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Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco

Nutritional correlations between plants and pathogens can crucially affect disease severity. As an essential macronutrient, the availability of nitrogen (N) and the types of N content play a fundamental part not only in energy metabolism and protein synthesis but also in pathogenesis. However, a dir...

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Autores principales: Yang, Zhixiao, Chen, Yi, Wang, Yi, Xia, Haiqian, Zheng, Shaoqing, Xie, Shengdong, Cao, Yi, Liu, Jiemin, Sehar, Shafaque, Lin, Yingchao, Guo, Yushuang, Shamsi, Imran Haider
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9538177/
https://www.ncbi.nlm.nih.gov/pubmed/36212279
http://dx.doi.org/10.3389/fpls.2022.1003534
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author Yang, Zhixiao
Chen, Yi
Wang, Yi
Xia, Haiqian
Zheng, Shaoqing
Xie, Shengdong
Cao, Yi
Liu, Jiemin
Sehar, Shafaque
Lin, Yingchao
Guo, Yushuang
Shamsi, Imran Haider
author_facet Yang, Zhixiao
Chen, Yi
Wang, Yi
Xia, Haiqian
Zheng, Shaoqing
Xie, Shengdong
Cao, Yi
Liu, Jiemin
Sehar, Shafaque
Lin, Yingchao
Guo, Yushuang
Shamsi, Imran Haider
author_sort Yang, Zhixiao
collection PubMed
description Nutritional correlations between plants and pathogens can crucially affect disease severity. As an essential macronutrient, the availability of nitrogen (N) and the types of N content play a fundamental part not only in energy metabolism and protein synthesis but also in pathogenesis. However, a direct connection has not yet been established between differences in the level of resistance and N metabolism. Pertinently, former studies hold ammonia (NH(3)) accountable for the development of diseases in tobacco (Nicotiana tabacum L.) and in some post-harvest fruits. With a purpose of pinpointing the function of NH(3) volatilization on Alternaria alternata (Fries) Keissl pathogenesis and its correlation with both N metabolism and resistance differences to Alternaria alternata infection in tobacco, leaf tissue of two tobacco cultivars with susceptibility (Changbohuang; CBH), or resistance (Jingyehuang; JYH) were analyzed apropos of ammonia compensation point, apoplastic NH(4)(+) concentration, pH value as well as activities of key enzymes and N status. At the leaf age of 40 to 60 d, the susceptible cultivar had a significantly higher foliar apoplastic ammonium (NH(4)(+)) concentration, pH value and NH(3) volatilization potential compared to the resistant one accompanied by a significant reduction in glutamine synthetase (GS), which in particular was a primary factor causing the NH(3) volatilization. The NH(4)(+) concentration in CBH was 1.44 times higher than that in JYH, and CBH had NH(3) compensation points that were 7.09, 6.15 and 4.35-fold higher than those of JYH at 40, 50 and 60 d, respectively. Moreover, the glutamate dehydrogenase (GDH) activity had an upward tendency related to an increased NH(4)(+) accumulation in both leaf tissues and apoplast but not with the NH(3) compensation point. Collectively, our results strongly suggest that the accumulation of NH(3) volatilization, rather than NH(4)(+) and total N, was the primary factor inducing the Alternaria alternata infection in tobacco. Meanwhile, the susceptible cultivar was characterized by a higher N re-transfer ability of NH(3) volatilization, in contrast to the disease–resistant cultivar, and had a stronger capability of N assimilation and reutilization. This study provides a deeper understanding of the pathogenicity mechanism induced by Alternaria alternata, which is useful for breeding Alternaria alternata-resistant varieties of tobacco, at the same time, our research is also conducive to control tobacco brown spot caused by Alternaria alternata in the field.
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spelling pubmed-95381772022-10-08 Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco Yang, Zhixiao Chen, Yi Wang, Yi Xia, Haiqian Zheng, Shaoqing Xie, Shengdong Cao, Yi Liu, Jiemin Sehar, Shafaque Lin, Yingchao Guo, Yushuang Shamsi, Imran Haider Front Plant Sci Plant Science Nutritional correlations between plants and pathogens can crucially affect disease severity. As an essential macronutrient, the availability of nitrogen (N) and the types of N content play a fundamental part not only in energy metabolism and protein synthesis but also in pathogenesis. However, a direct connection has not yet been established between differences in the level of resistance and N metabolism. Pertinently, former studies hold ammonia (NH(3)) accountable for the development of diseases in tobacco (Nicotiana tabacum L.) and in some post-harvest fruits. With a purpose of pinpointing the function of NH(3) volatilization on Alternaria alternata (Fries) Keissl pathogenesis and its correlation with both N metabolism and resistance differences to Alternaria alternata infection in tobacco, leaf tissue of two tobacco cultivars with susceptibility (Changbohuang; CBH), or resistance (Jingyehuang; JYH) were analyzed apropos of ammonia compensation point, apoplastic NH(4)(+) concentration, pH value as well as activities of key enzymes and N status. At the leaf age of 40 to 60 d, the susceptible cultivar had a significantly higher foliar apoplastic ammonium (NH(4)(+)) concentration, pH value and NH(3) volatilization potential compared to the resistant one accompanied by a significant reduction in glutamine synthetase (GS), which in particular was a primary factor causing the NH(3) volatilization. The NH(4)(+) concentration in CBH was 1.44 times higher than that in JYH, and CBH had NH(3) compensation points that were 7.09, 6.15 and 4.35-fold higher than those of JYH at 40, 50 and 60 d, respectively. Moreover, the glutamate dehydrogenase (GDH) activity had an upward tendency related to an increased NH(4)(+) accumulation in both leaf tissues and apoplast but not with the NH(3) compensation point. Collectively, our results strongly suggest that the accumulation of NH(3) volatilization, rather than NH(4)(+) and total N, was the primary factor inducing the Alternaria alternata infection in tobacco. Meanwhile, the susceptible cultivar was characterized by a higher N re-transfer ability of NH(3) volatilization, in contrast to the disease–resistant cultivar, and had a stronger capability of N assimilation and reutilization. This study provides a deeper understanding of the pathogenicity mechanism induced by Alternaria alternata, which is useful for breeding Alternaria alternata-resistant varieties of tobacco, at the same time, our research is also conducive to control tobacco brown spot caused by Alternaria alternata in the field. Frontiers Media S.A. 2022-09-23 /pmc/articles/PMC9538177/ /pubmed/36212279 http://dx.doi.org/10.3389/fpls.2022.1003534 Text en Copyright © 2022 Yang, Chen, Wang, Xia, Zheng, Xie, Cao, Liu, Sehar, Lin, Guo and Shamsi. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Yang, Zhixiao
Chen, Yi
Wang, Yi
Xia, Haiqian
Zheng, Shaoqing
Xie, Shengdong
Cao, Yi
Liu, Jiemin
Sehar, Shafaque
Lin, Yingchao
Guo, Yushuang
Shamsi, Imran Haider
Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title_full Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title_fullStr Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title_full_unstemmed Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title_short Nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus Alternaria alternata in tobacco
title_sort nitrogen metabolic rate and differential ammonia volatilization regulate resistance against opportunistic fungus alternaria alternata in tobacco
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9538177/
https://www.ncbi.nlm.nih.gov/pubmed/36212279
http://dx.doi.org/10.3389/fpls.2022.1003534
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