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Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana

BACKGROUND: Plants are continuously exposed to changing environmental conditions and biotic attacks that affect plant growth. In crops, the inability to respond appropriately to stress has strong detrimental effects on agricultural production and yield. Ca(2+) signalling plays a fundamental role in...

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Autores principales: Giridhar, Maya, Meier, Bastian, Imani, Jafargholi, Kogel, Karl-Heinz, Peiter, Edgar, Vothknecht, Ute C., Chigri, Fatima
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9482192/
https://www.ncbi.nlm.nih.gov/pubmed/36114461
http://dx.doi.org/10.1186/s12870-022-03820-5
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author Giridhar, Maya
Meier, Bastian
Imani, Jafargholi
Kogel, Karl-Heinz
Peiter, Edgar
Vothknecht, Ute C.
Chigri, Fatima
author_facet Giridhar, Maya
Meier, Bastian
Imani, Jafargholi
Kogel, Karl-Heinz
Peiter, Edgar
Vothknecht, Ute C.
Chigri, Fatima
author_sort Giridhar, Maya
collection PubMed
description BACKGROUND: Plants are continuously exposed to changing environmental conditions and biotic attacks that affect plant growth. In crops, the inability to respond appropriately to stress has strong detrimental effects on agricultural production and yield. Ca(2+) signalling plays a fundamental role in the response of plants to most abiotic and biotic stresses. However, research on stimulus-specific Ca(2+) signals has mostly been pursued in Arabidopsis thaliana, while in other species these events are little investigated . RESULTS: In this study, we introduced the Ca(2+) reporter-encoding gene APOAEQUORIN into the crop species barley (Hordeum vulgare). Measurements of the dynamic changes in [Ca(2+)](cyt) in response to various stimuli such as NaCl, mannitol, H(2)O(2), and flagellin 22 (flg22) revealed the occurrence of dose- as well as tissue-dependent [Ca(2+)](cyt) transients. Moreover, the Ca(2+) signatures were unique for each stimulus, suggesting the involvement of different Ca(2+) signalling components in the corresponding stress response. Alongside, the barley Ca(2+) signatures were compared to those produced by the phylogenetically distant model plant Arabidopsis. Notable differences in temporal kinetics and dose responses were observed, implying species-specific differences in stress response mechanisms. The plasma membrane Ca(2+) channel blocker La(3+) strongly inhibited the [Ca(2+)](cyt) response to all tested stimuli, indicating a critical role of extracellular Ca(2+) in the induction of stress-associated Ca(2+) signatures in barley. Moreover, by analysing spatio-temporal dynamics of the [Ca(2+)](cyt) transients along the developmental gradient of the barley leaf blade we demonstrate that different parts of the barley leaf show quantitative differences in [Ca(2+)](cyt) transients in response to NaCl and H(2)O(2). There were only marginal differences in the response to flg22, indicative of developmental stage-dependent Ca(2+) responses specifically to NaCl and H(2)O(2). CONCLUSION: This study reveals tissue-specific Ca(2+) signals with stimulus-specific kinetics in the crop species barley, as well as quantitative differences along the barley leaf blade. A number of notable differences to the model plants Arabidopsis may be linked to different stimulus sensitivity. These transgenic barley reporter lines thus present a valuable tool to further analyse mechanisms of Ca(2+) signalling in this crop and to gain insights into the variation of Ca(2+)-dependent stress responses between stress-susceptible and -resistant species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03820-5.
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spelling pubmed-94821922022-09-18 Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana Giridhar, Maya Meier, Bastian Imani, Jafargholi Kogel, Karl-Heinz Peiter, Edgar Vothknecht, Ute C. Chigri, Fatima BMC Plant Biol Research BACKGROUND: Plants are continuously exposed to changing environmental conditions and biotic attacks that affect plant growth. In crops, the inability to respond appropriately to stress has strong detrimental effects on agricultural production and yield. Ca(2+) signalling plays a fundamental role in the response of plants to most abiotic and biotic stresses. However, research on stimulus-specific Ca(2+) signals has mostly been pursued in Arabidopsis thaliana, while in other species these events are little investigated . RESULTS: In this study, we introduced the Ca(2+) reporter-encoding gene APOAEQUORIN into the crop species barley (Hordeum vulgare). Measurements of the dynamic changes in [Ca(2+)](cyt) in response to various stimuli such as NaCl, mannitol, H(2)O(2), and flagellin 22 (flg22) revealed the occurrence of dose- as well as tissue-dependent [Ca(2+)](cyt) transients. Moreover, the Ca(2+) signatures were unique for each stimulus, suggesting the involvement of different Ca(2+) signalling components in the corresponding stress response. Alongside, the barley Ca(2+) signatures were compared to those produced by the phylogenetically distant model plant Arabidopsis. Notable differences in temporal kinetics and dose responses were observed, implying species-specific differences in stress response mechanisms. The plasma membrane Ca(2+) channel blocker La(3+) strongly inhibited the [Ca(2+)](cyt) response to all tested stimuli, indicating a critical role of extracellular Ca(2+) in the induction of stress-associated Ca(2+) signatures in barley. Moreover, by analysing spatio-temporal dynamics of the [Ca(2+)](cyt) transients along the developmental gradient of the barley leaf blade we demonstrate that different parts of the barley leaf show quantitative differences in [Ca(2+)](cyt) transients in response to NaCl and H(2)O(2). There were only marginal differences in the response to flg22, indicative of developmental stage-dependent Ca(2+) responses specifically to NaCl and H(2)O(2). CONCLUSION: This study reveals tissue-specific Ca(2+) signals with stimulus-specific kinetics in the crop species barley, as well as quantitative differences along the barley leaf blade. A number of notable differences to the model plants Arabidopsis may be linked to different stimulus sensitivity. These transgenic barley reporter lines thus present a valuable tool to further analyse mechanisms of Ca(2+) signalling in this crop and to gain insights into the variation of Ca(2+)-dependent stress responses between stress-susceptible and -resistant species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03820-5. BioMed Central 2022-09-17 /pmc/articles/PMC9482192/ /pubmed/36114461 http://dx.doi.org/10.1186/s12870-022-03820-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Giridhar, Maya
Meier, Bastian
Imani, Jafargholi
Kogel, Karl-Heinz
Peiter, Edgar
Vothknecht, Ute C.
Chigri, Fatima
Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title_full Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title_fullStr Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title_full_unstemmed Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title_short Comparative analysis of stress-induced calcium signals in the crop species barley and the model plant Arabidopsis thaliana
title_sort comparative analysis of stress-induced calcium signals in the crop species barley and the model plant arabidopsis thaliana
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9482192/
https://www.ncbi.nlm.nih.gov/pubmed/36114461
http://dx.doi.org/10.1186/s12870-022-03820-5
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