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Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature

BACKGROUND: Low-temperature severely affects the growth and development of chrysanthemum which is one kind of ornamental plant well-known and widely used in the world. Lysine crotonylation is a recently identified post-translational modification (PTM) with multiple cellular functions. However, lysin...

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Autores principales: Lin, Ping, Bai, Hui-ru, He, Ling, Huang, Qiu-xiang, Zeng, Qin-han, Pan, Yuan-zhi, Jiang, Bei-bei, Zhang, Fan, Zhang, Lei, Liu, Qing-Lin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7809856/
https://www.ncbi.nlm.nih.gov/pubmed/33446097
http://dx.doi.org/10.1186/s12864-020-07365-5
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author Lin, Ping
Bai, Hui-ru
He, Ling
Huang, Qiu-xiang
Zeng, Qin-han
Pan, Yuan-zhi
Jiang, Bei-bei
Zhang, Fan
Zhang, Lei
Liu, Qing-Lin
author_facet Lin, Ping
Bai, Hui-ru
He, Ling
Huang, Qiu-xiang
Zeng, Qin-han
Pan, Yuan-zhi
Jiang, Bei-bei
Zhang, Fan
Zhang, Lei
Liu, Qing-Lin
author_sort Lin, Ping
collection PubMed
description BACKGROUND: Low-temperature severely affects the growth and development of chrysanthemum which is one kind of ornamental plant well-known and widely used in the world. Lysine crotonylation is a recently identified post-translational modification (PTM) with multiple cellular functions. However, lysine crotonylation under low-temperature stress has not been studied. RESULTS: Proteome-wide and lysine crotonylation of chrysanthemum at low-temperature was analyzed using TMT (Tandem Mass Tag) labeling, sensitive immuno-precipitation, and high-resolution LC-MS/MS. The results showed that 2017 crotonylation sites were identified in 1199 proteins. Treatment at 4 °C for 24 h and − 4 °C for 4 h resulted in 393 upregulated proteins and 500 downregulated proteins (1.2-fold threshold and P < 0.05). Analysis of biological information showed that lysine crotonylation was involved in photosynthesis, ribosomes, and antioxidant systems. The crotonylated proteins and motifs in chrysanthemum were compared with other plants to obtain orthologous proteins and conserved motifs. To further understand how lysine crotonylation at K136 affected APX (ascorbate peroxidase), we performed a site-directed mutation at K136 in APX. Site-directed crotonylation showed that lysine decrotonylation at K136 reduced APX activity, and lysine complete crotonylation at K136 increased APX activity. CONCLUSION: In summary, our study comparatively analyzed proteome-wide and crotonylation in chrysanthemum under low-temperature stress and provided insights into the mechanisms of crotonylation in positively regulated APX activity to reduce the oxidative damage caused by low-temperature stress. These data provided an important basis for studying crotonylation to regulate antioxidant enzyme activity in response to low-temperature stress and a new research ideas for chilling-tolerance and freezing-tolerance chrysanthemum molecular breeding. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07365-5.
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spelling pubmed-78098562021-01-18 Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature Lin, Ping Bai, Hui-ru He, Ling Huang, Qiu-xiang Zeng, Qin-han Pan, Yuan-zhi Jiang, Bei-bei Zhang, Fan Zhang, Lei Liu, Qing-Lin BMC Genomics Research Article BACKGROUND: Low-temperature severely affects the growth and development of chrysanthemum which is one kind of ornamental plant well-known and widely used in the world. Lysine crotonylation is a recently identified post-translational modification (PTM) with multiple cellular functions. However, lysine crotonylation under low-temperature stress has not been studied. RESULTS: Proteome-wide and lysine crotonylation of chrysanthemum at low-temperature was analyzed using TMT (Tandem Mass Tag) labeling, sensitive immuno-precipitation, and high-resolution LC-MS/MS. The results showed that 2017 crotonylation sites were identified in 1199 proteins. Treatment at 4 °C for 24 h and − 4 °C for 4 h resulted in 393 upregulated proteins and 500 downregulated proteins (1.2-fold threshold and P < 0.05). Analysis of biological information showed that lysine crotonylation was involved in photosynthesis, ribosomes, and antioxidant systems. The crotonylated proteins and motifs in chrysanthemum were compared with other plants to obtain orthologous proteins and conserved motifs. To further understand how lysine crotonylation at K136 affected APX (ascorbate peroxidase), we performed a site-directed mutation at K136 in APX. Site-directed crotonylation showed that lysine decrotonylation at K136 reduced APX activity, and lysine complete crotonylation at K136 increased APX activity. CONCLUSION: In summary, our study comparatively analyzed proteome-wide and crotonylation in chrysanthemum under low-temperature stress and provided insights into the mechanisms of crotonylation in positively regulated APX activity to reduce the oxidative damage caused by low-temperature stress. These data provided an important basis for studying crotonylation to regulate antioxidant enzyme activity in response to low-temperature stress and a new research ideas for chilling-tolerance and freezing-tolerance chrysanthemum molecular breeding. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07365-5. BioMed Central 2021-01-14 /pmc/articles/PMC7809856/ /pubmed/33446097 http://dx.doi.org/10.1186/s12864-020-07365-5 Text en © The Author(s) 2021 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
Lin, Ping
Bai, Hui-ru
He, Ling
Huang, Qiu-xiang
Zeng, Qin-han
Pan, Yuan-zhi
Jiang, Bei-bei
Zhang, Fan
Zhang, Lei
Liu, Qing-Lin
Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title_full Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title_fullStr Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title_full_unstemmed Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title_short Proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (Dendranthema grandiforum) under low-temperature
title_sort proteome-wide and lysine crotonylation profiling reveals the importance of crotonylation in chrysanthemum (dendranthema grandiforum) under low-temperature
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7809856/
https://www.ncbi.nlm.nih.gov/pubmed/33446097
http://dx.doi.org/10.1186/s12864-020-07365-5
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