Skip to main content
SpringerLink
Log in

The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

A growth chamber experiment was conducted to assess the effect of salinity on emergence, growth, water status, photosynthetic pigments, osmolyte accumulation, and ionic content of quinoa seedlings (Chenopodium quinoa). The aim was to test the hypothesis that quinoa seedlings are well adapted to grow under salinity due to their ability to adjust the metabolic functionality of their cotyledons. Seedlings were grown for 21 days at 250 mM NaCl from the start of the germination. Germination percentage and cotyledon area were not affected by salt whereas seedling height decreased 15%. FW increased in both control and salt-treated cotyledons, but the increase was higher under salinity. DW only increased in salt-treated cotyledons. The DW/FW ratio did not show significant differences between treatments. Relative water content, chlorophyll, carotenoids, lipids, and proteins were significantly lower under salinity. Total soluble sugars, sucrose and glucose concentrations were higher in salt-treated than in control cotyledons. Ion concentration showed a different distribution pattern. Na+ and Cl− concentrations were higher under salinity, while an inverse result was observed for K+ concentration. Proline and glycinebetaine concentrations increased under salinity, but the increase was higher in the former than the latter. The osmoprotective role of proline, glycinebetaine, and soluble sugars is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aldesuquy HS, Ibrahim AH (2001) Water relations, abscisic acid and yield of wheat plants in relation to the interactive effect of seawater and growth bioregulators. J Agron Crop Sci 187:97–104

    Article  CAS  Google Scholar 

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    Article  CAS  Google Scholar 

  • Bhargava A, Shukla S, Ohri D (2006) Chenopodium quinoa - An Indian perspective. Ind Crop Prod 23:73–87

    Article  CAS  Google Scholar 

  • Cardini C, Leloir LF, Chiriboga J (1955) The biosynthesis of sucrose. J Biol Chem 214:149–155

    CAS  PubMed  Google Scholar 

  • Chapelle EW, Kim MS (1992) Ratio analysis of reflectance spectra (RARS): an algorithm for the remote estimation of the concentration of chlorophyll a, chlorophyll b, and carotenoids in soybean leaves. Rem Sen Environ 39:39–247

    Google Scholar 

  • Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 155:455–463

    Article  CAS  Google Scholar 

  • Djanaguiraman M, Ramadass R (2004) Effect of salinity on chlorophyll content of rice genotypes. Agric Sci Digest 24:178–181

    Google Scholar 

  • Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U (2006) Rice can acclimate to lethal level of salinity by pre-treatment with sublethal level of salinity through osmotic adjustment. Plant Soil 284:363–373

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugar and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121

    Article  CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Quart Rev Biol 61:313–337

    Article  Google Scholar 

  • Foolad MR (1999) Comparison of salt tolerance during seed germination and vegetative growth in tomato by QTL mapping. Genome 42:727–734

    Article  CAS  Google Scholar 

  • Glenn E, Brown J, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  • González JA, Prado FE (1992) Germination in relation to salinity and temperature in Chenopodium quinoa (Willd.). Agrochimica 36:101–107

    Google Scholar 

  • Guerrier G, Patolia JS (1989) Comparative salt response of excised cotyledons and seedlings of pea to various osmotic and ionic stresses. J Plant Physiol 135:330–337

    CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Mol Biol 51:463–499

    Article  CAS  Google Scholar 

  • Hendry GAF, Price AH (1993) Stress indicators: chlorophylls and carotenoids. In: Hendry GAF, Grime JP (eds) Methods in comparative plant ecology. Chapman and Hall, London, pp 148–152

    Google Scholar 

  • Hernández JA, Olmos E, Corpas FJ, Sevilla F, del Río LA (1995) Salt-induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp St 347:1–39

    Google Scholar 

  • Hunt J (1982) Dilute hydrochloric acid extraction of plant material for routine cation analysis. Commu Soil Sci Plant Anal 13:49–55

    Article  CAS  Google Scholar 

  • Jacobsen SE (2007) Quinoa’s world potential. In: Ochatt S, Jain SM (eds) Breeding of neglected and under-utilized crops, spices and herbs. Science Publishers, Enfield, pp 109–122

    Google Scholar 

  • Jorgensen OS, Andersen B (1973) An improved glucose-oxidase-peroxidase-coupled assay for beta fructofuranosidase activity. Anal Biochem 53:141–145

    Article  CAS  PubMed  Google Scholar 

  • 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. Ann Bot 85:225–232

    Article  CAS  Google Scholar 

  • Khosravinejad F, Heydari R, Farboodnia T (2008) Effects of salinity on photosynthetic pigments, respiration, and water content in two barley varieties. Pakistan J Biol Sci 11:2438–2442

    Article  CAS  Google Scholar 

  • Kim DJ (2004) A study of cotyledon senescence in cucumber (Cucumis sativus L.) based on expressed sequence tags and gene expression. J Plant Biol 47:244–253

    Article  CAS  Google Scholar 

  • Koyro HW (2006) Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environ Exp Bot 56:136–146

    Article  CAS  Google Scholar 

  • Koyro HW, Sayed SE (2008) Effect of salinity on composition, viability and germination of seeds of Chenopodium quinoa Willd. Plant Soil 302:79–90

    Article  CAS  Google Scholar 

  • Ladyman AR, Ditz KM, Grumet R, Hanson AD (1983) Genotypic variation for glycinebetaine accumulation by cultivated and wild barley in relation to water stress. Crop Sci 23:465–468

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NH, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lynch MJ, Raphael SS, Meldon LD, Space PD, Hill P, Inwood MJH (1963) Cholesterol. Medical laboratory techniques. W.B. Saunders, London

    Google Scholar 

  • Maathuis FJM (2007) Monovalent cation transporters; establishing a link between bioinformatics and physiology. Plant Soil 301:1–15

    Article  CAS  Google Scholar 

  • Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133

    Article  CAS  Google Scholar 

  • Malcolm CV, Lindley VA, O’Leary JW, Runciman HV, Barrett-Lennard EG (2003) Halophyte and glycophyte salt tolerance at germination and the establishment of halophyte shrubs in saline environments. Plant Soil 253:171–185

    Article  CAS  Google Scholar 

  • Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–272

    Article  Google Scholar 

  • Matile P (2000) Biochemistry of Indian summer: Physiology of autumnal leaf coloration. Exp Gerontol 35:145–158

    Article  CAS  PubMed  Google Scholar 

  • Meloni DA, Gulotta MR, Martínez CA (2008) Salinity tolerance in Schinopsis quebracho colorado: seed germination, growth, ion relations and metabolic responses. J Arid Environ 72:1785–1792

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  CAS  PubMed  Google Scholar 

  • Omami EN, Hammes PS (2006) Interactive effects of salinity and water stress on growth, leaf water relations, and gas exchange in amaranth (Amaranthus spp.). N Z J Crop Hort Sci 34:33–44

    Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Safety 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer I, Kutschera U (1996) Sucrose metabolism and lipid mobilization during light-induced expansion of sunflower cotyledons. J Plant Physiol 147:553–558

    CAS  Google Scholar 

  • Prado FE, González JA, Gallardo M, Moris M, Boero C, Kortsarz A (1995) Changes in soluble carbohydrates and invertase activity in Chenopodium quinoa (“quinoa”) developed for saline stress during germination. Curr Top Phytochem 14:1–5

    Google Scholar 

  • Prado FE, Boero C, Gallardo M, Gonzalez JA (2000) Effect of NaCl on germination, growth, and soluble sugar content in Chenopodium quinoa (Willd.) seeds. Bot Bull Acad Sin 41:27–34

    CAS  Google Scholar 

  • Raven JA (1985) Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol 101:25–77

    Article  CAS  Google Scholar 

  • Repo-Carrasco R, Espinoza C, Jacobsen SE (2003) Nutritional value and use of the Andean crops quinoa (Chenopodium quinoa) and kañiwa (Chenopodium pallidicaule). Food Rev Int 19:179–189

    Article  Google Scholar 

  • Roe JH, Papadopoulos NM (1954) The determination of fructose-6-phosphate and fructose-1,6-diphosphate. J Biol Chem 210:703–707

    CAS  PubMed  Google Scholar 

  • Rosa M (2006) Efecto de las bajas temperaturas y la salinidad sobre la morfoanatomía y la fisiología en plántulas de quinoa (Chenopodium quinoa Willd.), con especial énfasis sobre el metabolismo de los carbohidratos y proteínas. PhD Thesis. Facultad de Ciencias Naturales e IML, Universidad Nacional de Tucumán

  • Rosa M, Hilal M, González JA, Prado FE (2004) Changes in soluble carbohydrates and related enzymes induced by low temperature during early developmental stages of quinoa (Chenopodium quinoa) seedlings. J Plant Physiol 161:683–689

    Article  CAS  PubMed  Google Scholar 

  • Rosa M, Hilal M, González 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 Physiol Biochem 47:300–307

    Article  CAS  PubMed  Google Scholar 

  • Roughan PG, Batt RD (1967) Quantitative analysis of sulpholipid (sulphoquinovosyl diglyceride) and galactolipids (monogalactosil and galactosil diglyceride) in plant tissues. Anal Biochem 22:74–88

    Article  Google Scholar 

  • SAS (1989) SAS/STAT User’s guide. Version 6, 4th edn., vol.2, Cary, NC: SAS Institute Inc

  • Scheumann V, Schoch S, Rüdiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209:364–370

    Article  CAS  PubMed  Google Scholar 

  • Shepherd KA, MacFarlane TD, Colmer TD (2005) Morphology, anatomy and histochemistry of Salicornioideae (Chenopodiaceae) fruits and seeds. Ann Bot 95:917–933

    Article  CAS  PubMed  Google Scholar 

  • Song J, Feng G, Tian C, Zhang F (2005) Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Ann Bot 96:399–405

    Article  CAS  PubMed  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • Ting SV, Rouseff RL (1979) Proline content in Florida frozen concentrated orange juice and canned grapefruit juice. Proc Flor St Hort Soc 92:143–145

    CAS  Google Scholar 

  • Tobe K, Li X, Omasa K (2000) Seed germination and radicle growth of a halophyte, Kalidium capsicum (Chenopodiaceae). Ann Bot 85:391–396

    Article  Google Scholar 

  • Ungar IA (1996) Effect of salinity on seed germination, growth and ion accumulation of Atriplex patula (Chenopodiaceae). Am J Bot 83:604–607

    Article  Google Scholar 

  • Vieira Santos CL, Campos A, Azevedo H, Caldeira G (2001) In situ and in vitro senescence induced by KCl stress: nutritional imbalance, lipid peroxidation and antioxidant metabolism. J Exp Bot 52:351–360

    Article  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Edwards GE (2004) Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ. Ann Bot 93:177–187

    Article  CAS  PubMed  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    CAS  Google Scholar 

  • Yang X, Ding Z, Fan X, Zhou Z, Ma N (2007) Processes and mechanisms of desertification in northern China during the last 30 years, with a special reference to the Hunshandake Sandy Land, eastern Inner Mongolia. Catena 71:2–12

    Article  Google Scholar 

  • Yeo AR (1983) Salinity resistance: physiologies and prices. Physiol Plant 58:214–222

    Article  CAS  Google Scholar 

  • Yeo AR, Flowers TJ (1980) Salt tolerance in the halophyte Suaeda maritima L. Dum.: evaluation of the effect of salinity upon growth. J Exp Bot 31:1171–1183

    Article  CAS  Google Scholar 

  • Zenoff AM, Hilal M, Galo M, Moreno H (1994) Changes in roots lipid composition and inhibition of the extrusion of protons during salt stress in two genotypes of soybean resistant or susceptible to stress. Varietal differences. Plant Cell Physiol 35:729–735

    CAS  Google Scholar 

Download references

Acknowledgements

This work was financed by Consejo de Investigaciones de la Universidad Nacional de Tucumán (CIUNT), and Agencia Nacional de Promoción Científica y Técnica (ANPCyT), Proyecto BID-1728-OC-AR PICT Nº 23153. We thank Facultad de Ciencias Naturales and Fundación Miguel Lillo for technical assistance. F.E.P is a career investigator from CONICET.

Author information

Authors and Affiliations

  1. Cátedra de Fisiología Vegetal, Facultad de Ciencias Naturales e IML, Miguel Lillo 205, CP 4000, Tucumán, Argentina

    Ana María C. Ruffino, Mariana Rosa, Mirna Hilal & Fernando E. Prado

  2. Instituto de Ecología, Area Botánica, Fundación Miguel Lillo, Miguel Lillo 251, CP 4000, Tucumán, Argentina

    Juan A. González

  3. Facultad de Ciencias Naturales e IML, Miguel Lillo 205, CP 4000, San Miguel de Tucumán, Argentina

    Fernando E. Prado

Authors
  1. Ana María C. Ruffino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariana Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mirna Hilal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan A. González
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fernando E. Prado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando E. Prado.

Additional information

Responsible Editor: Timothy J. Flowers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruffino, A.M.C., Rosa, M., Hilal, M. et al. The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity. Plant Soil 326, 213–224 (2010). https://doi.org/10.1007/s11104-009-9999-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-9999-8

Keywords

Search

Navigation