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Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice

BACKGROUND: Overuse of nitrogen fertilizers is often a major practice to ensure sufficient nitrogen demand of high–yielding rice, leading to persistent NH(4)(+) excess in the plant. However, this excessive portion of nitrogen nutrient does not correspond to further increase in grain yields. For find...

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Autores principales: Yang, Shunying, Hao, Dongli, Jin, Man, Li, Yi, Liu, Zengtai, Huang, Yanan, Chen, Tianxiang, Su, Yanhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7140567/
https://www.ncbi.nlm.nih.gov/pubmed/32264840
http://dx.doi.org/10.1186/s12870-020-02363-x
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author Yang, Shunying
Hao, Dongli
Jin, Man
Li, Yi
Liu, Zengtai
Huang, Yanan
Chen, Tianxiang
Su, Yanhua
author_facet Yang, Shunying
Hao, Dongli
Jin, Man
Li, Yi
Liu, Zengtai
Huang, Yanan
Chen, Tianxiang
Su, Yanhua
author_sort Yang, Shunying
collection PubMed
description BACKGROUND: Overuse of nitrogen fertilizers is often a major practice to ensure sufficient nitrogen demand of high–yielding rice, leading to persistent NH(4)(+) excess in the plant. However, this excessive portion of nitrogen nutrient does not correspond to further increase in grain yields. For finding out the main constraints related to this phenomenon, the performance of NH(4)(+) excess in rice plant needs to be clearly addressed beyond the well-defined root growth adjustment. The present work isolates an acute NH(4)(+) excess condition in rice plant from causing any measurable growth change and analyses the initial performance of such internal NH(4)(+) excess. RESULTS: We demonstrate that the acute internal NH(4)(+) excess in rice plant accompanies readily with a burst of reactive oxygen species (ROS) and initiates the downstream reactions. At the headstream of carbon production, photon caption genes and the activity of primary CO(2) fixation enzymes (Rubisco) are evidently suppressed, indicating a reduction in photosynthetic carbon income. Next, the vigorous induction of glutathione transferase (GST) genes and enzyme activities along with the rise of glutathione (GSH) production suggest the activation of GSH cycling for ROS cleavage. Third, as indicated by strong induction of glycolysis / glycogen breakdown related genes in shoots, carbohydrate metabolisms are redirected to enhance the production of energy and carbon skeletons for the cost of ROS scavenging. As the result of the development of these defensive reactions, a carbon scarcity would accumulatively occur and lead to a growth inhibition. Finally, a sucrose feeding cancels the ROS burst, restores the activity of Rubisco and alleviates the demand for the activation of GSH cycling. CONCLUSION: Our results demonstrate that acute NH(4)(+) excess accompanies with a spontaneous ROS burst and causes carbon scarcity in rice plant. Therefore, under overuse of N fertilizers carbon scarcity is probably a major constraint in rice plant that limits the performance of nitrogen.
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spelling pubmed-71405672020-04-14 Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice Yang, Shunying Hao, Dongli Jin, Man Li, Yi Liu, Zengtai Huang, Yanan Chen, Tianxiang Su, Yanhua BMC Plant Biol Research Article BACKGROUND: Overuse of nitrogen fertilizers is often a major practice to ensure sufficient nitrogen demand of high–yielding rice, leading to persistent NH(4)(+) excess in the plant. However, this excessive portion of nitrogen nutrient does not correspond to further increase in grain yields. For finding out the main constraints related to this phenomenon, the performance of NH(4)(+) excess in rice plant needs to be clearly addressed beyond the well-defined root growth adjustment. The present work isolates an acute NH(4)(+) excess condition in rice plant from causing any measurable growth change and analyses the initial performance of such internal NH(4)(+) excess. RESULTS: We demonstrate that the acute internal NH(4)(+) excess in rice plant accompanies readily with a burst of reactive oxygen species (ROS) and initiates the downstream reactions. At the headstream of carbon production, photon caption genes and the activity of primary CO(2) fixation enzymes (Rubisco) are evidently suppressed, indicating a reduction in photosynthetic carbon income. Next, the vigorous induction of glutathione transferase (GST) genes and enzyme activities along with the rise of glutathione (GSH) production suggest the activation of GSH cycling for ROS cleavage. Third, as indicated by strong induction of glycolysis / glycogen breakdown related genes in shoots, carbohydrate metabolisms are redirected to enhance the production of energy and carbon skeletons for the cost of ROS scavenging. As the result of the development of these defensive reactions, a carbon scarcity would accumulatively occur and lead to a growth inhibition. Finally, a sucrose feeding cancels the ROS burst, restores the activity of Rubisco and alleviates the demand for the activation of GSH cycling. CONCLUSION: Our results demonstrate that acute NH(4)(+) excess accompanies with a spontaneous ROS burst and causes carbon scarcity in rice plant. Therefore, under overuse of N fertilizers carbon scarcity is probably a major constraint in rice plant that limits the performance of nitrogen. BioMed Central 2020-04-07 /pmc/articles/PMC7140567/ /pubmed/32264840 http://dx.doi.org/10.1186/s12870-020-02363-x Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yang, Shunying
Hao, Dongli
Jin, Man
Li, Yi
Liu, Zengtai
Huang, Yanan
Chen, Tianxiang
Su, Yanhua
Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title_full Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title_fullStr Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title_full_unstemmed Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title_short Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice
title_sort internal ammonium excess induces ros-mediated reactions and causes carbon scarcity in rice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7140567/
https://www.ncbi.nlm.nih.gov/pubmed/32264840
http://dx.doi.org/10.1186/s12870-020-02363-x
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