Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Ionic and photosynthetic homeostasis in quinoa challenged by salinity and drought – mechanisms of tolerance

Fatemeh Razzaghi A C D , Sven-Erik Jacobsen B , Christian Richardt Jensen B and Mathias Neumann Andersen C
+ Author Affiliations
- Author Affiliations

A Water Engineering Department, College of Agriculture, Shiraz University, Iran.

B Department of Plant and Environmental Sciences, Faculty of Sciences, University of Copenhagen, Højbakkeggaard Allé 13, 2630 Taastrup, Denmark.

C Department of Agroecology, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, DK-8830 Tjele, Denmark.

D Corresponding authors. Emails: razzaghi@shirazu.ac.ir; razzaghi.f@gmail.com

Functional Plant Biology 42(2) 136-148 https://doi.org/10.1071/FP14132
Submitted: 3 May 2014  Accepted: 30 August 2014   Published: 8 October 2014

Abstract

Quinoa (Chenopodium quinoa Willd.) grown under field conditions was exposed to five irrigation water salinities (0, 10, 20, 30 and 40 dS m–1; 4 : 1 NaCl : CaCl2 molar ratio) from flowering, and divided between full irrigation and progressive drought (PD) during seed filling. Quinoa demonstrated homeostatic mechanisms which contributed to quinoa’s extraordinary tolerance. Salinity increased K+ and Na+ uptake by 60 and 100 kg ha–1, respectively, resulting in maintenance of cell turgor by osmotic adjustment, and a 50% increase of the leaf’s fresh weight (FW) : dry weight (DW) ratio and non-significant increase in elasticity enhanced crop water-capacitance. Day respiration (Rd) increased 2.7 times at high salinity but decreased 0.6 times during drought compared with control. Mesophyll conductance (gm) tended to be negatively affected by salinity as the increased succulence (FW : DW) possibly decreased intercellular space and increased cell-wall thickness. However, the increased K+ uptake seemed to alleviate biochemical limitations, as maximum Rubisco carboxylation rate (Vcmax) and photosynthetic electron transport (J) tended to increase under salinity. Overall, salinity and PD restricted stomatal conductance (gs) and photosynthesis (An) moderately, leading to decreased leaf internal to ambient [CO2], increase of intrinsic-water-use-efficiency (An/gs). The saturated electrical conductivity (ECe) resulting in 50% yield was estimated to be 25 dS m–1, reaching no yield at 51.5 dS m–1.

Additional keywords: intrinsic water use efficiency, ion uptake, mesophyll conductance, salinity threshold value, stomatal conductance.


References

Adolf VI, Shabala S, Andersen MN, Razzaghi F, Jacobsen S-E (2012) Varietal differences of quinoa’s tolerance to saline conditions. Plant and Soil 357, 117–129.
Varietal differences of quinoa’s tolerance to saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVegt7nN&md5=c4c07841ffd90d4edb17e670f7c3a0bbCAS |

Adolf VI, Jacobsen S-E, Shabala S (2013) Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.). Environmental and Experimental Botany 92, 43–54.
Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovVCgs7o%3D&md5=debdccc944700cce246c911543b3c263CAS |

Andersen MN, Jensen CR, Lösch R (1991) Derivation of pressure–volume curves by a non-linear regression procedure and determination of apoplastic water. Journal of Experimental Botany 42, 159–165.
Derivation of pressure–volume curves by a non-linear regression procedure and determination of apoplastic water.Crossref | GoogleScholarGoogle Scholar |

Awan AR, Chughtai MI, Ashraf MY, Mahmood K, Rizwan M, Akhtar M, Qureshi MAA, Siddiqui MT, Khan RA (2012) Comparison for physico-mechanical properties of farm-grown Eucalyptus camaldulensis Dehn with conventional timbers. Pakistan Journal of Botany 44, 2067–2070.

Ayers RS, Westcot DW (1976) ‘Water quality for agriculture. Irrigation and drainage paper, Paper 29.’ (Food and Agriculture Organization of the United Nations (FAO): Rome, Italy)

Barrett-Lennard EG (2002) Restoration of saline land through revegetation. Agricultural Water Management 53, 213–226.
Restoration of saline land through revegetation.Crossref | GoogleScholarGoogle Scholar |

Bartoli CG, Gomez F, Gergoff G, Guiamet JJ, Puntarulo S (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. Journal of Experimental Botany 56, 1269–1276.
Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVKmsbk%3D&md5=4b6b6a8cccdb5dd43efbe15876a80d82CAS | 15781442PubMed |

Bendevis M, Sun Y, Shabala S, Rosenqvist E, Liu F, Jacobsen S-E (2014) Differentiation of photoperiod induced ABA and soluble sugar responses of two quinoa (Chenopodium quinoa Willd.) cultivars. Journal of Plant Growth Regulation
Differentiation of photoperiod induced ABA and soluble sugar responses of two quinoa (Chenopodium quinoa Willd.) cultivars.Crossref | GoogleScholarGoogle Scholar |

Bonales-Alatorre E, Pottosin I, Shabala L, Chen Z-H, Zeng F, Jacobsen S-E, Shabala S (2013) Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. International Journal of Molecular Sciences 14, 9267–9285.
Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa.Crossref | GoogleScholarGoogle Scholar | 23629664PubMed |

Bosque Sanchez H, Lemeur R, Van Damme P, Jacobsen S-E (2003) Ecophysiological analysis of drought and salinity stress of quinoa (Chenopodium quinoa Willd.). Food Reviews International 19, 111–119.
Ecophysiological analysis of drought and salinity stress of quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar |

Bunce JA (2009) Use of the response of photosynthesis to oxygen to estimate mesophyll conductance to carbon dioxide in water-stressed soybean leaves. Plant, Cell & Environment 32, 875–881.
Use of the response of photosynthesis to oxygen to estimate mesophyll conductance to carbon dioxide in water-stressed soybean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jsLc%3D&md5=ab7892ad1a123182b073ee098e200879CAS |

Chaves MM (1991) Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42, 1–16.
Effects of water deficits on carbon assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFyntrw%3D&md5=be5b83a48b4282bc6b0f18767d2b9518CAS |

Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7s%3D&md5=a06bec980b7bade084536450bb0dec07CAS | 18662937PubMed |

Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiology 145, 1714–1725.
Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVCntbvP&md5=2bd360a35534ce471ea7f2d4029c4426CAS | 17965172PubMed |

Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Science 42, 122–131.
Improving intrinsic water-use efficiency and crop yield.Crossref | GoogleScholarGoogle Scholar | 11756262PubMed |

Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany 59, 2697–2706.
A root’s ability to retain K+ correlates with salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1WisLg%3D&md5=683fdd9da07e2a7346c3f2878a1f5a95CAS | 18495637PubMed |

de Jong van Lier Q, van Dam JC, Metselaar K (2009) Root water extraction under combined water and osmotic stress. Soil Science Society of America Journal 73, 862–875.

Delfine S, Alvino A, Zacchini M, Loreto F (1998) Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves. Australian Journal of Plant Physiology 25, 395–402.
Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVentbo%3D&md5=8d4064a04ae7e01d16f571ffb74bbff3CAS |

Dini I, Schettino O, Simioli T, Dini A (2001) Studies on the constituents of chenopodium quinoa seeds: isolation and characterization of new treterpene saponins. Journal of Agricultural and Food Chemistry 49, 741–746.
Studies on the constituents of chenopodium quinoa seeds: isolation and characterization of new treterpene saponins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFymtg%3D%3D&md5=eac44f88ddc30145eba733c872cb5b8eCAS | 11262022PubMed |

Draper NR, Smith H (1998) ‘Applied regression analysis.’ (3rd edn) (Wiley: New York)

Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology 29, 461–471.
Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations.Crossref | GoogleScholarGoogle Scholar |

Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 6, 269–279.
Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3ksVOlug%3D%3D&md5=7d142b7ea3e4d55721c556d5c0230445CAS | 15143435PubMed |

Flexas J, Diaz-Espejo A, Galmes J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell & Environment 30, 1284–1298.
Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFCgu7vL&md5=cd6f6e5af9416593a6e7e7231e30da43CAS |

Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
Mesophyll conductance to CO2: current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFehtbc%3D&md5=ad6d862d57cb993d28d80dc13c662f62CAS |

Flexas J, Barón M, Bota J, Ducruet J-M, Gallé A, Galmés J, Jiménez M, Pou A, Ribas-Carbó M, Sajnani C, Tomàs M, Medrano H (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri × V. rupestris). Journal of Experimental Botany 60, 2361–2377.
Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri × V. rupestris).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiurg%3D&md5=a60f59d68525dc5369a6d539b805c5e1CAS | 19351904PubMed |

Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Science 193–194, 70–84.
Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 22794920PubMed |

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
Improving crop salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1egtQ%3D%3D&md5=bf681f0dcb7040eccc0d9159397f3fa7CAS | 14718494PubMed |

Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytologist 174, 799–810.
Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery.Crossref | GoogleScholarGoogle Scholar | 17504463PubMed |

Galle A, Florez-Sarasa I, Tomas M, Pou A, Medrano H, Ribas-Carbo M, Flexas J (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? Journal of Experimental Botany 60, 2379–2390.
The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiur8%3D&md5=09bd7252eb490a799a4ce374acb9a62dCAS | 19321646PubMed |

Garcia M, Raes D, Jacobsen S-E (2003) Evapotranspiration analysis and irrigation requirements of quinoa (Chenopodium quinoa) in the Bolivian highlands. Agricultural Water Management 60, 119–134.
Evapotranspiration analysis and irrigation requirements of quinoa (Chenopodium quinoa) in the Bolivian highlands.Crossref | GoogleScholarGoogle Scholar |

Garcia M, Raes D, Jacobsen S-E, Michel T (2007) Agroclimatic constraints for rainfed agriculture in the Bolivian Altiplano. Journal of Arid Environments 71, 109–121.
Agroclimatic constraints for rainfed agriculture in the Bolivian Altiplano.Crossref | GoogleScholarGoogle Scholar |

Gattward JN, Almeide AAF, Souza JO, Gomes FP, Kronzucker HJ (2012) Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiologia Plantarum 146, 350–362.
Sodium-potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslaqsL3K&md5=ae83b8bb62a70188a79091b8d79c7715CAS | 22443491PubMed |

Geissler N, Hussin S, Koyro HW (2009) Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L. Journal of Experimental Botany 60, 137–151.
Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2qu70%3D&md5=dd8982f7d89b9e3d4b48edadcebf2db3CAS | 19036838PubMed |

Gómez-Pando LR, Àlvarez-Castro R, Equiluz-de la Barra A (2010) Effect of salt stress on Peruvian germplasm of Chenopodium quinoa Willd.: a promising crop. Journal Agronomy & Crop Science 196, 391–396.
Effect of salt stress on Peruvian germplasm of Chenopodium quinoa Willd.: a promising crop.Crossref | GoogleScholarGoogle Scholar |

González-Meler MA, Matamala R, Peñuelas J (1997) Effects of prolonged drought stress and nitrogen deficiency on the respiratory O2 uptake of bean and pepper leaves. Photosynthetica 34, 505–512.
Effects of prolonged drought stress and nitrogen deficiency on the respiratory O2 uptake of bean and pepper leaves.Crossref | GoogleScholarGoogle Scholar |

Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant, Cell & Environment 28, 834–849.
Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms12gsL0%3D&md5=904c1624fcd05f093ea80e006e0dfbc9CAS |

Greenway H (1962) Plant response to saline substrates. I. Growth and ion uptake of several varieties of Hordeum during and after sodium chloride treatment. Australian Journal of Biological Sciences 15, 16–38.

Haghighi Z, Karimi N, Modarresi M, Mollayi S (2012) Enhancement of compatible solute and secondary metabolites production in Plantago ovate Forsk. by salinity stress. Journal of Medicinal Plants Research 6, 3495–3500.

Haldimann P, Galle A, Feller U (2008) Impact of an exceptionally hot dry summer on photosynthetic traits in oak (Quercus pubescens) leaves. Tree Physiology 28, 785–795.
Impact of an exceptionally hot dry summer on photosynthetic traits in oak (Quercus pubescens) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVektbc%3D&md5=0b659b84e05d114ef8bf00aa3ba007c1CAS | 18316310PubMed |

Hariadi Y, Marandon K, Tian Y, Jacobsen S-E, Shabala S (2011) Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. Journal of Experimental Botany 62, 185–193.
Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurfM&md5=9e3b3b1bec1f4588502e1982f6b4f369CAS | 20732880PubMed |

Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60, 2303–2314.
Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiurs%3D&md5=cafb847c0282dace746264eea67b93bcCAS | 19286919PubMed |

Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress: a halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiology 135, 1718–1737.
Salt cress: a halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqsbg%3D&md5=26fd44ce72133a4f8a79cc5c1e1aa3c0CAS | 15247369PubMed |

Jacobsen S-E, Mujica A (2003) Quinoa: an alternative crop for saline soils. Journal of Experimental Botany 54, i25

Jacobsen S-E, Quispe H, Mujica A (2001) Quinoa: an alternative crop for saline soil in the Andes. In ‘Scientist and farmer – partners in research for the 21st century’. pp. 403–408. (CIP: Lima, Peru)

Jacobsen S-E, Mujica A, Jensen CR (2003) The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Reviews International 19, 99–109.
The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors.Crossref | GoogleScholarGoogle Scholar |

Jacobsen S-E, Liu F, Jensen CR (2009) Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Scientia Horticulturae 122, 281–287.
Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVamtbs%3D&md5=cd09eb9abf91a19c36b312297f24211cCAS |

Jacobsen S-E, Jensen CR, Liu F (2012) Improving crop production in the arid Mediterranean climate. Field Crops Research 128, 34–47.
Improving crop production in the arid Mediterranean climate.Crossref | GoogleScholarGoogle Scholar |

Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloids and Surfaces. B, Biointerfaces 61, 298–303.
Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFyisg%3D%3D&md5=1e1d4cdb090ab4694b5c657bbd5e692aCAS | 17949951PubMed |

James RA, Munns R, von Caemmerer S, Trejo C, Miller C, Condon TA (2006) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+, Cl– in salt-affected barley and wheat. Plant, Cell & Environment 29, 2185–2197.
Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+, Cl in salt-affected barley and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaisA%3D%3D&md5=736f65893a308a5a0f9c8a0f8e7b9562CAS |

Jensen CR, Jacobsen S-E, Anderson MN, Núñez N, Anderson SD, Rasmussen L, Mogensen VO (2000) Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying. European Journal of Agronomy 13, 11–25.
Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying.Crossref | GoogleScholarGoogle Scholar |

Kasai K, Fukayama H, Uchida N, Mori N, Yasuda T, Oji Y, Nakamura C (1998) Salinity tolerance in Triticum aestivum, Lophopyrum elongatum amphiploid and 5E disomic addition line evaluated by NaCl effects on photosynthesis and respiration. Cereal Research Communications 26, 281–287.

Kausar A, Ashraf MY, Ali I, Niaz M, Abbass Q (2012) Evaluation of sorghum varieties/lines for salt tolerance using physiological indices as screening tool. Pakistan Journal of Botany 44, 47–52.

Khan MA, Ungar IA, Showalter AM (2000) Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Annals of Botany 85, 225–232.
Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsFCisw%3D%3D&md5=9dad55358b27cc4cb6118dd03000ab8fCAS |

Koyro H-W, Eisa SS (2008) Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd. Plant and Soil 302, 79–90.
Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVGm&md5=3fa1389e2151f50cbc64fa2e774aecbfCAS |

Koyro HW, Geißler N, Hussin S, Huchzermeyer B (2008) Survival at extreme locations: life strategies of halophytes. The long way from system ecology, whole plant physiology, cell biochemistry and molecular aspects back to sustainable utilization at field sites. In ‘Biosaline agriculture and high salinity tolerance’. (Eds C Abdelly, M Ötztürck, M Ashraf, C Grignon) pp. 1–20. (Birkhäuser Verlag: Basel, Switzerland)

Koziol MJ (1991) Afrosimetric estimation of threshold saponin concentration for bitterness in quinoa (Chenopodium quinoa Willd.). Journal of the Science of Food and Agriculture 54, 211–219.
Afrosimetric estimation of threshold saponin concentration for bitterness in quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhs1amtrw%3D&md5=319cfdd459ea8fde18deeef174e8ee6dCAS |

Kozioł MJ (1992) Chemical composition and nutritional evaluation of quinoa (Chenopodium quinoa Willd.). Journal of Food Composition and Analysis 5, 35–68.
Chemical composition and nutritional evaluation of quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar |

Lambers H, Chapin FS, III, Pons TL (2008) ‘Plant physiological ecology.’ (2nd edn) (Springer-Verlag: New York)

Larcher W (1980) ‘Physiological plant ecology.’ (2nd rev. edn) (Springer-Verlag: New York)

Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment 25, 275–294.
Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakur0%3D&md5=2976b9458aa5c91694e9e77c07899fb1CAS |

Lima Neto MC, Lobo AKM, Martins MO, Fontenele AV, Silveira JA (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. Journal of Plant Physiology 171, 23–30.
Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOgur7I&md5=053800f033e23bef550708e57ad86923CAS | 24094996PubMed |

Lin JT, Chen SL, Liu SC, Yang DJ (2009) Effect of harvest time on saponins in Yam (Dioscoreapseudojaponica Yamamoto). Journal of Food and Drug Analysis 17, 116–122.

Longstreth DJ, Nobel PS (1979) Salinity effects on leaf anatomy. Plant Physiology 63, 700–703.
Salinity effects on leaf anatomy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnht12ksQ%3D%3D&md5=fac88f2fbe82084dec713c7faed91278CAS | 16660795PubMed |

Maas EV (1986) Salt tolerance of plants. Applied Agricultural Research 1, 12–26.

Maas EV, Hoffman GJ (1977) Crop salt tolerance, current assessment. Journal of the Irrigation and Drainage Division 103, 115–134.

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (2nd edn) (Academic Press: San Diego, CA, USA)

Martin B, Ruiz-Torres NA (1992) Effects of water-deficit stress on photosynthesis, its components and component limitations, and on water use efficiency in wheat (Triticum aestivum L.). Plant Physiology 100, 733–739.
Effects of water-deficit stress on photosynthesis, its components and component limitations, and on water use efficiency in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsVykt70%3D&md5=11b3d37297a7173021eb04268dd7ebb2CAS | 16653053PubMed |

Mehta SC, Poonia SR, Pal R (1983) Exchange equilibria of potassium versus calcium and sodium in soils from a semi-arid region, India. Soil Science 135, 214–220.
Exchange equilibria of potassium versus calcium and sodium in soils from a semi-arid region, India.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktVCmtL8%3D&md5=91b907671c9752f34f8d27f1f24b8828CAS |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=b0cf2c24ed0afbb17d466344b5ea8b75CAS |

Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1GlsrY%3D&md5=5018ffaf7b7bf3dccd113cf80ac42d79CAS | 16510517PubMed |

Nieman RH (1962) Some effects of sodium chloride on growth, photosynthesis and respiration of twelve crop plants. Botanical Gazette 123, 279–285.
Some effects of sodium chloride on growth, photosynthesis and respiration of twelve crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XktlOqur4%3D&md5=667f6c88741d3b82d40572e7540491ecCAS |

Ogburn RM, Edwards EJ (2010) The ecological water-use strategies of succulent plants. In ‘Advances in botanical research’. (Eds JC Kader, M Delseny) pp. 179–225. (Academic Press: Burlington, MA, USA)

Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Carrasco KBR, 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 halomorphism. Functional Plant Biology 38, 818–831.
Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halomorphism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFymsL7M&md5=db26bc24397e0dbd8ae97dfa82da6149CAS |

Parida AK, Das AB, Mittra B (2003) Effects of NaCl stress on the structure, pigment complex composition and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts. Photosynthetica 41, 191–200.
Effects of NaCl stress on the structure, pigment complex composition and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqtrbM&md5=88c5bac7b3014e0614e50d38094b6947CAS |

Parida AK, Das AB, Mittra B (2004) Effect of salt and growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees 18, 167–174.
Effect of salt and growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsl2htLk%3D&md5=e71bf10688944b55225de2349e5918dcCAS |

Pérez-López U, Robredo A, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2012) Elevated CO2 reduces stomatal and metabolic limitations on photosynthesis caused by salinity in Hordeum vulgare. Photosynthesis Research 111, 269–283.
Elevated CO2 reduces stomatal and metabolic limitations on photosynthesis caused by salinity in Hordeum vulgare.Crossref | GoogleScholarGoogle Scholar | 22286185PubMed |

Plauborg FL, Iversen BV, Lærke PE (2005) In situ comparison of three dielectric soil moisture sensors in drip irrigated sandy soils. Vadose Zone Journal 4, 1037–1047.
In situ comparison of three dielectric soil moisture sensors in drip irrigated sandy soils.Crossref | GoogleScholarGoogle Scholar |

Pulvento C, Riccardi M, Lavini A, Iafelice G, Marconi E, ďAndria R (2012) Yield and quality characteristics of quinoa grown in open field under saline and non-saline irrigation regimes. Journal Agronomy & Crop Science 198, 254–263.
Yield and quality characteristics of quinoa grown in open field under saline and non-saline irrigation regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtl2hu7rM&md5=784230d77d270d24410aaee67c9364ceCAS |

Ranade-Malvi U (2011) Interaction of micronutrients with major nutrients with special reference to potassium. Karnataka Journal of Agricultural Sciences 24, 106–109.

Razzaghi F, Ahmadi SH, Adolf VI, Jensen CR, Jacobsen S-E, Andersen MN (2011) Water relations and transpiration of quinoa (Chenopodium quinoa Willd.) under salinity and soil drying. Journal Agronomy & Crop Science 197, 348–360.
Water relations and transpiration of quinoa (Chenopodium quinoa Willd.) under salinity and soil drying.Crossref | GoogleScholarGoogle Scholar |

Razzaghi F, Ahmadi SH, Jacobsen S-E, Jensen CR, Andersen MN (2012) Effects of salinity and soil–drying on radiation use efficiency, water productivity and yield of quinoa (Chenopodium quinoa Willd.). Journal Agronomy & Crop Science 198, 173–184.
Effects of salinity and soil–drying on radiation use efficiency, water productivity and yield of quinoa (Chenopodium quinoa Willd.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGgs77N&md5=6650a162cdf98f9ad33e2133a1e51d69CAS |

Ribas-Carbo M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J (2005) Effects of water stress on respiration in soybean leaves. Plant Physiology 139, 466–473.
Effects of water stress on respiration in soybean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgurrI&md5=6441f074ccbdf0750eb330070e423ac2CAS | 16126857PubMed |

Riccardi M, Pulvento C, Lavini A, d’Andria R, Jacobsen S-E (2014) Growth and ionic content of quinoa under saline irrigation. Journal Agronomy & Crop Science 200, 246–260.
Growth and ionic content of quinoa under saline irrigation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVymurzP&md5=68a3012690cc8f3a6b9ba119850272ecCAS |

Rosa M, Hilal M, Gonzalez JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiology and Biochemistry 47, 300–307.
Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVGrtLk%3D&md5=ce5ba93e7d163990b137513bbee21e42CAS | 19124255PubMed |

Ruiz KB, Biondi S, Oses R, Acuña-Rodríguez IS, Antognoni F, Martinez-Mosqueira EA, Coulibaly A, Canahua-Murillo A, Pinto M, Zurita-Silva A, Bazile D, Jacobsen S-E, Molina-Montenegro MA (2014) Quinoa biodiversity and sustainability for food security under climate change. A review. Agronomy for Sustainable Development 34, 349–359.
Quinoa biodiversity and sustainability for food security under climate change. A review.Crossref | GoogleScholarGoogle Scholar |

Sabir Ali AK, Mohamed BF, Dreyling G (2014) Salt tolerance and effects of salinity on some agricultural crops in the Sudan. Journal of Forest Products & Industries 3, 56–65.

Scheffer F, Schachtschabel P (1979) Lehrbuch der Bodenkunde, 10. durchgesehene Auflage von Schachtschabel P, Blume HP, Hartge KH, Schwertmann U, Ferdinand Enke Verlag, Stuttgart.

Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant, Cell & Environment 23, 825–837.
Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt1CitLo%3D&md5=a9a201100fcb94e158bf2a019af8a9e7CAS |

Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit70%3D&md5=41f08ed37c691216935175c2ed7ae9cfCAS | 18724408PubMed |

Shabala S, Shabala S, Cuin TA, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. The Plant Journal 61, 839–853.
Xylem ionic relations and salinity tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFaktr0%3D&md5=bf93248851c43bbc376b35ff61cbcafcCAS | 20015063PubMed |

Shabala L, Mackay A, Tian Y, Jacobsen S-E, Zhou D, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa Willd). Physiologia Plantarum 146, 26–38.
Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa Willd).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWltb3E&md5=0b9b26cdcdd63a9c41cefc4e602e0230CAS | 22324972PubMed |

Shabala S, Hariadi Y, Jacobsen S-E (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology 170, 906–914.
Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFSrurk%3D&md5=56fc3088898743b2d2cd431381225d63CAS | 23485259PubMed |

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=a98955521cb2fe2211000f28ffa89a52CAS |

Solíz-Guerrero JB, de Rodriguez DJ, Rodríguez-García R, Angulo-Sánchez JL, Méndez-Padilla G (2002) Quinoa saponins: concentration and composition analysis. In ‘Trends in new crops and new uses’. (Eds J Janick, A Whipkey) pp. 110–114. (ASHS Press: Alexandria, VA, USA)

Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity – inhibition by ammonia and stimulation by sodium. The Journal of General Physiology 113, 909–918.
Potassium uptake supporting plant growth in the absence of AKT1 channel activity – inhibition by ammonia and stimulation by sodium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktVSrsLo%3D&md5=47775498536b009732be74a442b426a5CAS | 10352038PubMed |

Sun J, Chen SL, Dai SX, Wang RG, Li NY, Shen X, Zhou XY, Lu CF, Zheng XJ, Hu ZM, Zhang ZK, Song J, Xu Y (2009) Ion flux profiles and plant ion homeostasis control under salt stress. Plant Signaling & Behavior 4, 261–264.
Ion flux profiles and plant ion homeostasis control under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVyqurg%3D&md5=a4506a649852d9dfb337b6d9d6931780CAS |

Sun Y, Liu F, Bendevis M, Shabala S, Jacobsen S-E (2014) Sensitivity of two quinoa (Chenopodium quinoa Willd.) varieties to progressive drought stress. Journal Agronomy & Crop Science 200, 12–23.
Sensitivity of two quinoa (Chenopodium quinoa Willd.) varieties to progressive drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtVCntA%3D%3D&md5=b940b80ac4b2d0b370a0490f85aed60aCAS |

Szakiel A, Paczkowski C, Henry M (2011) Influence of environmental abiotic factors on the content of saponins in plants. Phytochemistry Reviews 10, 471–491.
Influence of environmental abiotic factors on the content of saponins in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVGmt7zK&md5=bee9a7f86d3f5294e7b2b8e086db477eCAS |

Valencia-Chamorro SA (2003) Quinoa. In ‘Encyclopedia of food science and nutrition. Vol. 8’. (Ed. B Caballero) pp. 4895–4902. (Academic Press: Amsterdam)

Wang L, Showalter AM, Ungar IA (1997) Effect of salinity on growth, ion content, and cell wall chemistry in Atriplex prostrata (Chenopodiaceae). American Journal of Botany 84, 1247–1255.
Effect of salinity on growth, ion content, and cell wall chemistry in Atriplex prostrata (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmslOkt70%3D&md5=95cbaaea05cf18ffc352497b4c8d5291CAS | 21708680PubMed |

Warren CR (2008) Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not. Journal of Experimental Botany 59, 327–334.
Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVamt78%3D&md5=c37e696d4e511183308c24a7ed7eed93CAS | 18238801PubMed |

Wilson C, Read JJ, Abo KE (2002) Effect of mixed-salt salinity on growth and ion relations of a quinoa and a wheat variety. Journal of Plant Nutrition 25, 2689–2704.
Effect of mixed-salt salinity on growth and ion relations of a quinoa and a wheat variety.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsVOkt74%3D&md5=297d4a2ec291d79d53ac1a9adb5220caCAS |

Zhang Y-H, Zhong J-J, Yu J-T (1996) Enhancement of ginseng saponin production in suspension cultures of Panax notoginseng: manipulation of medium sucrose. Journal of Biotechnology 51, 49–56.
Enhancement of ginseng saponin production in suspension cultures of Panax notoginseng: manipulation of medium sucrose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvValsr8%3D&md5=05cc5c586e6f0a1f0d32f40b5026591bCAS |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbc%3D&md5=6447d00a1abed2f15ac51866c4da72a7CAS | 12221975PubMed |

Zurita-Silva A, Fuentes F, Zamora P, Jacobsen SE, Schwember A (2014) Breeding quinoa (Chenopodium quinoa Willd.): potential and perspectives. Molecular Breeding.
Breeding quinoa (Chenopodium quinoa Willd.): potential and perspectives.Crossref | GoogleScholarGoogle Scholar |