Biochemical Characterization and Responses of Two Contrasting Genotypes of Chenopodium quinoa Willd. to Salinity in a Hydroponic System

Sirpaul Jaikishun *

College of Life Sciences and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China and Department of Biology, Faculty of Natural Sciences, University of Guyana, Guyana.

Shikui Song

College of Life Sciences and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China.

Zhenbiao Yang

College of Life Sciences and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China and Institute of Integrative Genome Biology and Department of Botany and Plant Sciences, University of California, Riverside, CA, USA.

*Author to whom correspondence should be addressed.


Abstract

Chenopodium quinoa is a promising species for future food security and combating climate change due to its nutritional content and halophytic nature. This study focuses on the temporal differential responses of the salt-tolerant (Chadmo) and the salt-sensitive (Kankolla) under control (CK) and 400 mM NaCl arranged under the randomised block designed (RBD). Biochemical features assessed and results indicate a significant difference (p<0.05) being identified by ANOVA and Tukey analyses in total chlorophyll (CHL), carotenoids (CAR), proline, glycine betaine (GB),  soluble sugars,  K+, Na+, K+/Na+ ratio, Mg2+ and Ca2+ in both genotypes between the CK and 400 mM NaCl. Na+ increased while K+ and the bivalent ions Mg2+ and Ca2+ decreased progressively with time points (CK and 24 h) in both genotypes but more pronounced in Kankolla. Proline increased by 24.45 and 18.63% between the CK and 24 h after exposure to 400 mM NaCl in Chadmo and Kankolla, respectively. Similarly, significant increases were observed in ABA, glycine betaine and soluble sugars from the CK to 24 h after exposure to 400 mM NaCl in both genotypes. Using these biochemical responses to salinity, Chadmo proved to be the better-performing genotype when exposed to 400 mM NaCl and hence identified as the salt-tolerant genotype.

Keywords: Climate change, biochemical, halophytes, nutrients, proline, quinoa, salinity, salt-tolerant


How to Cite

Jaikishun , S., Song , S., & Yang , Z. (2023). Biochemical Characterization and Responses of Two Contrasting Genotypes of Chenopodium quinoa Willd. to Salinity in a Hydroponic System. Asian Research Journal of Agriculture, 16(1), 41–54. https://doi.org/10.9734/arja/2023/v16i1381

Downloads

Download data is not yet available.

References

Wang H-L et al. Remediation of heavy metals contaminated saline soils: a halophyte choice?. Building climate resilience for food security and nutrition. 2013;2.

FAO et al. The State of Food Security and Nutrition in the World; 2018. DOI: 10.1021/es405052j.

Mujica A, Jacobsen S-E. La quinua (Chenopodium quinoa Willed.) y sus parientes silvestres. Bot Econ Andes Centrales. 2006;32:449-57.

Jarvis DE, Ho YS, Lightfoot DJ, Schmöckel SM, Li B, Borm TJ et al. The genome of Chenopodium quinoa. Nature. 2017;542(7641):307-12. doi: 10.1038/nature21370, PMID 28178233.

Valencia-Chamorro S. Quinoa. In: Encyclopedia of food science and nutrition. Vol. 8’.(Ed. B Caballero). 2003;4895-902. DOI: 10.1016/B0-12-227055-X/00995-0

Jacobsen S-E, Mujica A, Jensen CR. The Resistance of Quinoa (Chenopodium quinoa Willd.) to Adverse Abiotic Factors. Food Rev Int. 2003;19(1-2):99-109. DOI: 10.1081/FRI-120018872

Ruiz KB, Biondi S, Martínez EA, Orsini F, Antognoni F, Jacobsen S-E. Quinoa–a model crop for understanding salt-tolerance mechanisms in halophytes. Plant Biosyst. 2016;150(2):357-71. DOI: 10.1080/11263504.2015.1027317.

Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou D, Shabala S. Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol Plant. 2012;146(1):26-38. DOI: 10.1111/j.1399-3054.2012.01599.x

Bazile D, Jacobsen SE, Verniau A. The global expansion of quinoa: trends and limits. Front Plant Sci. 2016;7:622.

DOI: 10.3389/fpls.2016.00622

Jacobsen S-E, Monteros C, Corcuera LJ, Bravo LA, Christiansen JL, Mujica A. Frost resistance mechanisms in quinoa (Chenopodium quinoa Willd.). Eur J Agron. 2007;26(4):471-5. DOI: 10.1016/j.eja.2007.01.006

Prado FE et al. Effect of NaCl on germination, growth, and soluble sugar content in Chenopodium quinoa Willed. seeds. Bot Bull Acad Sin. 2000;41.

Hariadi Y, Marandon K, Tian Y, Jacobsen SE, Shabala S. Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J Exp Bot. 2011;62(1):185-93. DOI: 10.1093/jxb/erq257, PMID 20732880

Adolf VI, Shabala S, Andersen MN, Razzaghi F, Jacobsen S. Varietal differences of quinoa’s tolerance to saline conditions. Plant Soil. 2012;357(1-2): 117-29. DOI: 10.1007/s11104-012-1133-7.

Morales AJ et al. Physiological responses of Chenopodium quinoa to salt stress. Int J Plant Physiol Biochem. 2011;3:219-32. DOI:10.5897/IJPPB11.026

Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol. 2000;12(4):431-4. Doi: 10.1016/S0955-0674(00)00112-5

Brownlee C. Plant physiology: One way to dump salt. Curr Biol. 2018;28(19):R1145-7. DOI: 10.1016/j.cub.2018.08.062

Hasegawa PM. Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot. 2013;92:19-31. DOI: 10.1016/j.envexpbot.2013.03.001

Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25(2):239-50. DOI: 10.1046/j.0016-8025.2001.00808.x

Riccardi M, Pulvento C, Lavini A, d’Andria R, Jacobsen S-E. Growth and ionic content of quinoa under saline irrigation. J Agron Crop Sci. 2014;200(4):246-60. DOI: 10.1111/jac.12061

Abugoch L, Castro E, Tapia C, Añón MC, Gajardo P, Villarroel A. Stability of quinoa flour proteins (Chenopodium quinoa Willd.) during storage. Int J Food Sci Technol. 2009;44(10):2013-20. DOI: 10.1111/j.1365-2621.2009.02023.x

Aloisi I, Parrotta L, Ruiz KB, Landi C, Bini L, Cai G et al. New insight into quinoa seed quality under salinity: changes in proteomic and amino acid profiles, phenolic content, and antioxidant activity of protein extracts. Front Plant Sci. 2016;7:656. DOI: 10.3389/fpls.2016.00656

Escuredo O, González Martín MI, Wells Moncada G, Fischer S, Hernández Hierro JM. Amino acid profile of the quinoa (Chenopodium quinoa Willed.) using near-infrared spectroscopy and chemometric techniques. J Cereal Sci. 2014;60(1): 67-74. DOI: 10.1016/j.jcs.2014.01.016

Filho AM, Pirozi MR, Borges JT, Pinheiro Sant’Ana HM, Chaves JB, Coimbra JS. Quinoa: nutritional, functional, and antinutritional aspects. Crit Rev Food Sci Nutr. 2017;57(8):1618-30. DOI: 10.1080/10408398.2014.1001811

Gonzalez JA, Konishi Y, Bruno M, Valoy M, Prado FE. Interrelationships among seed yield, total protein and amino acid composition of ten quinoa (Chenopodium quinoa) cultivars from two different agroecological regions. J Sci Food Agric. 2012;92(6):1222-9. DOI: 10.1002/jsfa.4686

Repo-Carrasco R, Espinoza C, Jacobsen S-E. Nutritional value and use of the Andean crops quinoa (Chenopodium quinoa) and kañiwa (Chenopodium pallidicaule). Food Rev Int. 2003;19(1-2):179-89. DOI: 10.1081/FRI-120018884

USDA; 2005. National nutrient database for standard reference. Release 28. United States Department of Agriculture.

Chaudhary N, Walia S, Kumar R. Functional composition, physiological effect and agronomy of future food quinoa (Chenopodium quinoa Willd.): A review. J Food Compos Anal. 2023;118: 105192. DOI: 10.1016/j.jfca.2023.105192

Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Carrasco KBR et al. Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol. 2011;38(10):818-31. DOI: 10.1071/FP11088, PMID 32480939

Pulvento C, Riccardi M, Lavini A, Iafelice G, Marconi E, d’Andria R. Yield and quality characteristics of quinoa grown in open field under different saline and non-saline irrigation regimes. J Agron Crop Sci. 2012; 198(4):254-63.

DOI: 10.1111/j.1439-037X.2012.00509.x

Flowers TJ, Colmer TD. Salinity tolerance in halophytes. New Phytol. 2008;179(4):945-63.

DOI: 10.1111/j.1469-8137.2008.02531.x

Gómez-Pando LR, Álvarez-Castro R, Eguiluz-de la Barra A. Short communication: Effect of salt stress on peruvian germplasm of Chenopodium quinoa Willd.: A promising crop. J Agron Crop Sci. 2010;196(5):391-6. DOI: 10.1111/j.1439-037X.2010.00429.x

USDA, NRCS. The PLANTS Database. 15 April 2020). Greensboro, NC: National Plant Data Team. USA. p. 27401-4901; 2018. Available: https://https://plants. Available from: http://usda.gov/java/citePlants.

Hoagland DR, Arnon DI. The water-culture method for growing plants without soil; 1950. (circular. Vol. 2nd edit. CA: agricultural experiment station).

Bai J, Yan W, Wang Y, Yin Q, Liu J, Wight C et al. Screening oat genotypes for tolerance to salinity and alkalinity. Front Plant Sci. 2018;9. https://doi:10.3389/fpls.2018.01302:1302. DOI: 10.3389/fpls.2018.01302, PMID 30333838

Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39(1):205-7. DOI: 10.1007/BF00018060

Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A. Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol. 2003;158(3):455-63. DOI: 10.1046/j.1469-8137.2003.00770.x

Almeida Trapp M, De Souza GD, Rodrigues-Filho E, Boland W, Mithöfer A. Validated method for phytohormone quantification in plants. Front Plant Sci. 2014;5:417-.

DOI: 10.3389/fpls.2014.00417

Fiehn O. Metabolomics by gas chromatography–mass spectrometry: combined targeted and untargeted profiling. Curr Protoc Mol Biol, 30.34. 2016;31-30(34. 32). DOI:10.1002/0471142727.mb3004s114:30.4.1-30.4.32. DOI: 10.1002/0471142727.mb3004s114

Haliński ŁP, Stepnowski P. GC-MS and MALDI-TOF MS Profi ling of sucrose Esters from Nicotiana tabacum and Nicotiana rustica. Z Naturforsch C. 2013;68(5-6):210-22. DOI: 10.1515/znc-2013-5-607

Tandon HLS. Methods of analysis of soils, plants, waters, fertilisers & organic manures. Fertiliser development and consultation organization; 2005.

Peronico VC, Raposo JL, Jr. Ultrasound-assisted extraction for the determination of Cu, Mn, Ca, and Mg in alternative oilseed crops using flame atomic absorption spectrometry. Food Chem. 2016;196:1287-92. DOI: 10.1016/j.foodchem.2015.10.080

Sairam RK, Rao KV, Srivastava GC. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 2002;163(5):1037-46. DOI: 10.1016/S0168-9452(02)00278-9

Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K. Salt stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. Biol Plant. 2009;53(2):243-8. DOI: 10.1007/s10535-009-0046-7

Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot. 2009;103(4):551-60. DOI: 10.1093/aob/mcn125

Gomes MAdC, Pestana IA, Santa-Catarina C, Hauser-Davis RA, Suzuki MS. Salinity effects on photosynthetic pigments, proline, biomass and nitric oxide in Salvinia auriculata Aubl. Acta Limnol Bras. 2017;29. DOI: 10.1590/s2179-975x4716

Houimli SIM, Denden M, Mouhandes BD. Effects of 24-epibrassinolide on growth, chlorophyll, electrolyte leakage and proline by pepper plants under NaCl-stress. Eurasian J Biosci. 2010;4:96-104. DOI: 10.5053/ejobios.2010.4.0.12

Pinheiro HA, Silva JV, Endres L, Ferreira VM, Câmara CdA, Cabral FF et al. Leaf gas exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus communis L.) seedlings subjected to salt stress conditions. Ind Crops Prod. 2008;27(3):385-92. DOI: 10.1016/j.indcrop.2007.10.003

Ruffino AMC, Rosa M, Hilal M, González JA, Prado FE. The role of cotyledon metabolism in the establishment of quinoa (Chenopodium quinoa) seedlings growing under salinity. Plant Soil. 2010;326(1-2):213-24. DOI: 10.1007/s11104-009-9999-8

Jampeetong A, Brix H. Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. Aquat Bot. 2009;91(3):181-6. DOI: 10.1016/j.aquabot.2009.05.003

Netondo GW, Onyango JC, Beck E. Sorghum and salinity: II. Gas exchange and chlorophyll fluorescence of sorghum under salt stress. Crop Sci. 2004;44 (3):806-11. DOI: 10.2135/cropsci2004.8060

Pérez-Romero JA, Barcia-Piedras JM, Redondo-Gómez S, Mateos-Naranjo E. Impact of short-term extreme temperature events on physiological performance of Salicornia ramosissima J. Woods under optimal and sub-optimal saline conditions. Sci Rep. 2019;9(1):659. DOI: 10.1038/s41598-018-37346-4

Srivastava J et al. Effect of salt stress on physiological and biochemical parameters of wheat; 1988.

Available:http://www.cropj.com/shahid_6_5_2012_828_838.pdf

Thind S, Malik C. Carboxylation and related reactions in wheat seedlings under osmotic stress. Plant Physiol Biochem. 1988.

Upadhyay RK, Panda SK. Salt tolerance of two aquatic macrophytes, Pistia stratiotes and Salvinia molesta. Biol Plant. 2005;49(1):157-9. DOI: 10.1007/s10535-005-7159-4

Hernández JA, Olmos E, Corpas FJ, Sevilla F, del Río LA. Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci. 1995;105(2): 151-67. DOI: 10.1016/0168-9452(94)04047-8

Shahid M et al. Differential response of pea (Pisum sativum L.) Genotypes to salt stress in relation to the growth, physiological attributes antioxidant activity and organic solutes. Aust J Crop Sci. 2012;6:828.

Parida AK, Das AB, Mittra B. Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees Struct Funct. 2004;18(2):167-74. DOI: 10.1007/s00468-003-0293-8

Gadallah MAA. Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant. 1999;42(2):249-57. DOI: 10.1023/A:1002164719609

Taïbi K, Taïbi F, Ait Abderrahim L, Ennajah A, Belkhodja M, Mulet JM. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot. 2016;105:306-12.

DOI: 10.1016/j.sajb.2016.03.011

Saleh B. Effect of salt stress on growth and chlorophyll content of some cultivated cotton varieties grown in Syria. Commun Soil Sci Plant Anal. 2012;43(15): 1976-83. DOI: 10.1080/00103624.2012.693229

Centritto M, Loreto F, Chartzoulakis K. The use of low [CO2] to estimate diffusional and non‐diffusional limitations of photosynthetic capacity of salt‐stressed olive saplings. Plant Cell Environ. 2003; 26(4):585-94.

DOI: 10.1046/j.1365-3040.2003.00993.x

Bassi R, Sharma SS. Changes in proline content accompanying the uptake of zinc and copper by Lemna minor. Ann Bot. 1993;72(2):151-4. DOI: 10.1006/anbo.1993.1093

Munns R, Rawson HM. Effect of salinity on salt accumulation and reproductive development in the apical meristem of wheat and barley. Funct Plant Biol. 1999;26(5):459. DOI: 10.1071/PP99049

Naidu BP, Paleg LG, Aspinall D, Jennings AC, Jones GP. Amino acid and glycine betaine accumulation in cold-stressed wheat seedlings. Phytochemistry. 1991;30(2):407-9. DOI: 10.1016/0031-9422(91)83693-F

Rhodes D et al. Salinity, osmolytes and compatible solutes. In: Lauchli A, Luttge U, editors. Salinity, environment, plant, molecules. Netherlands: Al-Kluwer academic publishers; 2002.

Saxena P, Srivastava RP, Sharma ML. Studies on salinity stress tolerance in sugarcane varieties. Sugar Tech. 2010;12 (1):59-63. DOI: 10.1007/s12355-010-0011-y

Shabala S, Mackay A. Ion transport in halophytes. Adv Bot Res. 2011;57:151-99. DOI: 10.1016/B978-0-12-387692-8.0000 5-9

Genard H. Effect of salinity on lipid composition, glycine betaine content and photosynthetic activity in chloroplasts of Suaeda maritima. Plant Physiol Biochem. 1991;29:421-7.

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav. 2012;7(11):1456-66. DOI: 10.4161/psb.21949

Kavi Kishor PB, Hima Kumari P, Sunita MS, Sreenivasulu N. Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci. 2015;6:544. DOI: 10.3389/fpls.2015.00544.

Robinson S, Jones G. Accumulation of glycinebetaine in chloroplasts provides osmotic adjustment during salt stress. Funct Plant Biol. 1986;13(5):659-68. DOI: 10.1071/PP9860659

Schmidt R, Stransky H, Koch W. The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta. 2007;226(4):805-13. DOI: 10.1007/s00425-007-0527-x

Sharma SS, Dietz KJ. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot. 2006;57(4):711-26. DOI: 10.1093/jxb/erj073

Yang WJ, Rich PJ, Axtell JD, Wood KV, Bonham CC, Ejeta G et al. Genotypic variation for glycinebetaine in sorghum. Crop Sci. 2003;43(1):162-9. DOI: 10.2135/cropsci2003.1620

Stoleru V, Slabu C, Vitanescu M, Peres C, Cojocaru A, Covasa M et al. Tolerance of Three quinoa Cultivars (Chenopodium quinoa Willd.) to Salinity and Alkalinity Stress during Germination Stage. Agronomy. 2019;9(6):287.

DOI: 10.3390/agronomy9060287

Ruiz-Carrasco K, Antognoni F, Coulibaly AK, Lizardi S, Covarrubias A, Martínez EA et al. 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 Biochem. 2011;49(11):1333-41.

DOI: 10.1016/j.plaphy.2011.08.005

Ruiz KB, Rapparini F, Bertazza G, Silva H, Torrigiani P, Biondi S. Comparing salt-induced responses at the transcript level in a salares and coastal-lowlands landrace of quinoa (Chenopodium quinoa Willd). Environmental and Experimental Botany. 2017;139(127/142):127-42. DOI: 10.1016/j.envexpbot.2017.05.003

Niu X, Bressan RA, Hasegawa PM, Pardo JM. Ion homeostasis in NaCl stress environments. Plant Physiol. 1995;109 (3):735-42. DOI: 10.1104/pp.109.3.735

Sharma N, Gupta NK, Gupta S, Hasegawa H. Effect of NaCl salinity on photosynthetic rate, transpiration rate, and oxidative stress tolerance in contrasting wheat genotypes. Photosynthetica. 2005;43(4): 609-13. DOI: 10.1007/s11099-005-0095-x

Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q. Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. 2010;326(1-2):321-30. DOI: 10.1007/s11104-009-0011-4

Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiol Plant. 2008;133(4):651-69. DOI: 10.1111/j.1399-3054.2007.01008.x

Marschner H. Saline soils. In: Mineral nutrition of higher plants. Academic Press; 1995.

Shabala S. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot. 2013;112(7):1209-21. DOI: 10.1093/aob/mct205

Shabala S. Regulation of potassium transport in leaves: From molecular to tissue level. Ann Bot. 2003;92(5):627-34. DOI: 10.1093/aob/mcg191

Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ et al. Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis Root and Leaf Cells by controlling plasma membrane K+-permeable channels. Plant Physiol. 2006;141(4):1653-65. DOI: 10.1104/pp.106.082388.

Luan S, Lan W, Chul Lee S. Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL–CIPK network. Curr Opin Plant Biol. 2009;12(3):339-46. DOI: 10.1016/j.pbi.2009.05.003

Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S et al. Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci. 2010;123(9):1468-79. DOI: 10.1242/jcs.064352

Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008;59:651-81. DOI:10.1146/annurev.arplant.59.032607.09 2911