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<sub>4</sub><sup>+</sup>) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH<sub>4</sub><sup>+</sup> suggests involvement of overlappi...

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Main Authors: Martina Paponov, Aleksandr Arakelyan, Petre I. Dobrev, Michel J. Verheul, Ivan A. Paponov
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/10/3/573
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author Martina Paponov
Aleksandr Arakelyan
Petre I. Dobrev
Michel J. Verheul
Ivan A. Paponov
author_facet Martina Paponov
Aleksandr Arakelyan
Petre I. Dobrev
Michel J. Verheul
Ivan A. Paponov
author_sort Martina Paponov
collection DOAJ
description Continuous light (CL) or a predominant nitrogen supply as ammonium (NH<sub>4</sub><sup>+</sup>) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH<sub>4</sub><sup>+</sup> 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<sub>3</sub><sup>−</sup> or NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup> supply from mild to strong. Under DL, we also studied the effect of nitrogen (N) deficiency and mixed application of NO<sub>3</sub><sup>−</sup> and NH<sub>4</sub><sup>+</sup>. Under strong stress, CL and exclusive NH<sub>4</sub><sup>+</sup> supply synergistically inhibited plant growth and reduced chlorophyll content. Under mild stress, when no synergetic effect between CL and NH<sub>4</sub><sup>+</sup> was apparent on plant growth and chlorophyll content, we found a synergetic effect of CL and NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup>. No synergetic effect was observed between CL and NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup> application. Under diurnal light, NH<sub>4</sub><sup>+</sup> 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<sub>3</sub><sup>−</sup> or NH<sub>4</sub><sup>+</sup> in the nutrient solution drives the hormone composition of the xylem sap. In conclusion, N deficiency or a combined application of CL and NH<sub>4</sub><sup>+</sup> 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 doaj.art-64aebb42601a4b1f9f719628bf6da6332023-11-21T10:59:47ZengMDPI AGPlants2223-77472021-03-0110357310.3390/plants10030573Nitrogen Deficiency and Synergism between Continuous Light and Root Ammonium Supply Modulate Distinct but Overlapping Patterns of Phytohormone Composition in Xylem Sap of Tomato PlantsMartina Paponov0Aleksandr Arakelyan1Petre I. Dobrev2Michel J. Verheul3Ivan A. Paponov4NIBIO, Norwegian Institute of Bioeconomy Research (NIBIO), Division of Food Production and Society, P.O. Box 115, NO 1431 Ås, NorwayDepartment of Agronomy, Armenian National Agrarian University, Yerevan 0009, ArmeniaInstitute of Experimental Botany, Czech Academy of Sciences, Rozvojova 263, 16502 Prague, Czech RepublicNIBIO, Norwegian Institute of Bioeconomy Research (NIBIO), Division of Food Production and Society, P.O. Box 115, NO 1431 Ås, NorwayNIBIO, Norwegian Institute of Bioeconomy Research (NIBIO), Division of Food Production and Society, P.O. Box 115, NO 1431 Ås, NorwayContinuous light (CL) or a predominant nitrogen supply as ammonium (NH<sub>4</sub><sup>+</sup>) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH<sub>4</sub><sup>+</sup> 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<sub>3</sub><sup>−</sup> or NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup> supply from mild to strong. Under DL, we also studied the effect of nitrogen (N) deficiency and mixed application of NO<sub>3</sub><sup>−</sup> and NH<sub>4</sub><sup>+</sup>. Under strong stress, CL and exclusive NH<sub>4</sub><sup>+</sup> supply synergistically inhibited plant growth and reduced chlorophyll content. Under mild stress, when no synergetic effect between CL and NH<sub>4</sub><sup>+</sup> was apparent on plant growth and chlorophyll content, we found a synergetic effect of CL and NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup>. No synergetic effect was observed between CL and NH<sub>4</sub><sup>+</sup> 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<sub>4</sub><sup>+</sup> application. Under diurnal light, NH<sub>4</sub><sup>+</sup> 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<sub>3</sub><sup>−</sup> or NH<sub>4</sub><sup>+</sup> in the nutrient solution drives the hormone composition of the xylem sap. In conclusion, N deficiency or a combined application of CL and NH<sub>4</sub><sup>+</sup> induced the accumulation of JA in xylem sap. This accumulation, in combination with other plant hormones, defines the specific plant response to stress conditions.https://www.mdpi.com/2223-7747/10/3/573tomatonitrogennitrateammoniumphytohormonesabscisic acid
spellingShingle Martina Paponov
Aleksandr Arakelyan
Petre I. Dobrev
Michel J. Verheul
Ivan A. Paponov
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
Plants
tomato
nitrogen
nitrate
ammonium
phytohormones
abscisic acid
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 tomato
nitrogen
nitrate
ammonium
phytohormones
abscisic acid
url https://www.mdpi.com/2223-7747/10/3/573
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