Abstract
The present investigation was carried out to understand the impact of carbon and nitrogen metabolism in quinoa genotypes IC411824, IC411825, EC507747 and EC507742 during pre-anthesis stage. It was observed that activities of acid invertase, sucrose synthase (cleavage) and sucrose phosphate synthase (SPS) increased up to 75 days after sowing (DAS) and this might be responsible for providing reducing sugars for the development of vegetative parts. Enhanced activities of nitrate reductase, glutamate synthase, glutamine synthetase during vegetative growth of leaves and stem at 90 DAS assist the fixation of ammonia on glutamate molecule to synthesize amino acids at early stages. However, the glutamate dehydrogenase and nitrite reductase play a central role in the re-assimilation of amides from the amino group of asparaginase. As a result, these photosynthetic products will be responsible for providing both the energy and the C-skeletons for ammonium assimilation during amino acid biosynthesis. Leaves and stem of IC411824 and IC411825 had higher total phenol and total flavonoid content. DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging activity was found to be higher in leaves of IC411825 and in stem of IC411824 and IC411825 indicating their capability to act as natural antioxidants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdelrahman M, Burritt DJ, Gupta A, Tsujimoto H, LSP Tran (2020) Heat stress effects on source–sink relationships and metabolome dynamics in wheat. J Exp Bot 71(2):543–544. https://doi.org/10.1093/jxb/erz296
Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell CAK (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A Proposed Nomenclature Plant Physiol 125(4):1912–1918. https://doi.org/10.1104/pp.125.4.1912
Aluko OO, Li C, Wang Q, Liu H (2021) Sucrose utilization for improved crop yields: a review Article. Int J Mol Sci 22(9):4704. https://doi.org/10.3390/ijms22094704
Angeli V, Miguel Silva P, CrispimMassuela D, Khan MW, Hamar A, Khajehei F, Graeff-Hönninger S, Piatti C (2020) Quinoa (Chenopodium quinoa Willd.): an overview of the potentials of the “Golden Grain” and socio-economic and environmental aspects of its cultivation and marketization. Foods 9(2):216. https://doi.org/10.3390/foods9020216
Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232. https://doi.org/10.1093/pcp/pcg030
Bakhtavar MA (2020) Afzl I (2021) Climate smart dry chain technology for safe storage of quinoa seeds. Sci Rep 10:12554. https://doi.org/10.1038/s41598-020-69190-w
Bihmidine S, Hunter CT, Johns CE, Koch KE, Braun DM (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci 4:177. https://doi.org/10.3389/fpls.2013.00177
Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200
Borges JTS, Bonomo RC, Paula CD, Oliveira LC, Cesario MC (2010) Physicochemical and nutritional characteristics and uses of Quinoa (Chenopodium quinoa Willd). Temas Agrarios 15(1):9–23
Cai Z, Xie T, Xu J (2021) Source–sink manipulations differentially affect carbon and nitrogen dynamics, fruit metabolites and yield of Sacha Inchi plants. BMC Plant Biol 21:160. https://doi.org/10.1186/s12870-021-02931-9
Claussen W, Loveys BR, Hawker JS (1985) Comparative investigations on the distribution of sucrose synthase activity and invertase activity within growing, mature and old leaves of some C3 and C4 plant species. Physiol Plant 65:275–280. https://doi.org/10.1111/j.1399-3054.1985.tb02395.x
Daubresse MC, Cren RM, Pageau K, Lelandais M, Grandjean O, Kronenberger J, 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(2):444–456. https://doi.org/10.1104/pp.105.071910
Daubresse MC, Vedele DF, 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(7):1141–1157. https://doi.org/10.1093/aob/mcq028
Dey PM (1986) Changes in the forms of invertase during germination of mung bean seeds. Phytochem 25(1):51–53. https://doi.org/10.1016/S0031-9422(00)94499-6
Drossopoulos JB, Karamanos AJ, Niavis CA (1987) Changes in ethanol soluble carbohydrates during the development of two wheat cultivars subjected to different degrees of water stress. Ann Bot 59(2):173–180. https://doi.org/10.1093/oxfordjournals.aob.a087299
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017
Duke SH, Ham GE (1976) The effect of nitrogen addition on N2 fixation and on glutamate dehydrogenase and glutamate synthase activities in nodules and roots of soybeans inoculated with various strains of Rhizobium japonicum. Plant Cell Physiol 17(5):1037–1044. https://doi.org/10.1093/oxfordjournals.pcp.a075349
Elliott WH (1953) Isolation of glutamine synthetase and glutamotransferase from green peas. J Biol Chem 201(2):661–672
Farrar J, Pollock C, Gallagher J (2000) Sucrose and the integration of metabolism in vascular plants. Plant Sci 154(1):1–11. https://doi.org/10.1016/S0168-9452(99)00260-5
Fernandez FI, Marinetto J, Royo C, Ramos JM, Del Moral LG (2000) Amino acid composition and protein and carbohydrate accumulation in the grain of triticale grown under terminal water stress simulated by a senescing agent. J Cereal Sci 32(3):249–258. https://doi.org/10.1006/jcrs.2000.0329
Fernie AR, Bachem CWB, Helariutta Y, Neuhaus HE, Prat S, Ruan YL, Sonnewald U (2020) Synchronization of developmental, molecular and metabolic aspects of source–sink interactions. Nature Plants 6(2):55–66. https://doi.org/10.1038/s41477-020-0590-x
Groenewald JH, Botha FC (2008) Down-regulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes. Transgenic Res 17(1):85–92. https://doi.org/10.1007/s11248-007-9079-x
Hageman RH, Hucklesby DP (1971) Nitrate reductase from higher plants. Methods Enzymol 23:491–503. https://doi.org/10.1016/S0076-6879(71)23121-9
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334. https://doi.org/10.1139/b79-163
Hsiao-Ling C, Xiang-Zhen L, Yan-Yi W, Yu-Wen O, Tsung Chi C, Wen-Tzu W (2017) The antioxidant activity and nitric oxide production of extracts obtained from the leaves of Chenopodium quinoa Willd,. 7(4) doi: https://doi.org/10.1051/bmdcn/2017070424
Huber SC, Huber JL, McMichael RW (1994) Control of plant enzyme activity by reversible protein phosphorylation. Int Rev Cytol 149:47–98. https://doi.org/10.1016/S0074-7696(08)62086-0
Ivanova TV, Maiorova OV, Orlova YV, Kuznetsova EI, Khalilova LA, Myasoedov N, Tsydendambaev VD (2016) Cell ultrastructure and fatty acid composition of lipids in vegetative organs of Chenopodium album L. under salt stress conditions. Russian J Plant Physiol 63(6):763–775
Joy KW, Hageman RH (1966) The purification and properties of nitrite reductase from higher plants, and its dependence on ferredoxin. Biochem J 100(1):263–273. https://doi.org/10.1042/bj1000263
Kaur H, Peel A, Acosta K, Gebril S, Ortega JL, Sengupta-Gopalan C (2019) Comparison of alfalfa plants overexpressing glutamine synthetase with those overexpressing sucrose phosphate synthase demonstrates a signaling mechanism integrating carbon and nitrogen metabolism between the leaves and nodules. Plant Direct 3(1):e00115. https://doi.org/10.1002/pld3.115
Kerr PS, Torres KW, Huber SC (1987) Resolution of two molecular forms of sucrose-phosphate synthase from maize, soybean and spinach leaves. Planta 170(4):515–519
Keys AJ (2006) The re-assimilation of ammonia produced by photorespiration and the nitrogen economy of C3 higher plants. Photosynth Res 87:65. https://doi.org/10.1007/s11120-005-9024-x
Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Cur Opin Plant Biol 7(3):235–246. https://doi.org/10.1016/j.pbi.2004.03.014
Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14(1):71–77. https://doi.org/10.1016/0003-2697(66)90057-1
Li M, Li C, Allen A, Stanley CA, Smith TJ (2011) The structure and allosteric regulation of glutamate dehydrogenase. Neurochem Int 59(4):445–455. https://doi.org/10.1016/j.neuint.2010.10.017
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275
Miller AH, Fan X, Orsel M, Smith SL, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58(9):2297–2306. https://doi.org/10.1093/jxb/erm066
Misra S, Oaks A (1981) Enzymes of nitrogen assimilation during seed development in normal and high lysine mutants in maize (Zea mays, W64A). Can J Bot 59(12):2735–2743. https://doi.org/10.1139/b81-323
Mugford ST, Fernandez O, Brinton J, Flis A, Krohn N, Encke B, Smith AM (2014) Regulatory properties of ADP glucose pyrophosphorylase are required for adjustment of leaf starch synthesis in different photoperiods. Plant Physiol 166(4):1733–1747. https://doi.org/10.1104/pp.114.247759
Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153(2):375–379. https://doi.org/10.1016/s0021-9258(18)71980-7
Noor S, Punekar NS (2005) Allosteric NADP-glutamate dehydrogenase from aspergilli: purification, characterization and implications for metabolic regulation at the carbon–nitrogen interface. Microbiol 151(5):1409–1419. https://doi.org/10.1099/mic.0.27751-0
Plett DC, Holtham LR, Okamoto M, Garnett TP (2018) Nitrate uptake and its regulation in relation to improving nitrogen use efficiency in cereals. Semin Cell Dev Biol 74:97–104. https://doi.org/10.1016/j.semcdb.2017.08.027
Pollock CJ, Farrar JF (1996) Source-sink relations: the role of sucrose. Photosynthesis Environ, pp. 261–279. https://doi.org/10.1007/0-306-48135-9_10
Pulvento C, Riccardi M, Lavini A, Iafelice G, Marconi E, Andria DR (2012) Yield and quality characteristics of quinoa grown in open field under different saline and non-saline irrigation regimes. J Agron Crop Sci 198(4):254–263. https://doi.org/10.1111/j.1439-037X.2012.00509.x
Qazi HA, Paranjpe S, Bhargava S (2012) Stem sugar accumulation in sweet sorghum–activity and expression of sucrose metabolizing enzymes and sucrose transporters. J Plant Physio 169(6):605–613. https://doi.org/10.1016/j.jplph.2012.01.005
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) seedling. Plant Physiol Biochem 47(4):300–307. https://doi.org/10.1016/j.plaphy.2008.12.001
Sathee L, Jha SK, Rajput OS, Singh D, Kumar S, Kumar A (2021) Expression dynamics of genes encoding nitrate and ammonium assimilation enzymes in rice genotypes exposed to reproductive stage salinity stress. Plant Physiol Biochem 165:161–172. https://doi.org/10.1016/j.plaphy.2021.05.013
Schaffer AA, Sagee O, Goldschmidt EE, Goren R (1987) Invertase and sucrose synthase activity, carbohydrate status and endogenous IAA levels during citrus leaf development. Physiol Plant 69(1):151–155. https://doi.org/10.1111/j.1399-3054.1987.tb01959.x
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149. https://doi.org/10.1111/j.1365-3040.2007.01708.x
Sonnewald U, Willmitzer L (1992) Molecular approaches to sink-source interactions. Plant Physiol 99(4):1267–1270. https://doi.org/10.1104/pp.99.4.1267
Swain T, Hillis WE (1959) The phenolic constituents of Prunus domestica. I.—The quantitative analysis of phenolic constituents. J Sci Food Agric 10:63–68. https://doi.org/10.1002/jsfa.2740100110
Turhan E, Ergin S (2012) Soluble sugars and sucrose-metabolizing enzymes related to cold acclimation of sweet cherry cultivars grafted on different root stocks. Sci World J 979682. https://doi.org/10.1100/2012/979682
Unno H, Uchida T, Sugawara H, Kurisu G, Sugiyama T, Yamaya T, Kusunoki M (2006) Atomic structure of plant glutamine synthetase: a key enzyme for plant productivity. J Biol Chem 281(39):29287–29296. https://doi.org/10.1074/jbc.M601497200
Van Handel E (1968) Direct micro determination of sucrose. Anal Biochem 22:280–283. https://doi.org/10.1016/0003-2697(68)90317-5
Vazquez-Luna A, Pimentel Cortés V, Fuentes Carmona F, Díaz-Sobac R (2019) Quinoa leaf as a nutritional alternative. Cien Inv Agr 46(2):137–143. https://doi.org/10.7764/rcia.v46i2.2098
Verma AK, Upadhyay SK, Verma PC, Solomon S, Singh SB (2011) Functional analysis of sucrose phosphate synthase (SPS) and sucrose synthase (SS) in sugarcane (Saccharum) cultivars. Plant Biol 13(2):325–332. https://doi.org/10.1111/j.1438-8677.2010.00379.x
Wang DR, Han R, Wolfrum EJ, McCouch SR (2017) The buffering capacity of stems: genetic architecture of non structural carbohydrates in cultivated Asian rice. Oryza Sativa New Phytol 215(2):658–671. https://doi.org/10.1111/nph.14614
Wu Y, Xia M, Zhao N, Tu L, Xue D, Zhang X, Wang M (2021) Metabolic profile of main organic acids and its regulatory mechanism in solid-state fermentation of Chinese cereal vinegar. Food Res Int 145:110400. https://doi.org/10.1016/j.foodres.2021.110400
Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Ann Rev Plant Bio 63:153–182. https://doi.org/10.1146/annurev-arplant-042811-105532
Yoshida S (1976) Determination of sugar and starch in plant tissue. Laboratory manual for physiological studies of rice. Los Banos, the Philippines: Int Rice Res Institute: 46–49
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559. https://doi.org/10.1016/S0308-8146(98)00102-2
Author information
Authors and Affiliations
Contributions
SKG was involved in planning all the aspects of research, supervision, and editing of the manuscript. S performed the experiments, analysed the data, and wrote the manuscript. RKG contributed in the planning, raising of the crop in the field, and editing of the manuscript. All the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no competing interests.
Additional information
Handling Editor: Peter Nick
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sonali, Grewal, S.K. & Gill, R.K. Insights into carbon and nitrogen metabolism and antioxidant potential during vegetative phase in quinoa (Chenopodium quinoa Willd.). Protoplasma 259, 1301–1319 (2022). https://doi.org/10.1007/s00709-022-01736-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-022-01736-3