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https://doi.org/10.53941/plantecophys.2025.100004
Ostria-Gallardo, E., Cabrera, V., Zúñiga-Contreras, E., Ortiz, J., Bravo, L., Coba de La Peña, T., Cuevas, J. G., & Bascuñán, L. Nitrogen-Driven Changes in Metabolic Profile Modulate Photosynthetic Performance and Antioxidant Defense of Amaranthus cruentus. Plant Ecophysiology. 2025. doi: https://doi.org/10.53941/plantecophys.2025.100004
Volume 1, Issue 1, 2025
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Article

Nitrogen-Driven Changes in Metabolic Profile Modulate Photosynthetic Performance and Antioxidant Defense of Amaranthus cruentus

Enrique Ostria-Gallardo 1,*, Valentina Cabrera 1, Estrella Zúñiga-Contreras 2, José Ortiz1, León Bravo 3, Teodoro Coba de La Peña 2, Jaime G. Cuevas 2 and Luisa Bascuñán-Godoy 1

1 Laboratorio de Fisiología Vegetal, Departamento de Botánica, Facultad de Cs. Naturales y Oceanográficas, Universidad de Concepción, Concepción 4030000, Chile

2 Centro de Estudios Avanzados en Zonas Áridas, CEAZA, La Serena 1700000, Chile

3 Laboratorio de Fisiología y Biología Molecular Vegetal, Instituto de Agroindustria, Departamento de Ciencias Agronómicas y Recursos Naturales, Facultad de Ciencias Agropecuarias y Medioambiente, Universidad de La Frontera, Temuco 4780000, Chile

* Correspondence: eostria@udec.cl; Tel.: +56-41-2661032

Received: 10 August 2024; Revised: 6 March 2025; Accepted: 12 March 2025; Published: 14 March 2025

Abstract: Nitrogen is crucial for plant development and crop production. Amaranthus cruentus, a C4 species, has been pointed out as a high-nutritious and stress resilient crop. Here we studied the effects of sufficient and low nitrogen supplementation on the photosynthetic efficiency and metabolic responses of A. cruentus. Photochemical parameters from dark-adapted and transient chlorophyll fluorescence measurements, antioxidant enzymes activity, and metabolomic analysis, were evaluated to depict the impact of nitrogen availability. Photochemical parameters showed a significant decrease compared to those from gas exchange. The antioxidant enzymes activity revealed variations among treatments, being important at low nitrogen availability. At the metabolic level, there is a significant accumulation of L-glutamine, aromatic amino acids and ascorbic acid in A. cruentus with sufficient nitrogen. At low nitrogen, the metabolic profile of A. cruentus suggests stabilization of membrane structure and efficient use of available nitrogen by accumulating L-glutamic acid. The differential accumulation of L-glutamine and L-glutamic acid reflects an adaptive strategy for maintaining nitrogen. Nitrogen-rich conditions, the plant stores excess nitrogen as L-glutamine, while in deficiency, it utilizes L-glutamic acid for essential metabolic functions. Overall, A. cruentus activates a coordinated metabolic strategy under LN to optimize nitrogen use. This includes effective ROS detoxification via both enzymatic and non-enzymatic antioxidants, structural reinforcement through membrane-stabilizing lipids, and efficient nitrogen storage and redistribution to meet metabolic demands during nitrogen limitation.

Keywords:

nitrogen supplementation chlorophyl fluorescence gas exchange antioxidant activity metabolic profiling

References

  1. Agati G, Brunetti C, Fini A, Gori A, Guidi L, Landi M, & Tattini M. (2020). Are flavonoids effective antioxidants in plants? Twenty years of our investigation. Antioxidants, 9(11), 1098. https://doi.org/10.3390/antiox9111098
  2. Bradford MM. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72(1–2), 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
  3. Brueck H. (2008). Effect of nitrogen supply on water-use efficiency of higher plants. Plant Nutrition and Soil Science, 171(2), 210–219. https://doi.org/10.1002/jpln.200700080
  4. Cechin I, & Valquilha ÉM. (2019). Nitrogen effect on gas exchange characteristics, dry matter production and nitrate accumulation of Amaranthus cruentus L. Brazilian Journal of Botany, 42, 373–381. https://doi.org/10.1007/s40415-019-00542-1
  5. Cechin I, da Silva LP, Ferreira ET, Barrochelo SC, de Melo FPdSR, Dokkedal AL, & Saldanha LL. (2022). Physiological responses of Amaranthus cruentus L. to drought stress under sufficient- and deficient-nitrogen conditions. PLoS ONE, 17(7), e0270849. https://doi.org/10.1371/journal.pone.0270849
  6. Chow PS, & Landhäusser SM. (2004). A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiology, 24(10), 1129–1136. https://doi.org/10.1093/treephys/24.10.1129
  7. Cifuentes L, González M, Pinto-Irish K, Álvarez R, Coba de la Peña T, Ostria-Gallardo E, Franck N, Fischer S, Barros G, Castro C, Ortiz J, Sanhueza C, Del-Saz NF, Bascunan-Godoy L, & Castro PA. (2023). Metabolic imprint induced by seed halo-priming promotes a differential physiological performance in two contrasting quinoa ecotypes. Frontiers in Plant Science, 13, 1034788. https://doi.org/10.3389/fpls.2022.1034788
  8. Colin LA, & Jaillais Y. (2020). Phospholipids across scales: Lipid patterns and plant development. Current Opinion in Plant Biology, 53, 1–9. https://doi.org/10.1016/j.pbi.2019.08.007
  9. Ding H, Wang B, Han Y, & Li S. (2020). The pivotal function of dehydroascorbate reductase in glutathione homeostasis in plants. Journal of Experimental Botany, 71(12), 3405–3416. https://doi.org/10.1093/jxb/eraa107
  10. Hamada, A., Tanaka, Y., Ishikawa, T., & Maruta, T. (2023). Chloroplast dehydroascorbate reductase and glutathione cooperatively determine the capacity for ascorbate accumulation under photooxidative stress conditions. The Plant journal: for cell and molecular biology. https://doi.org/10.1111/tpj.16117
  11. Kramer DM, Johnson G, Kiirats O, & Edwards GE. (2004). New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research, 79(2), 209–218. https://doi.org/10.1023/B:PRES.0000015391.99477.0d
  12. Lee K, Liao H, & Hsieh M. (2023). Glutamine metabolism, sensing, and signaling in plants. Plant & Cell Physiology, 64(12), 1466–1481. https://doi.org/10.1093/pcp/pcad054
  13. Li C, Yang Z, Zhang C, Luo J, Jiang N, Zhang F, & Zhu W. (2023). Heat Stress Recovery of Chlorophyll Fluorescence in Tomato (Lycopersicon esculentum Mill.) Leaves through Nitrogen Levels. Agronomy, 13(12), 2858. https://doi.org/10.3390/agronomy13122858
  14. Marečková M, Barták M, & Hájek J. (2019). Temperature effects on photosynthetic performance of Antarctic lichen Dermatocarpon polyphyllizum: A chlorophyll fluorescence study. Polar Biology, 42, 685–701. https://doi.org/10.1007/s00300-019-02464-w
  15. Mariem S, González-Torralba J, Collar C, Aranjuelo Í, & Morales F. (2020). Durum Wheat Grain Yield and Quality under Low and High Nitrogen Conditions: Insights into Natural Variation in Low- and High-Yielding Genotypes. Plants, 9(12), 1636. https://doi.org/10.3390/plants9121636
  16. Maxwell K, & Johnson GN. (2000). Chlorophyll fluorescence—A practical guide. Journal of Experimental Botany, 51(345), 659–668. https://doi.org/10.1093/jexbot/51.345.659
  17. Netshimbupfe M, Berner J, & Gouws C. (2022). The interactive effects of drought and heat stress on photosynthetic efficiency and biochemical defense mechanisms of Amaranthus species. Plant-Environment Interactions, 3(5), 212–225. https://doi.org/10.1002/pei3.10092
  18. Ostria-Gallardo E, Larama G, Berríos G, Fallard A, Gutiérrez-Moraga A, Ensminger I, Manque P, Bascuñán-Godoy L, & Bravo LA. (2020). Decoding gene networks modules that explain the recovery of Hymenoglossum cruentum Cav. after extreme desiccation. Frontiers in Plant Science, 11, 574. https://doi.org/10.3389/fpls.2020.00574
  19. Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gomez M, & del Río LA. (2014). Antioxidative enzymes from chloroplasts, mitochondria, peroxisomes, and cytosol. Plant Peroxisomes in JM Palma, FJ Corpas, LA del Río (eds.), pp. 1–35. https://doi.org/10.1007/978-94-007-6889-5_12
  20. Pang Z, Lu Y, Zhou G, Hui F, Xu L, Viau C, & Xia J. (2024). MetaboAnalyst 6.0: Towards a unified platform for metabolomics data processing, analysis and interpretation. Nucleic Acids Research, 52(W1), W398–W406. https://doi.org/10.1093/nar/gkae253
  21. Peng J, Feng Y, Wang X, Li J, Xu G, Phonenasay S, Luo Q, Han Z, & Lu W. (2021). Effects of nitrogen application rate on the photosynthetic pigment, leaf fluorescence characteristics, and yield of indica hybrid rice and their interrelations. Scientific Reports, 11, 7485, https://doi.org/10.1038/s41598-021-86858-z
  22. Perera-Castro A, & Flexas J. (2023). The ratio of electron transport to assimilation (ETR/An): Underutilized but essential for assessing both equipment’s proper performance and plant status. Planta, 257, 29. https://doi.org/10.1007/s00425-022-04063-2
  23. Plett D, Ranathunge K, Melino V, Kuya N, Uga Y, & Kronzucker H. (2020). The intersection of nitrogen nutrition and water use in plants: New paths toward improved crop productivity. Journal of Experimental Botany, 71(15), 4452–4468. https://doi.org/10.1093/jxb/eraa049
  24. Pollastrini M, Brüggeman W, Fotelli M, & Bussotti F. (2022). Downregulation of PSI regulates photosynthesis in early successional tree species. Evidence from a field survey across European forests. Journal of Photochemistry and Photobiology, 12, 100145. https://doi.org/10.1016/j.jpap.2022.100145
  25. Purcell LC, & King CA. (1996). Drought and nitrogen source effects on nitrogen nutrition, seed growth, and yield in soybean. Journal of Plant Nutrition, 19(6), 969–993. https://doi.org/10.1080/01904169609365173
  26. Ren B, Dong S, Zhao B, Liu P, & Zhang J. (2017). Responses of nitrogen metabolism, uptake and translocation of maize to waterlogging at different growth stages. Frontiers in Plant Science, 8, 1216. https://doi.org/10.3389/fpls.2017.01216
  27. Rice-Evans C, Miller N, & Paganga G. (1997) Antioxidant properties of phenolic compounds. Trends in Plant Science, 2(4), 152–159. https://doi.org/10.1016/S1360-1385(97)01018-2
  28. Sadak MS, & Ramadan AAEM. (2021). Impact of melatonin and tryptophan on water stress tolerance in white lupine (Lupinus termis L.). Physiology and Molecular Biology of Plants, 27, 469–481. https://doi.org/10.1007/s12298-021-00958-8
  29. Sadras VO, & Rodriguez D. (2010). Modelling the nitrogen-driven trade-off between nitrogen utilisation efficiency and water use efficiency of wheat in eastern Australia. Field Crops Research, 118(3), 297–305. https://doi.org/10.1016/j.fcr.2010.06.010
  30. Serôdio J, Schmidt W, & Frankenbach S. (2017). A chlorophyll fluorescence‐based method for the integrated characterization of the photophysiological response to light stress. Journal of Experimental Botany, 68(5), 1123–1135. https://doi.org/10.1093/jxb/erw492
  31. Song Y, Li J, Liu M, Meng Z, Liu K, & Sui N. (2019a). Nitrogen increases drought tolerance in maize seedlings. Functional Plant Biology, 46(4), 350–359. https://doi.org/10.1071/FP18186
  32. Song X, Zhou G, Ma B, Wu W, Ahmad I, Zhu G, Yan W, & Jiao X. (2019b). Nitrogen Application Improved Photosynthetic Productivity, Chlorophyll Fluorescence, Yield and Yield Components of Two Oat Genotypes under Saline Conditions. Agronomy, 9(3), 115. https://doi.org/10.3390/AGRONOMY9030115
  33. Sumner L, Amberg A, Barrett D, Beale M, Beger R, Daykin C, Fan T, Fiehn O, Goodacre R, Griffin J, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane A, Lindon J, Marriott P, Nicholls A, Reily M, Thaden J, & Viant M. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics, 3, 211–221. https://doi.org/10.1007/s11306-007-0082-2
  34. Sun JY, Gao JL, & Lu XH. (2007). The effects of nitrogen on physiological indexes of drought tolerance and water use efficiency in soybean. Soybean Science. 26(4), 517–522.
  35. Tariq A, Pan K, Olatunji OA, Graciano C, Li N, Li Z, Song D, Sun F, Justine MF, Huang D, Gong S, Pandey B, Idrees M, & Dakhill MA. (2019). Role of nitrogen supplementation in alleviating drought-associated growth and metabolic impairments in Phoebe zhennan seedlings. Journal of Plant Nutrition and Soil Science, 182(4), 586–596. https://doi.org/10.1002/jpln.201800435
  36. The S, Snyder R, & Tegeder M. (2021). Targeting Nitrogen Metabolism and Transport Processes to Improve Plant Nitrogen Use Efficiency. Frontiers in Plant Science, 11. https://doi.org/10.3389/fpls.2020.628366
  37. Watanabe M, Balazadeh S, Toghe T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie A, & Hoefgen R. (2013). Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiology, 162(3), 1290–1310. https://doi.org/10.1104/pp.113.217380
  38. Wu Y, Li Q, Jin R, Chen W, Liu X, Kong F, Ke Y, Shi H, & Yuan J. (2019). Effect of low-nitrogen stress on photosynthesis and chlorophyll fluorescence characteristics of maize cultivars with different low-nitrogen tolerances. Journal of Integrative Agriculture, 18(6), 1246–1256. https://doi.org/10.1016/S2095-3119(18)62030-1
  39. Wu Y, Zhao B, Li Q, Kong F, Du L, Zhou F, Shi H, Ke Y, Liu Q, Feng D, & Yuan J. (2019). Non-structural carbohydrates in maize with different nitrogen tolerance are affected by nitrogen addition. PLoS ONE, 14, e0225753. https://doi.org/10.1371/journal.pone.0225753
  40. Zhao H, Sun S, Zhang L, Yang J, Wang Z, Ma F, & Li M. (2020). Carbohydrate metabolism and transport in apple roots under nitrogen deficiency. Plant Physiology and Biochemistry, 155, 455–463. https://doi.org/10.1016/j.plaphy.2020.07.037
  41. Zubillaga MF, Camina R, Orioli GA, & Barrio DA. (2019). Response of Amaranthus cruentus cv Mexicano to nitrogen fertilization under irrigation in the temperate, semiarid climate of North Patagonia, Argentina. Journal of Plant Nutrition, 42(2), 99–110. https://doi.org/10.1080/01904167.2018.1549674