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Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants

Continuous light (CL) or a predominant nitrogen supply as ammonium (NH(4)(+)) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH(4)(+) suggests involvement of overlapping mechanisms in plant responses to these conditions; however, these mechanisms are...

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Autores principales: Paponov, Martina, Arakelyan, Aleksandr, Dobrev, Petre I., Verheul, Michel J., Paponov, Ivan A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8003008/
https://www.ncbi.nlm.nih.gov/pubmed/33803638
http://dx.doi.org/10.3390/plants10030573
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author Paponov, Martina
Arakelyan, Aleksandr
Dobrev, Petre I.
Verheul, Michel J.
Paponov, Ivan A.
author_facet Paponov, Martina
Arakelyan, Aleksandr
Dobrev, Petre I.
Verheul, Michel J.
Paponov, Ivan A.
author_sort Paponov, Martina
collection PubMed
description Continuous light (CL) or a predominant nitrogen supply as ammonium (NH(4)(+)) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH(4)(+) suggests involvement of overlapping mechanisms in plant responses to these conditions; however, these mechanisms are poorly understood. We addressed this topic by conducting full factorial experiments with tomato plants to investigate the effects of NO(3)(−) or NH(4)(+) supply under diurnal light (DL) or CL. We used plants at ages of 26 and 15 days after sowing to initiate the treatments, and we modulated the intensity of the stress induced by CL and an exclusive NH(4)(+) supply from mild to strong. Under DL, we also studied the effect of nitrogen (N) deficiency and mixed application of NO(3)(−) and NH(4)(+). Under strong stress, CL and exclusive NH(4)(+) supply synergistically inhibited plant growth and reduced chlorophyll content. Under mild stress, when no synergetic effect between CL and NH(4)(+) was apparent on plant growth and chlorophyll content, we found a synergetic effect of CL and NH(4)(+) on the accumulation of several plant stress hormones, with an especially strong effect for jasmonic acid (JA) and 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, in xylem sap. This modulation of the hormonal composition suggests a potential role for these plant hormones in plant growth responses to the combined application of CL and NH(4)(+). No synergetic effect was observed between CL and NH(4)(+) for the accumulation of soluble carbohydrates or of mineral ions, indicating that these plant traits are less sensitive than the modulation of hormonal composition in xylem sap to the combined CL and NH(4)(+) application. Under diurnal light, NH(4)(+) did not affect the hormonal composition of xylem sap; however, N deficiency strongly increased the concentrations of phaseic acid (PA), JA, and salicylic acid (SA), indicating that decreased N concentration rather than the presence of NO(3)(−) or NH(4)(+) in the nutrient solution drives the hormone composition of the xylem sap. In conclusion, N deficiency or a combined application of CL and NH(4)(+) induced the accumulation of JA in xylem sap. This accumulation, in combination with other plant hormones, defines the specific plant response to stress conditions.
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spelling pubmed-80030082021-03-28 Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants Paponov, Martina Arakelyan, Aleksandr Dobrev, Petre I. Verheul, Michel J. Paponov, Ivan A. Plants (Basel) Article Continuous light (CL) or a predominant nitrogen supply as ammonium (NH(4)(+)) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH(4)(+) suggests involvement of overlapping mechanisms in plant responses to these conditions; however, these mechanisms are poorly understood. We addressed this topic by conducting full factorial experiments with tomato plants to investigate the effects of NO(3)(−) or NH(4)(+) supply under diurnal light (DL) or CL. We used plants at ages of 26 and 15 days after sowing to initiate the treatments, and we modulated the intensity of the stress induced by CL and an exclusive NH(4)(+) supply from mild to strong. Under DL, we also studied the effect of nitrogen (N) deficiency and mixed application of NO(3)(−) and NH(4)(+). Under strong stress, CL and exclusive NH(4)(+) supply synergistically inhibited plant growth and reduced chlorophyll content. Under mild stress, when no synergetic effect between CL and NH(4)(+) was apparent on plant growth and chlorophyll content, we found a synergetic effect of CL and NH(4)(+) on the accumulation of several plant stress hormones, with an especially strong effect for jasmonic acid (JA) and 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, in xylem sap. This modulation of the hormonal composition suggests a potential role for these plant hormones in plant growth responses to the combined application of CL and NH(4)(+). No synergetic effect was observed between CL and NH(4)(+) for the accumulation of soluble carbohydrates or of mineral ions, indicating that these plant traits are less sensitive than the modulation of hormonal composition in xylem sap to the combined CL and NH(4)(+) application. Under diurnal light, NH(4)(+) did not affect the hormonal composition of xylem sap; however, N deficiency strongly increased the concentrations of phaseic acid (PA), JA, and salicylic acid (SA), indicating that decreased N concentration rather than the presence of NO(3)(−) or NH(4)(+) in the nutrient solution drives the hormone composition of the xylem sap. In conclusion, N deficiency or a combined application of CL and NH(4)(+) induced the accumulation of JA in xylem sap. This accumulation, in combination with other plant hormones, defines the specific plant response to stress conditions. MDPI 2021-03-18 /pmc/articles/PMC8003008/ /pubmed/33803638 http://dx.doi.org/10.3390/plants10030573 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ).
spellingShingle Article
Paponov, Martina
Arakelyan, Aleksandr
Dobrev, Petre I.
Verheul, Michel J.
Paponov, Ivan A.
Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title_full Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title_fullStr Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title_full_unstemmed Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title_short Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato Plants
title_sort nitrogen deficiency and synergism between continuous light and root ammonium supply modulate distinct but overlapping patterns of phytohormone composition in xylem sap of tomato plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8003008/
https://www.ncbi.nlm.nih.gov/pubmed/33803638
http://dx.doi.org/10.3390/plants10030573
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