Quinoa – a Model Crop for Understanding Salt-tolerance Mechanisms in Halophytes

Plant Biosystems

Volumn 150, Issue 2, 2016, Pages 357-371

  Ruiz, K B ^a   Biondi, S ^b   Martinez E A ^c   Orsini, F ^b   Antognoni, F ^b   Jacobsen, S E ^d  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSIDAD CATÓLICA DEL NORTE   (Chile)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Abiotic stress; adaptation; Andean crop; genetic variability; halophyte crop; nutritional properties; salinity

Indexed keywords

EID: 84927537451     PISSN: 11263504     EISSN: 17245575     Source Type: Journal    
DOI: 10.1080/11263504.2015.1027317     Document Type: Article

References (103)

1. V.I.Adolf, S.-E.Jacobsen, S.Shabala. 2013. Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.). Env Exp Bot92: 43–54. doi:10.1016/j.envexpbot.2012.07.004.
2. V.I.Adolf, S.Shabala, M.N.Andersen, F.Razzaghi, S.-E.Jacobsen. 2012. Varietal differences of quinoa's tolerance to saline conditions. Plant Soil357(1-2): 117–129. doi:10.1007/s11104-012-1133-7.
3. S.Agarie, T.Shimoda, Y.Shimizu, K.Baumann, H.Sunagawa, A.Kondo, et al. 2007. Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. J Exp Bot58(8): 1957–1967. doi:10.1093/jxb/erm057.
4. P.C.Aguilar, Z.Cutipa, E.Machaca, M.López, S.-E.Jacobsen. 2003. Variation of proline content of quinoa (Chenopodium quinoa Willd.) in high beds (waru waru). Food Rev Int19(1-2): 121–127. doi:10.1081/FRI-120018878.
5. + on the salt resistance of Aeluropus lagopoides. Funct Plant Biol.40: 860–871.
6. R.Alcázar, T.Altabella, F.Marco, C.Bortolotti, M.Reymond, C.Koncz, et al. 2010. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta231: 1237–1249.
7. +-ATPase and upregulating its transport activity. Mol Cell Biol27(22): 7781–7790. doi:10.1128/MCB.00430-07.
8. M.Battaglia, Y.Olvera-Carrillo, A.Garciarrubio, F.Campos, A.A.Covarrubias. 2008. The enigmatic lea proteins and other hydrophilins. Plant Physiol148(1): 6–24. doi:10.1104/pp.108.120725.
9. D.Bazile, H.D.Bertero, C.Nieto, editors. 2015. State of the Art Report on Quinoa around the World in 2013: FAO (Santiago, Chile)/ CIRAD (Montpellier, France). ISBN 978-92-5-108558-5.
10. 14C assimilation and overall carbon and nitrogen allocation patterns in contrasting quinoa cultivars. Env Exp Bot104: 9–15. doi:10.1016/j.envexpbot.2014.03.002.
11. M.A.Bendevis, Y.Sun, S.Shabala, E.Rosenqvist, F.Liu, S.-E.Jacobsen. 2014a. Differentiation of photoperiod induced ABA and soluble sugar responses of two quinoa (Chenopodium quinoa Willd.) cultivars. J Plant Growth Reguldoi:10.1007/s00344-013-9406-9.
12. A.Ben Hassine, M.E.Ghanem, S.Bouzid, S.Lutts. 2009. Abscisic acid has contrasting effects on salt excretion and polyamine concentrations of an inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus. Ann Bot104(5): 925–936. doi:10.1093/aob/mcp174.
13. O.Benlhabib, A.Yazar, M.Qadir, E.Lourenço, S.E.Jacobsen. 2014. How can we improve Mediterranean cropping systems?J Agron Crop Sci. doi:10.1111/jac.12066.
14. E.Blumwald, G.S.Aharon, M.P.Apse. 2000. Sodium transport in plant cells. Biochim. Biophys. Acta-Biomembranes1465(1-2): 140–151. doi:10.1016/S0005-2736(00)00135-8.
15. J.F.Bois, T.Winkel, J.P.Lhomme, J.P.Raffaillac, A.Rocheteau. 2006. Response of some Andean cultivars of quinoa (Chenopodium quinoa Willd.) to temperature: effects on germination, phenology, growth and freezing. Eur J Agron25(4): 299–308. doi:10.1016/j.eja.2006.06.007.
16. E.Bonales-Alatorre, I.Pottosin, L.Shabala, Z.-H.Chen, F.Zeng, S.-E.Jacobsen, et al. 2013. Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a halophyte species, Chenopodium quinoa. Int J Mol Sci14(5): 9267–9285. doi:10.3390/ijms14059267.
17. H.Bosque-Sánchez, R.Lemeur, P.Van Damme, S.-E.Jacobsen. 2003. Ecophysiological analysis of drought and salinity stress of quinoa. Food Rev Int19: 111–119.
18. H.P.Burrieza, H.-W.Koyro, L.M.Tosar, K.Kobayashi, S.Maldonado. 2012. High salinity induces dehydrin accumulation in Chenopodium quinoa Willd. Cv. Hualhuas embryos. Plant Soil354(1-2): 69–79. doi:10.1007/s11104-011-1045-y.
19. P.Carjuzáa, M.Castellión, A.J.Distéfano, M.del Vas, S.Maldonado. 2008. Detection and subcellular localization of dehydrin-like proteins in quinoa (Chenopodium quinoa Willd.) embryos. Protoplasma233: 149–156.
20. D.Carlson, J.A.Fernandez, H.D.Poulsen, B.Nielsen, S.-E.Jacobsen. 2012. Effects of quinoa hull meal on piglet performance and intestinal epithelial physiology. J Anim Physiol An N96(2): 198–205. doi:10.1111/j.1439-0396.2011.01138.x.
21. D.Ceccato, J.Delatorre-Herrera, H.Burrieza, D.Bertero, E.A.Martínez, I.Delfino, et al. 2015. Seed physiology and response to germination conditions. In: State of the Art Report on Quinoa around the World in 2013. Montpellier, France: FAO (Santiago, Chile) & CIRAD. ISBN 978-92-5-108558-5. pp. 131–142.
22. G.Chilo, M.V.Molina, R.Carabajal, M.Ochoa. 2009. Temperature and salinity effects on germination and seedling growth on two varieties of Chenopodium quinoa. AgriScientia26: 15–22.
23. J.L.Christiansen, S.-E.Jacobsen, S.T.Jørgensen. 2010. Photoperiodic effect on flowering and seed development in quinoa (Chenopodium quinoa Willd.). Acta Agr Scand Section B - S P60: 539–544.
24. S.A.Christensen, D.B.Pratt, C.Pratt, P.T.Nelson, M.R.Stevens, E.N.Jellen, et al. 2007. Assessment of genetic diversity in the USDA and CIP-FAO international nursery collections of quinoa (Chenopodium quinoa Willd.) using microsatellite markers. Plant Genetic Res5(2): 82–95. doi:10.1017/S1479262107672293.
25. C.Cocozza, C.Pulvento, A.Lavini, M.Riccardi, R.d'Andria, R.Tognetti. 2013. Effects of increasing salinity stress and decreasing water availability on ecophysiological traits of quinoa (Chenopodium quinoa Willd.) grown in a Mediterranean-type agroecosystem. J Agron Crop Sci199(4): 229–240. doi:10.1111/jac.12012.
26. T.A.Cuin, S.Shabala. 2007. Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ30(7): 875–885. doi:10.1111/j.1365-3040.2007.01674.x.
27. T.A.Cuin, S.Shabala. 2005. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol46(12): 1924–1933. doi:10.1093/pcp/pci205.
28. A.Debez, K.Ben Hamed, C.Grignon, C.Abdelly. 2004. Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant Soil262(1/2): 179–189. doi:10.1023/B:PLSO.0000037034.47247.67.
29. J.Delatorre-Herrera, M.Pinto. 2009. Importance of ionic and osmotic components of salt stress on the germination of four quinoa (Chenopodium quinoa Willd.) selections. Chilean J Agric Res69(4): 477–485. doi:10.4067/S0718-58392009000400001.
30. +-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci123(9): 1468–1479. doi:10.1242/jcs.064352.
31. J.Duan, J.Li, S.Guo, Y.Kang. 2008. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol165(15): 1620–1635. doi:10.1016/j.jplph.2007.11.006.
32. C.Espinoza, R.Repo-Carrasco, S.-E.Jacobsen. 2001. Caracterización de la fracción lipídica de quinua. In: S.-E.Jacobsen, A.Mujica, Z.Portillo, editors. Primer Taller Internacional sobre Quinua – Recursos Geneticos y Sistemas de Producción, 10–14 May 1999, UNALM. Lima: CIP. pp. 447–448.
33. T.J.Flowers. 2004. Improving crop salt tolerance. J Exp Bot55(396): 307–319. doi:10.1093/jxb/erh003.
34. T.J.Flowers, T.D.Colmer. 2008. Salinity tolerance in halophytes. New Phytol179(4): 945–963. doi:10.1111/j.1469-8137.2008.02531.x.
35. F.F.Fuentes, A.Bhargava. 2011. Morphological analysis of quinoa germplasm grown under lowland desert conditions. J Agron Crop Sci197(2): 124–134. doi:10.1111/j.1439-037X.2010.00445.x.
36. F.F.Fuentes, D.Bazile, A.Bhargava, E.A.Martínez. 2012. Implications of farmers' seed exchanges for on-farm conservation of quinoa, as revealed by its genetic diversity in Chile. J Agric Sci150(6): 702–716. doi:10.1017/S0021859612000056.
37. F.F.Fuentes, E.A.Martínez, P.V.Hinrichsen, E.N.Jellen, P.J.Maughan. 2009. Assessment of genetic diversity patterns in Chilean quinoa (Chenopodium quinoa Willd.) germplasm using multiplex fluorescent microsatellite markers. Conserv. Genetics10(2): 369–377. doi:10.1007/s10592-008-9604-3.
38. E.P.Glenn, T.Anday, R.Chaturvedi, R.Martinez-Garcia, S.Pearlstein, D.Soliz, et al. 2013. Three halophytes for saline-water agriculture: An oilseed, a forage and a grain crop. Env Exp Bot92: 110–121. doi:10.1016/j.envexpbot.2012.05.002.
39. A.Gómez-Caravaca, G.Iafelice, A.Lavini, C.Pulvento, M.Caboni, E.Marconi. 2012. Phenolic compounds and saponins in quinoa samples (Chenopodium quinoa Willd.) grown under different saline and nonsaline irrigation regimes. J Agric Food Chem60: 4620–4627.
40. L.R.Gómez-Pando, R.Álvarez-Castro, E.de la Barra. 2010. Effect of salt stress on Peruvian germplasm of Chenopodium quinoa Willd.: a promising crop. J Agron Crop Sci196: 391–396.
41. J.A.González, Y.Konishi, M.Bruno, M.Valoy, F.E.Prado. 2011. Interrelationships among seed yield, total protein and amino acid composition of ten quinoa (Chenopodium quinoa) cultivars from two different agroecological regions. J Sci Food Agr92: 1222–1229.
42. J.A.González, F.Prado. 1992. Germination in relation to temperature and different salt concentration in Chenopodium quinoa. Agrochimica36: 101–107.
43. K.B.Hamed, H.Ellouzi, O.Z.Talbi, K.Hessini, I.Slama, T.Ghnaya, et al. 2013. Physiological response of halophytes to multiple stresses. Funct Plant Biol40: 883–896.
44. Y.Hariadi, K.Marandon, Y.Tian, S.-E.Jacobsen, S.Shabala. 2011. Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J Exp Bot62(1): 185–193. doi:10.1093/jxb/erq257.
45. P.M.Hasegawa, R.A.Bressan, J.K.Zhu, H.J.Bohnert. 2000. Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol51(1): 463–499. doi:10.1146/annurev.arplant.51.1.463.
46. A.Hirich, A.Jelloul, R.Choukr-Allah, S.-E.Jacobsen. 2014. Saline water irrigation of quinoa and chickpea: Seedling rate, stomatal conductance and yield responses. J Agron Crop Sci. doi:10.1111/jac.12072.
47. S.S.Hussain, M.Ali, M.Ahmad, K.H.M.Siddique. 2011. Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotech Adv29(3): 300–311. doi:10.1016/j.biotechadv.2011.01.003.
48. E.R.R.Iyengar, M.P.Reddy. 1997. Photosynthesis in highly salt tolerant plants. In: M.Pesserakli, editor. Handbook of plant and crop stress. New York, Basel. Hong Kong: Marcel Dekker Inc. pp. 897–909.
49. G.Inan, Q.Zhang, P.H.Li, Z.Wang, Z.Cao, H.Zhang, et al. 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 Physiol135(3): 1718–1737. doi:10.1104/pp.104.041723.
50. S.-E.Jacobsen. 2014. New climate proof cropping systems in dry areas of the Mediterranean region. J Agro Crop Scidoi:10.1111/jac.12080.
51. S.-E.Jacobsen, J.L.Christiansen, J.Rasmussen. 2010. Weed harrowing and inter-row hoeing in organic grown quinoa (Chenopodium quinoa Willd.). Outlook Agric39(3): 223–227. doi:10.5367/oa.2010.0001.
52. S.-E.Jacobsen, C.R.Jensen, F.Liu. 2012. Improving crop production in the arid Mediterranean climate. Field Crop Res128: 34–47. doi:10.1016/j.fcr.2011.12.001.
53. S.-E.Jacobsen, F.Liu, C.R.Jensen. 2009. Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Sci Hortic Amsterdam122(2): 281–287. doi:10.1016/j.scienta.2009.05.019.
54. S.-E.Jacobsen, C.Monteros, J.L.Christiansen, L.A.Bravo, L.J.Corcuera, A.Mujica. 2005. Plant responses of quinoa (Chenopodium quinoa Willd.) to frost at various phenological stages. Eur J Agron22(2): 131–139. doi:10.1016/j.eja.2004.01.003.
55. S.-E.Jacobsen, C.Monteros, L.J.Corcuera, L.A.Bravo, J.L.Christiansen, A.Mujica. 2007. Frost resistance mechanisms in quinoa (Chenopodium quinoa Willd.). Eur J Agron26(4): 471–475. doi:10.1016/j.eja.2007.01.006.
56. S.-E.Jacobsen, A.Mujica, C.R.Jensen. 2003. The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Rev Int19(1-2): 99–109. doi:10.1081/FRI-120018872.
57. M.Janicka-Russak, K.Kabała, E.Młodzińska, G.Kłobus. 2010. The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. J Plant Physiol167(4): 261–269. doi:10.1016/j.jplph.2009.09.010.
58. D.Jha, N.Shirley, M.Tester, S.J.Roy. 2010. Variation in salinity tolerance and shoot sodium accumulation in Arabidopsis ecotypes linked to differences in the natural expression levels of transporters involved in sodium transport. Plant Cell Environ337: 93–804.
59. Y.Jou, Y.L.Wang, H.C.E.Yen. 2007. Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum. Funct Plant Biol34(4): 353–359. doi:10.1071/FP06269.
60. T.KaryotisTh, C.Iliadis, C.NoulasCh, T.MitsibonasTh. 2003. Preliminary research on seed production and nutrient content for certain quinoa varieties in a saline-sodic soil. J Agron Crop Sci189(6): 402–408. doi:10.1046/j.0931-2250.2003.00063.x.
61. H.-W.Koyro, S.S.Eisa. 2008. Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa willd. Plant Soil302(1-2): 79–90. doi:10.1007/s11104-007-9457-4.
62. T.Kusano, T.Berberich, C.Tateda, Y.Takahashi. 2008. Polyamines: essential factors for growth and survival. Planta228(3): 367–381. doi:10.1007/s00425-008-0772-7.
63. A.Lavini, C.Pulvento, R.d'Andria, M.Riccardi, R.Choukr-Allah, O.Belhabib, et al. 2014. Quinoa's potential in the Mediterranean region. J Agron Crop Sci. doi:10.1111/jac.12069.
64. P.J.Maughan, T.B.Turner, C.E.Coleman, D.B.Elzinga, E.N.Jellen, J.A.Morales, et al. 2009. Characterization of Salt Overly Sensitive1 (SOS1) gene homoeologs in quinoa (Chenopodium quinoa Willd.). Genome52(7): 647–657. doi:10.1139/G09-041.
65. M.Miranda, A.Vega-gálvez, E.A.Martínez, J.López, R.Marín, M.Aranda, F.Fuentes. 2013. Influence of contrasting environments on seed composition of two quinoa genotypes: nutritional and functional properties. Chil J Agr Res73(2): 06–07. doi:10.4067/S0718-58392013000200004.
66. A.J.Morales, P.Bajgain, Z.Garver, P.J.Maughan, J.A.Udall. 2011. Physiological responses of Chenopodium quinoa to salt stress. Int J Plant Physiol Biochem3: 219–232.
67. R.Munns, A.R.James, A.Läuchli. 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot57(5): 1025–1043. doi:10.1093/jxb/erj100.
68. R.Munns, M.Tester. 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol59(1): 651–681. doi:10.1146/annurev.arplant.59.032607.092911.
69. G.Noctor, C.H.Foyer. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol49(1): 249–279. doi:10.1146/annurev.arplant.49.1.249.
70. F.Orsini, M.Accorsi, G.Gianquinto, G.Dinelli, F.Antognoni, K.B.Ruiz Carrasco, et al. 2011. Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol38(10): 818–831. doi:10.1071/FP11088.
71. S.Panta, T.Flowers, P.Lane, R.Doyle, G.Haros, S.Shabala. 2014. Halophyte agriculture: Success stories. Env Exp Bot107: 71–83. doi:10.1016/j.envexpbot.2014.05.006.
72. I.Pottosin, E.Bonales-Alatorre, S.Shabala2014. Choline but not its derivative betaine blocks slow vacuolar channels in the halophyte Chenopodium quinoa: implications for salinity stress responses. FEBS Lett588: 3918–3923.
73. F.E.Prado, C.Boero, M.Gallardo, J.A.González. 2000. Effect of NaCl on germination, growth, and soluble sugar content in Chenopodium quinoa Willd. seeds. Bot Bull Acad Sinica41: 27–34.
74. C.Pulvento, M.Riccardi, A.Lavini, R.d'Andria, G.Iafelice, E.Marconi. 2010. Field trial evaluation of two Chenopodium quinoa genotypes grown under rain-fed conditions in a typical Mediterranean environment in south Italy. J Agron Crop Sci196(6): 407–411. doi:10.1111/j.1439-037X.2010.00431.x.
75. C.Pulvento, M.Riccardi, A.Lavini, G.Iafelice, E.Marconi, R.d'Andria. 2012. Yield and quality characteristics of quinoa grown in open field under different saline and non-saline irrigation regimes. J Agron Crop Sci198(4): 254–263. doi:10.1111/j.1439-037X.2012.00509.x.
76. +exchanger in Arabidopsis thaliana, by SOS2 and SOS3. P Natl Acad Sci USA99(12): 8436–8441. doi:10.1073/pnas.122224699.
77. F.Razzaghi, S.H.Ahmadi, V.I.Adolf, C.R.Jensen, S.-E.Jacobsen, M.N.Andersen. 2011. Water relations and transpiration of quinoa (Chenopodium quinoa Willd.) under salinity and soil drying. J Agron Crop Sci197(5): 348–360. doi:10.1111/j.1439-037X.2011.00473.x.
78. F.Razzaghi, S.H.Ahmadi, S.-E.Jacobsen, C.R.Jensen, M.N.Andersen. 2012. Effects of salinity and soil-drying on radiation use efficiency, water productivity and yield of quinoa (Chenopodium quinoa Willd.). J Agron Crop Sci198(3): 173–184. doi:10.1111/j.1439-037X.2011.00496.x.
79. F.Razzaghi, S.-E.Jacobsen, C.R.Jensen, M.N.Andersen. 2014. Ionic and photosynthetic homeostasis in quinoa challenged by salinity and drought - mechanisms of tolerance. Funct Plant Biol. doi:10.1071/FP14132.
80. R.Repo-Carrasco, C.Espinoza, S.-E.Jacobsen. 2003. Nutritional value and use of the Andean crops quinoa (Chenopodium quinoa) and kañiwa (Chenopodium pallidicaule). Food Rev Int19(1-2): 179–189. doi:10.1081/FRI-120018884.
81. M.C.Riccardi, C.Pulvento, A.Lavini, R.d'Andria, S.-E.Jacobsen. 2014. Growth and ionic content of quinoa under saline irrigation. J Agron Crop Sci. doi:10.1111/jac.12061.
82. J.C.Risi, N.W.Galwey. 1984. The Chenopodium grains of the Andes: Inca crops for modern agriculture. Adv Appl Biol10: 145–216.
83. T.Rorat. 2006. Plant dehydrins — tissue location, structure and function. Cell Mol Biol Lett11(4): 536–556. doi:10.2478/s11658-006-0044-0.
84. M.Rosa, M.Hilal, J.A.González, F.E.Prado. 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 Physiol Biochem47(4): 300–307. doi:10.1016/j.plaphy.2008.12.001.
85. A.M.C.Ruffino, M.Rosa, M.Hilal, J.A.González, F.E.Prado. 2010. The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity. Plant Soil326(1-2): 213–224. doi:10.1007/s11104-009-9999-8.
86. K.Ruiz-Carrasco, F.Antognoni, A.K.Coulibaly, S.Lizardi, A.Covarrubias, E.A.Martínez, et al. 2011. Variation in salinity tolerance of four lowland genotypes of quinoa (Chenopodium quinoa Willd.) as assessed by growth, physiological traits, and sodium transporter gene expression. Plant Physiol Biochem49(11): 1333–1341. doi:10.1016/j.plaphy.2011.08.005.
87. K.B.Ruiz, S.Biondi, R.Oses, I.S.Acuña-Rodríguez, F.Antognoni, E.A.Martinez-Mosqueira, et al. 2014. Quinoa biodiversity and sustainability for food security under climate change. A review. Agron Sustain Dev34(2): 349–359. doi:10.1007/s13593-013-0195-0.
88. L.Saavedra, J.Svensson, V.Carballo, D.Izmendi, B.Welin, S.Vidal. 2006. A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J45(2): 237–249. doi:10.1111/j.1365-313X.2005.02603.x.
89. F.I.Schabes, E.E.Sigstad. 2005. Calorimetric studies of quinoa (Chenopodium quinoa Willd.) seed germination under saline stress conditions. Thermochim Acta428(1-2): 71–75. doi:10.1016/j.tca.2004.09.027.
90. + loading and stomatal density. J Plant Physiol170(10): 906–914. doi:10.1016/j.jplph.2013.01.014.
91. S.Shabala, A.Mackay. 2011. Ion transport in halophytes. Adv Bot Res57: 151–187.
92. L.Shabala, A.Mackay, Y.Tian, S.-E.Jacobsen, D.Zhou, S.Shabala. 2012. Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol Plant146(1): 26–38. doi:10.1111/j.1399-3054.2012.01599.x.
93. + transport in plants. Plant Cell14(2): 465–477. doi:10.1105/tpc.010371.
94. E.Small. 2013. 42. Quinoa – is the United Nations' featured crop of 2013 bad for biodiversity?Biodiversity14(3): 169–179. doi:10.1080/14888386.2013.835551.
95. C.G.Suhayda, R.E.Redmann, B.L.Harvey, A.L.Cipywnyk. 1992. Comparative response of cultivated and wild barley species to salinity stress and calcium supply. Crop Sci32(1): 154–163. doi:10.2135/cropsci1992.0011183X003200010033x.
96. Y.Sun, F.Liu, M.Bendevis, S.Shabala, S.-E.Jacobsen. 2014. Sensitivity of two quinoa (Chenopodium quinoa Willd.) varieties to progressive drought stress. J Agron Crop Sci200(1): 12–23. doi:10.1111/jac.12042.
97. L.Szabados, A.Savouré. 2010. Proline: a multifunctional amino acid. Trends Plant Sci15(2): 89–97. doi:10.1016/j.tplants.2009.11.009.
98. W.Tang, R.J.Newton. 2005. Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul46(1): 31–43. doi:10.1007/s10725-005-6395-0.
99. A.Vega-Gálvez, M.Miranda, J.Vergara, E.Uribe, L.Puente, E.A.Martínez. 2010. Nutrition facts and functional potential of quinoa (Chenopodium quinoa Willd.), an ancient Andean grain: a review. J Sci Food Agric90: 2541–2547.
100. C.Wilson, J.J.Read, E.Abo-Kassem. 2002. Effect of mixed-salt salinity on growth and ion relations of a quinoa and a wheat variety. J Plant Nutr25(12): 2689–2704. doi:10.1081/PLN-120015532.
101. G.M.Woldemichael, M.Wink. 2001. Identification and biological activities of triterpenoid saponins from Chenopodium quinoa. J Agric Food Chem49(5): 2327–2332. doi:10.1021/jf0013499.
102. K.Yamaguchi, Y.Takahashi, T.Berberich, A.Imai, T.Takahashi, A.J.Michael, et al. 2007. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun352(2): 486–490. doi:10.1016/j.bbrc.2006.11.041.
103. A.Zurita-Silva, F.Fuentes, P.Zamora, S.-E.Jacobsen, A.Schwember. 2014. Breeding quinoa (Chenopodium quinoa Willd.): potential and perspectives. Mol Breeding34(1): 13–30. doi:10.1007/s11032-014-0023-5.