Skip to main content
Log in

Water deficit stress-induced changes in carbon and nitrogen partitioning in Chenopodium quinoa Willd.

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Water deficit stress followed by re-watering during grain filling resulted in the induction of the ornithine pathway and in changes in Quinoa grain quality.

The genetic diversity of Chenopodium quinoa Willd. (Quinoa) is accompanied by an outstanding environmental adaptability and high nutritional properties of the grains. However, little is known about the biochemical and physiological mechanisms associated with the abiotic stress tolerance of Quinoa. Here, we characterized carbon and nitrogen metabolic changes in Quinoa leaves and grains in response to water deficit stress analyzing their impact on the grain quality of two lowland ecotypes (Faro and BO78). Differences in the stress recovery response were found between genotypes including changes in the activity of nitrogen assimilation-associated enzymes that resulted in differences in grain quality. Both genotypes showed a common strategy to overcome water stress including the stress-induced synthesis of reactive oxygen species scavengers and osmolytes. Particularly, water deficit stress induced the stimulation of the ornithine and raffinose pathways. Our results would suggest that the regulation of C- and N partitioning in Quinoa during grain filling could be used for the improvement of the grain quality without altering grain yields.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

GDH:

Glutamate dehydrogenase

GS:

Glutamine synthetase

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

References

  • Aguilar PC, Jacobsen SE (2003) Cultivation of Quinoa on the Peruvian Altiplano. Food Rev Int 19:31–41

    Article  Google Scholar 

  • Allen AE, Dupont CL, Obornik M, Horak A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473:203–207

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Jubete L, Arendt EK, Gallagher E (2010) Nutritive value of pseudocereals and their increasing use as functional gluten-free ingredients. Trends Food Sci Technol 21:106–113

    Article  CAS  Google Scholar 

  • Alvarez-Suarez JM, Giampieri F, Tulipani S, Casoli T, Di Stefano G, González-Paramás AM, Santos-Buelga C, Busco F, Quiles JL, Cordero MD, Bompadre S, Mezzetti B, Battino M (2014) One-month strawberry-rich anthocyanin supplementation ameliorates cardiovascular risk, oxidative stress markers and platelet activation in humans. J Nutr Biochem 25:289–294

    Article  PubMed  CAS  Google Scholar 

  • An Y, Zhang M, Liu G, Han R, Liang Z (2013) Proline accumulation in leaves of Periploca sepium via both biosynthesis up-regulation and transport during recovery from severe drought. PLoS One. doi:10.1371/journal.pone.0069942

    Google Scholar 

  • Bates LS, Waldren RP, Teare IK (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Berg JM, Tymoczko JL, Stryer L (2002) Ammonium ion is converted into urea in most terrestrial vertebrates. In: Berg JM, Tymoczko JL, Stryer L (eds) Biochemistry. Freeman WH and Company, New York, pp 959–965

    Google Scholar 

  • Bois JF, Winkel T, Lhomme JP, Raffaillac JP, Rocheteau A (2006) Response of some Andean cultivars of quinoa (Chenopodium quinoa Willd.) to temperature: effects on germination, phenology, growth and freezing. Eur J Agron 25:299–308

    Article  Google Scholar 

  • Botanga CJ, Bethke G, Chen Z, Gallie DR, Fiehn O, Glazebrook J (2012) Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Mol Plant Microbe In 25:1628–1638

    Article  CAS  Google Scholar 

  • Carletti G, Lucini L, Busconi M, Marocco A, Bernardi J (2013) Insight into the role of anthocyanin biosynthesis-related genes in Medicago truncatula mutants impaired in pigmentation in leaves. Plant Physiol Biochem 70:123–132

    Article  PubMed  CAS  Google Scholar 

  • Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253

    Article  PubMed  CAS  Google Scholar 

  • Cvikrova M, Gemperlova L, Martincova O, Vankova R (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiol Biochem 73:7–15

    Article  PubMed  CAS  Google Scholar 

  • da Rocha IM, Vitorello VA, Silva JS, Ferreira-Silva SL, Viégas RA, Silva EN, Silveira JA (2012) Exogenous ornithine is an effective precursor and the δ-ornithine amino transferase pathway contributes to proline accumulation under high N recycling in salt-stressed cashew leaves. J Plant Physiol 161:41–49

    Article  CAS  Google Scholar 

  • Derkx AP, Orford S, Griffiths S, Foulkes MJ, Hawkesford MJ (2012) Identification of differentially senescing mutants of wheat and impacts on yield, biomass and nitrogen partitioning. J Integr Plant Biol 54:555–566

    Article  PubMed  CAS  Google Scholar 

  • Doane TA, Horwáth WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722

    Article  CAS  Google Scholar 

  • Duan JZ, Zhang MH, Zhang HL, Xiong HY, Liu PL, Ali J, Li JJ, Li Z (2012) OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci 196:143–151

    Article  PubMed  CAS  Google Scholar 

  • FAO (2011) Quinoa: an ancient crop to contribute to world food security. Food and Agricultural Organization of the United Nations. http://www.fao.org/docrep/017/aq287e/aq287e.pdf. Accessed 2 July 2011

  • Forster JC (1995) Soil nitrogen. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, San Diego, pp 79–87

    Google Scholar 

  • Fuentes FF, Martinez EA, Hinrichsen PV, Jellen EN, Maughan PJ (2009) Assessment of genetic diversity patterns in Chilean quinoa (Chenopodium quinoa Willd.) germplasm using multiplex fluorescent microsatellite markers. Conserv Genet 10:369–377

    Article  CAS  Google Scholar 

  • Fuentes FF, Bazile D, Bhargava A, Martinez EA (2012) Implications of farmers’ seed exchanges for on-farm conservation of quinoa, as revealed by its genetic diversity in Chile. J Agr Sci 150:702–716

    Article  Google Scholar 

  • Gonzalez JA, Bruno M, Valoy M, Prado FE (2011) Genotypic variation of gas exchange parameters and leaf stable carbon and nitrogen isotopes in ten quinoa cultivars grown under drought. Agron Crop Sci 197:81–93

    Article  Google Scholar 

  • Gorai M, Laajili W, Santiago LS, Neffati M (2015) Rapid recovery of photosynthesis and water relations following soil drying and re-watering is related to the adaptation of desert shrub Ephedra alata subsp. alenda (Ephedraceae) to arid environments. Environ Exp Bot 109:113–121

    Article  CAS  Google Scholar 

  • Hacham Y, Avraham T, Amir R (2002) The N-terminal region of Arabidopsis cystathionine γ-synthase plays an important regulatory role in methionine metabolism. Plant Physiol 128:454–462

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hariadi Y, Marandon K, Tian Y, Jacobsen SE, Shabala S (2011) Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J Exp Bot 62:185–193

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937

    Article  PubMed  Google Scholar 

  • Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9:537–548

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Monteros C, Corcuera LJ, Bravo LA, Christiansen JL, Mujica A (2007) Frost resistance mechanisms in quinoa (Chenopodium quinoa Willd.). Eur J Agron 26:471–475

    Article  Google Scholar 

  • Kalamaki MS, Alexandrou D, Lazari D, Merkouropoulos G, Fotopoulos V, Pateraki I, Aggelis A, Carrillo-Lopez A, Rubio-Cabetas MJ, Kanellis AK (2009) Over-expression of a tomato N-acetyl-L-glutamate synthase gene (SlNAGS1) in Arabidopsis thaliana results in high ornithine levels and increased tolerance in salt and drought stresses. J Exp Bot 60:1859–1871

    Article  PubMed Central  PubMed  Google Scholar 

  • Karner U, Peterbauer T, Raboy V, Jones DA, Hedley CL, Richter A (2004) myo-Inositol and sucrose concentrations affect the accumulation of raffinose family oligosaccharides in seeds. J Exp Bot 55:1981–1987

    Article  PubMed  CAS  Google Scholar 

  • Kind T, Fiehn O (2006) Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm. BMC Bioinform 7:234. doi:10.1186/1471-2105-7-234

    Article  CAS  Google Scholar 

  • Kjeldahl J (1883) A new method for the determination of nitrogen in organic matter. Z Anal Chem 22:366–382

    Article  Google Scholar 

  • Linka M, Weber APM (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends Plant Sci 10:461–465

    Article  PubMed  CAS  Google Scholar 

  • Mancinelli AL (1984) Photoregulation of anthocyanin synthesis: VIII. Effect of light pretreatments. Plant Physiol 75:447–453

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martínez EA, Veas E, Jorquera C, San Martín R, Jara P (2009) Re-introduction of quínoa into arid Chile: cultivation of two lowland races under extremely low irrigation. J Agron Crop Sci 195:1–10

    Article  Google Scholar 

  • Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K, Lelandais M, Grandjean O, Kronenberger J, Valadier M-H, Feraud M, Jouglet T, Suzuki A (2006) Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol 140:444–456

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157

    Article  PubMed Central  PubMed  Google Scholar 

  • Miller G, Stein H, Honig A, Kapulnik Y, Zilberstein A (2005) Responsive modes of Medicago sativa proline dehydrogenase genes during salt stress and recovery dictate free proline accumulation. Planta 222:70–79

    Article  PubMed  CAS  Google Scholar 

  • Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175. doi:10.3389/fpls.2014.00175

    Article  PubMed Central  PubMed  Google Scholar 

  • Miret JA, Munné-Bosch S (2015) Redox signaling and stress tolerance in plants: a focus on vitamin E. Ann N Y Acad Sci 1340:29–38

    Article  PubMed  CAS  Google Scholar 

  • Monreal JA, Jimenez ET, Remesal E, Morillo-Velarde R, Garcia-Maurino S, Echevarria C (2007) Proline content of sugar beet storage roots: response to water deficit and nitrogen fertilization at field conditions. Environ Exp Bot 60:257–267

    Article  CAS  Google Scholar 

  • Neff MM, Chory J (1998) Genetic Interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 118:27–35

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ortega-Villasante C, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251

    Article  PubMed  CAS  Google Scholar 

  • Pasko P, Bartoń H, Zagrodzki P, Gorinstein S, Fołta M, Zachwieja Z (2009) Anthocyanins, total polyphenols and antioxidant activity in amaranth and quinoa seeds and sprouts during their growth. Food Chem 115:994–998

    Article  CAS  Google Scholar 

  • Pasko P, Zagrodzki P, Barton H, Chlopicka J, Gorinstein S (2010) Effect of quinoa seeds (Chenopodium quinoa) in diet on some biochemical parameters and essential elements in blood of high fructose-fed rats. Plant Foods Hum Nutr 65:333–338

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pinheiro C, Chaves MM (2010) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  PubMed  CAS  Google Scholar 

  • Razzaghi F, Ahmadi SH, Adolf VI, Jensen CR, Jacobsen SE, Andersen MN (2011) Water relations and transpiration of quinoa (Chenopodium quinoa Willd.) under salinity and soil drying. J Agron Crop Sci 197:348–360

    Article  Google Scholar 

  • Razzaghi F, Plauborg F, Jacobsen S-E, Jensen CR, Andersen MN (2012a) Effect of nitrogen and water availability of three soil types on yield, radiation use efficiency and evapotranspiration in field-grown quinoa. Agr Water Manage 109:20–29

    Article  Google Scholar 

  • Razzaghi F, Ahmadi SH, Jacobsen SE, Jensen CR, Andersen MN (2012b) Effects of salinity and soil–drying on radiation use efficiency, water productivity and yield of quinoa (Chenopodium quinoa Willd.). J Agron Crop Sci 198:173–184

    Article  CAS  Google Scholar 

  • Razzaghi F, Jacobsen S-E, Jensen CR, Andersen MN (2015) Ionic and photosynthetic homeostasis in quinoa challenged by salinity and drought—mechanisms of tolerance. Funct Plant Biol 42:136–148

    Article  CAS  Google Scholar 

  • Reguera M, Peleg Z, Abdel-Tawab YM, Tumimbang EB, Delatorre CA, Blumwald E (2013) Stress-induced cytokinin synthesis increases drought tolerance through the coordinated regulation of carbon and nitrogen assimilation in rice. Plant Physiol 163:1609–1622

    Article  PubMed Central  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Ruiz K, Biondi S, Oses R, Acuña-Rodríguez I, Antognoni F, Martinez-Mosqueira E, Coulibaly A, Canahua-Murillo A, Pinto M, Zurita-Silva A, Bazile D, Jacobsen S-E, Molina-Montenegro M (2014) Quinoa biodiversity and sustainability for food security under climate change. A review. Agron Sustain Dev 34:349–359

    Article  Google Scholar 

  • Shabala S, 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

    Article  PubMed  CAS  Google Scholar 

  • Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM (2008) Higher plant antioxidants and redox signaling under environmental stresses. C R Biol 331:433–441

    Article  PubMed  CAS  Google Scholar 

  • Shelp BJ, Brown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452

    Article  PubMed  Google Scholar 

  • Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1:1342–1345

    Article  PubMed  CAS  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  PubMed  CAS  Google Scholar 

  • Varisi VA, Camargos LS, Aguiar LF, Christofoleti RM, Medici LO, Azevedo RA (2008) Lysine biosynthesis and nitrogen metabolism in quinoa (Chenopodium quinoa): study of enzymes and nitrogen-containing compounds. Plant Physiol Biochem 46:11–18

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Zhang J (2006) Grain filling of cereals under soil drying. New Phytol 169:223–236

    Article  PubMed  CAS  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Zhu QS, Liu LJ (2003) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell Environ 26:1621–1631

    Article  CAS  Google Scholar 

  • Yokota A, Kawasaki S, Iwano M, Nakamura C, Miyake C, Akashi K (2002) Citrulline and DRIP-1 protein (ArgE homologue) in drought tolerance of wild watermelon. Ann Bot 89:825–832

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • You J, Hu H, Xiong L (2012) An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci 197:59–69

    Article  PubMed  CAS  Google Scholar 

  • Zurita-Silva A, Fuentes F, Zamora P, Jacobsen SE, Schwember AR (2014) Breeding quinoa (Chenopodium quinoa Willd.): potential and perspectives. Mol Breed 34:13–30

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by Fondecyt Initiation No 11130480 to L.B.-G. and by the Will W. Lester Endowment of the University of California to E.B. We thank Dr. Pedro León Lobos at the INIA-Intihuasi Chile National Seed Bank Repository and Cooperative “Las Nieves” for providing the Quinoa seeds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luisa Bascuñán-Godoy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

L. Bascuñán-Godoy and M. Reguera contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2015_2424_MOESM1_ESM.jpg

Supplementary material 1: Effects of water stress and re-watering on relative water content and soil water content of two genotypes of Chenopodium quinoa. Relative water content (a) and soil water content (b) was calculated every 2 days during water stress and after 3 days of re-watering. Values are mean ± SD (n = 6). Significant differences between conditions were indicated by asterisks using one-way ANOVA followed by Tukey t test. Asterisks indicate significant differences respect to initial condition for each of the genotypes (P ≤ 0.05) (JPEG 448 kb)

425_2015_2424_MOESM2_ESM.jpg

Supplementary material 2: Effects of water stress and re-watering on photosynthesis of two genotypes of Chenopodium quinoa. A/Ci curves (net CO2 assimilation rate versus CO2 concentration (Ci)) were performed at zero (a), two (b), four (c) and six days of water stress (d), and after 3 days of re-watering (e). Fully expanded third leaves (from the top part of the plant) were used for the photosynthetic measurements. Values are mean ± SD (n = 6). Significant differences between conditions were indicated by asterisks using one-way ANOVA followed by Tukey t-test. Asterisks indicate significant differences by condition for each of the genotypes (P ≤ 0.05) (JPEG 738 kb)

Supplementary material 3 (PDF 148 kb)

Supplementary material 4 (PDF 288 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bascuñán-Godoy, L., Reguera, M., Abdel-Tawab, Y.M. et al. Water deficit stress-induced changes in carbon and nitrogen partitioning in Chenopodium quinoa Willd.. Planta 243, 591–603 (2016). https://doi.org/10.1007/s00425-015-2424-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2424-z

Keywords

Navigation