashi H, Masaoka Y, Takahashi Y, Ide Y, Sato S (2007) Ability of salt glands in Rhodes grass (Chloris gayana Kunth) to secrete Na+ and K+. Soil Sci Plant Nutr 53:764–771. CrossRefGoogle Scholar
  59. Liphschitz N, Adiva-Shomer-Ilan, Eshel A, Waisel Y (1974) Salt glands on leaves of Rhodes grass (Chloris gayana Kth.) Ann Bot 38:459–462. CrossRefGoogle Scholar
  60. Lovelock CE, Ball MC (2002) Influence of salinity on photosynthesis of halophytes. In: Lauchli A, Luttge U (eds) Salinity: environment-plants-molecules. Springer, Dordrecht, pp 315–339. Google Scholar
  61. 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 salt accumulating halophyte Suaeda altissima. Russian J Plant Physiol 52:635–644. CrossRefGoogle Scholar
  62. Ma H, Tian C, Feng G, Yuan J (2011) Ability of multicellular salt glands in Tamarix species to secrete Na+ and K+ selectively. Sci China Life Sci 54:282–289. CrossRefPubMedGoogle Scholar
  63. Marius-Nicusor G, Constantin T (2010) A proposal for a new halophytes classification based on integrative anatomy observations. Muz. Olteniei, Craiova, Stud. şi Com., Şt. Nat 26:45–50.Google Scholar
  64. Marschner H (1995) Mineral nutrition of higher plants. San Diego, Academic Press, USA.
  65. Martin C, Glover BJ (2007) Functional aspects of cell patterning in aerial epidermis. Curr Opin Plant Biol 10:70–82. CrossRefPubMedGoogle Scholar
  66. Martinez JP, Kinet JM, Bajji M, Lutts S (2005) NaCl alleviates polyethylene glycol-induced water stress in the halophyte species Atriplex halimus L. J Exp Bot 56:2421–2431. CrossRefPubMedGoogle Scholar
  67. Millar J, Roots J (2012) Changes in Australian agriculture and land use: implications for future food security. Int J Agric Sustain 10:25–39Google Scholar
  68. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19. CrossRefPubMedGoogle Scholar
  69. Mott KA, Peak D (2007) Stomatal patchiness and task-performing networks. Ann Bot 99:219–226. CrossRefPubMedGoogle Scholar
  70. 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. CrossRefGoogle Scholar
  71. Niu X, Narasimhan ML, Salzman RA, Bressan RA, Hasegawa PM (1993) NaCl regulation of plasma membrane H+-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol 103:713–718. PubMedCentralCrossRefPubMedGoogle Scholar
  72. Niu X, Damsz B, Kononowicz AK, Bressan RA, Hasegawa PM (1996) NaCl-induced alterations in both cell structure and tissue-specific plasma membrane H+-ATPase gene expression. Plant Physiol 111:679–686. PubMedCentralCrossRefPubMedGoogle Scholar
  73. Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61:1205–1213. PubMedCentralCrossRefPubMedGoogle Scholar
  74. Oh DH, Barkla BJ, Vera-Estrella R, Pantoja O, Lee SY, Bohnert HJ, Dassanayake M (2015) Cell type-specific responses to salinity-the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum. New Phytol 207:627–644. CrossRefPubMedGoogle Scholar
  75. Omami EN, Hammes PS, Robbertse PJ (2006) Differences in salinity tolerance for growth and water-use efficiency in some amaranth (Amaranthus spp.) genotypes. New Zealand J Crop Hort Sci 34:11–22. CrossRefGoogle Scholar
  76. Orsini F, Matilde Paino D'Urzo F, Inan G, Serra S, Oh D, Mickelbart MV, Consiglio F, Xia Li X, Jeong JC, Yun DJ, Bohnert HJ, Bressan RA, Maggio A (2010) A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana. J Exp Bot 61:3787–3798. PubMedCentralCrossRefPubMedGoogle Scholar
  77. Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Ruiz Carrasco KB, Martinez EA, Alnayef M, Marotti I, Bosi S, Biondi S (2011) Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol 38:818–831. CrossRefGoogle Scholar
  78. Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311. CrossRefGoogle Scholar
  79. Pallaghy CK (1970) The effect of Ca2+ on the ion specificity of stomatal opening in epidermal strips of Vicia faba. Z Pflanzenphysiol 62:58–62Google Scholar
  80. Pan Y, Guo H, Wang S, Zhao B, Zhang J, Ma Q, Yin HJ, Bao AK (2016) The photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens in response to salinity. Front Plant Sci 7:848. PubMedCentralPubMedGoogle Scholar
  81. Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:351. PubMedCentralCrossRefPubMedGoogle Scholar
  82. Patrut DI, Adelina P, Ioan C (2005) Biodiversitatea halofitelor din Campia Banatului. Edit, Eurobit, TimisoaraGoogle Scholar
  83. 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 Environ 17:335–340. CrossRefGoogle Scholar
  84. Perera LKRR, De Silva DLR, Mansfield TA (1997) Avoidance of sodium accumulation by the stomatal guard cells of the halophyte Aster tripolium. J Exp Bot 48:707–717. CrossRefGoogle Scholar
  85. Peterson PM (2000) Systematics of the Muhlenbergiinae (Poaceae: Eragrostidae). In: Jacobs SWL, Everett J (eds) Grasses: systematics and evolution. CSIRO Publishing, Collingwood, pp 195–212Google Scholar
  86. 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 Mol Biol 51:773–787. CrossRefPubMedGoogle Scholar
  87. Popp M, Polania J, Weiper M (1993) Physiological adaptations to different salinity levels in mangrove. In: Lieth H, Al Masoom A (eds) Towards the rational use of high salinity tolerant plants, vol 1. Kluwer Academic Publisher, Dordrecht, pp 217–224. CrossRefGoogle Scholar
  88. Pospisilova J, Santrucek J (1994) Stomatal patchiness. Biologia Plant 36:481–510. CrossRefGoogle Scholar
  89. Quarrie SA, Jones HG (1977) Effects of abscisic acid and water stress on development and morphology of wheat. J Exp Bot 28:192–203. CrossRefGoogle Scholar
  90. Rajput KS (2016) Development of successive cambia and wood structure in stem of Rivea hypocriteriformis (Convolvulaceae). Polish Bot J 61:89–98. Google Scholar
  91. Rajput KS, Marcati CR (2013) Stem anatomy and development of successive cambia in Hebanthe eriantha (Poir.) Pedersen: a neotropical climbing species of the Amaranthaceae. Plant Systematic Evol 299:1449–1459. CrossRefGoogle Scholar
  92. Ramadan T (1998) Ecophysiology of salt excretion in the xero-halophyte Reaumuria hirtella. New Phytol 139:273–281. CrossRefGoogle Scholar
  93. Ramadan T, Flowers TJ (2004) Effects of salinity and benzyl adenine on development and function of micro hairs of Zea mays L. Planta 219:639–648. CrossRefPubMedGoogle Scholar
  94. Reginato M, Reinoso H, Llanes AS, Luna MV (2013) Stomatal abundance and distribution in Prosopis strombulifera plants growing under different iso-osmotic salt treatments. American J Plant Sci 4:80–90. CrossRefGoogle Scholar
  95. Robert EMR, Schmitz N, Boeren I, Driessens T, Herremans K, De Mey J, Van de Casteele E, Beeckman H, Koedam N (2011) Successive cambia: a developmental oddity or an adaptive structure? PLoS one 6(1):e16558. PubMedCentralCrossRefPubMedGoogle Scholar
  96. Robinson MF (1996) Sodium-induced stomatal closure in the maritime halophyte Aster tripolium (L.). Lancaster University U.K, Ph.D. Thesis.Google Scholar
  97. Sabovljevic M, Sabovljevic A (2007) Contribution to the coastal bryophytes of the Northern Mediterranean: are there halophytes among bryophytes? Phytol Balcanica 13:131–135Google Scholar
  98. Sanadhya P, Agarwal P, Khedia J, Agarwal PK (2015) A low-affinity K+ transporter AlHKT2; 1 from recretohalophyte Aeluropus lagopoides confers salt tolerance in yeast. Mol Biotechnol 57:489–498. CrossRefPubMedGoogle Scholar
  99. Santos J, Al-Azzawi M, Aronson J, Flowers TJ (2016) eHALOPH a database of salt-tolerant plants: helping put halophytes to work. Plant Cell Physiol 57:e10. CrossRefPubMedGoogle Scholar
  100. Serna L (2009) Cell fate transitions during stomatal development. BioEssays 31:865–873. CrossRefPubMedGoogle Scholar
  101. Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221. PubMedCentralCrossRefPubMedGoogle Scholar
  102. Shabala S, Mackay A (2011) Ion transport in halophytes. Adv Bot Res 57:151–199. CrossRefGoogle Scholar
  103. Shabala S, Babourina O, Newman I (2000) Ion-specific mechanisms of osmoregulation in bean mesophyll cells. J Exp Bot 51:1243–1253. CrossRefPubMedGoogle Scholar
  104. 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). Physiol Plant 146:26–38. CrossRefPubMedGoogle Scholar
  105. Shabala L, Hariadi Y, Jacobsen SE (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. J Plant Physiol 170:906–914. CrossRefPubMedGoogle Scholar
  106. Shabala S, Bose J, Hedrich R (2014) Salt bladders: do they matter? Trends Plant Sci 19:687–691. CrossRefPubMedGoogle Scholar
  107. Shi HZ, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477. PubMedCentralCrossRefPubMedGoogle Scholar
  108. Shtein I, Shelef Y, Marom Z, Zelinger E, Schwartz A, Popper ZA, Bar-On B, Harpaz-Saad S (2017) Stomatal cell wall composition: distinctive structural patterns associated with different phylogenetic groups. Ann Bot 119:1021–1033. PubMedCentralCrossRefPubMedGoogle Scholar
  109. Sobrado MA, Greaves ED (2000) Leaf secretion composition of the mangrove species Avicennia germinans (L.) in relation to salinity: a case study by using total-reflection X-ray fluorescence analysis. Plant Sci 159:1–5. CrossRefPubMedGoogle Scholar
  110. Spence RD, Wu H, Sharpe PJ, Clark K (1986) Water stress effects on guard cell anatomy and the mechanical advantage of the epidermal cells. Plant Cell Environ 9:197–202. Google Scholar
  111. Steiner M (1934) To the ecology of the salt march of the Nordostlichen united countries of Nordamerika. Jahrb Know Offered 81:94Google Scholar
  112. Tamaio N, Cardoso-Vieira R, Angyalossy V (2009) Origin of successive cambia on stem in three species of Menispermaceae. Rev Bras Bot 32:839–848. CrossRefGoogle Scholar
  113. Tan WK, Lim TM, Loh CS (2010) A simple, rapid method to isolate salt glands for three-dimensional visualization, fluorescence imaging and cytological studies. Plant Methods 6:24. PubMedCentralCrossRefPubMedGoogle Scholar
  114. Tan WK, Lin Q, Lim TM, Kumar P, Loh CS (2013) Dynamic secretion changes in the salt glands of the mangrove tree species Avicennia officinalis in response to a changing saline environment. Plant Cell Environ 36:1410–1422. CrossRefPubMedGoogle Scholar
  115. Terrazas T, Aguilar-Rodríguez S, Ojanguren CT (2011) Development of successive cambia, cambial activity, and their relationship to physiological traits in Ipomoea arborescens (Convolvulaceae) seedlings. Am J Bot 98:765–774. CrossRefPubMedGoogle Scholar
  116. Tester M (1988) Blockade of potassium channels in the plasmalemma of Chara corallina by tetraethylammonium, Ba2+, Na+ and Cs+. J Membrane Biol 105:77–85.
  117. Thiel G, Blatt MR (1991) The mechanism of ion permeation through K+ channels of stomatal guard cells: voltage-dependent block by Na+. J Plant Physiol 138:326–334. CrossRefGoogle Scholar
  118. Thomson W, Platt-Aloia K (1985) The ultrastructure of the plasmodesmata of the salt glands of Tamarix as revealed by transmission and freeze-fracture electron microscopy. Protoplasma 125:13–23. CrossRefGoogle Scholar
  119. Thomson WW, Faraday CD, Oross JW (1988) Salt glands. In: Baker DA, Hall JL (eds) Solute transport in plant cells and tissues. Longman, Harlow, pp 498–537Google Scholar
  120. Topa E (1939) Vegetatia halofitelor din nordul Romaniei in legatura cu cea din restul tarii. Teza presentata la Facultatea de Stiinte din Cernauti pentru obtinerea titlului de doctor in Stiintele NaturaleGoogle Scholar
  121. Tsiantis MS, Bartholomew DM, Smith JA (1996) Salt regulation of transcript levels for the c subunit of a leaf vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum. Plant J 9:729–736. CrossRefPubMedGoogle Scholar
  122. Ungar IA (1978) Halophyte seed germination. Bot Rev 44:233–364CrossRefGoogle Scholar
  123. van Eijk M (1939) Analyse der Wirkung des NaCl auf die Entwicklung Sukkulenze und Transpiration bei Salicornia herbacea, sowie Untersuchungen über den Einfluss der Salzaufnahme, auf die Wurzelatmung bei Aster tripolium. Rec Trav Bot Neerl 36:559–657Google Scholar
  124. Véry AA, Robinson MF, Mansfield TA, Sanders D (1998) Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. Plant J 14:509–521. CrossRefGoogle Scholar
  125. Vijayan K, Chakraborti SP, Ercisli S, Ghosh PD (2008) NaCl induced morpho-biochemical and anatomical changes in mulberry (Morus spp.) Plant Growth Regul 56:61–69. CrossRefGoogle Scholar
  126. Weber DJ (2009) Adaptive mechanisms of halophytes in desert regions. In: Ashraf M, Ozturk M, Athar H (eds) Salinity and water stress. Tasks for vegetation sciences, vol 44. Springer, Dordrecht. Google Scholar
  127. Wegner LH, De Boer AH (1997) Properties of two outward-rectifying channels in root xylem parenchyma cells suggest a role in K+ homeostasis and long distance signaling. Plant Physiol 115:1707–1719. PubMedCentralCrossRefPubMedGoogle Scholar
  128. 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 Physiol 105:799–813. PubMedCentralCrossRefPubMedGoogle Scholar
  129. Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325. PubMedCentralCrossRefPubMedGoogle Scholar
  130. Yan L, Li H, Liu Y (2002) The anatomical ecology studies on the leaf of 13 species in Caragana genus. J Arid Land Resour Environ 16:100–106Google Scholar
  131. Yang HM, Wang GX (2001) Leaf stomatal densities and distribution in Triticum aestivum under drought and CO2 enrichment. Acta Phytoecologica Sin 25:312–316Google Scholar
  132. Yensen NP, Biel KY (2006) Soil remediation via salt-conduction and the hypotheses of halosynthesis and photoprotection. Tasks for Vegetation Science. Series-40. Ecophysiology of High Salinity Tolerant Plants. pp 313–344.
  133. Youssef AM (2009) Salt tolerance mechanisms in some halophytes from Saudi Arabia and Egypt. Res J Agr Biol Sci 5:623–638Google Scholar
  134. Yuan F, Chen M, Leng BY, Wang B (2013) An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion. S Afr J Bot 88:110–117. CrossRefGoogle Scholar
  135. Yuan F, Lyu MA, Leng B, Zheng GY, Feng ZT, Li P, Zhu XG, Wang BS (2015) Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ 38:1637–1657. CrossRefPubMedGoogle Scholar
  136. Yuan F, Lyu MJA, Leng BY, Zhu XG, Wang BS (2016) The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Mol Biol 91:241–256. CrossRefPubMedGoogle Scholar
  137. Zeiger E (1983) The biology of stomatal guard cells. Ann Rev Plant Physiol 34:441–474. CrossRefGoogle Scholar
  138. Zhang YP, Wang ZM, Wu YC, Zhang X (2006) Stomatal characteristics of different green organs in wheat under different irrigation regimes. Acta Agron Sin 32:70–75Google Scholar
  139. Zhao KF, Li FZ (1999) Halophytes in China. Scientific, Beijing. (in Chinese)Google Scholar
  140. Zhao KF, Song J, Feng G, Zhao M, Liu JP (2011) Species, types, distribution, and economic potential of halophytes in China. Plant Soil 342:495–509. CrossRefGoogle Scholar
  141. Zouhaier B, Abdallah A, Najla T, Wahbi D, Wided C, Aouatef BA et al (2015) Scanning and transmission electron microscopy and X-ray analysis of leaf salt glands of Limoniastrum guyonianum Boiss. under NaCl salinity. Micron 78:1–9. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ankanagari Srinivas
    • 1
  • Guddimalli Rajasheker
    • 1
  • Gandra Jawahar
    • 1
  • Punita L. Devineni
    • 1
  • Maheshwari Parveda
    • 1
  • Somanaboina Anil Kumar
    • 1
  • Polavarapu B. Kavi Kishor
    • 1
  1. 1.Department of GeneticsOsmania UniversityHyderabadIndia

Personalised recommendations