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Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis

BACKGROUND: Suspension culture is widely used in the establishment of efficient plant regeneration systems, as well as in the mass production of plant secondary metabolites. However, the establishment of a suspension culture system of Cunninghamia lanceolata is genotype-dependent given that proembry...

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Autores principales: Hao, Zhaodong, Shi, Jinyu, Wu, Hua, Yan, Yiqing, Xing, Kaifei, Zheng, Renhua, Shi, Jisen, Chen, Jinhui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561472/
https://www.ncbi.nlm.nih.gov/pubmed/37814230
http://dx.doi.org/10.1186/s12870-023-04496-1
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author Hao, Zhaodong
Shi, Jinyu
Wu, Hua
Yan, Yiqing
Xing, Kaifei
Zheng, Renhua
Shi, Jisen
Chen, Jinhui
author_facet Hao, Zhaodong
Shi, Jinyu
Wu, Hua
Yan, Yiqing
Xing, Kaifei
Zheng, Renhua
Shi, Jisen
Chen, Jinhui
author_sort Hao, Zhaodong
collection PubMed
description BACKGROUND: Suspension culture is widely used in the establishment of efficient plant regeneration systems, as well as in the mass production of plant secondary metabolites. However, the establishment of a suspension culture system of Cunninghamia lanceolata is genotype-dependent given that proembryogenic masses (PEMs) are prone to browning during this process in recalcitrant genotypes. Previously, we reported that the plant peptide hormone phytosulfokine (PSK) can tremendously decrease the hydrogen peroxide (H(2)O(2)) level and help to initiate somatic embryogenesis (SE) in recalcitrant C. lanceolata genotypes. However, to date, no studies have revealed whether or how PSK may contribute to the establishment of a suspension culture system in these recalcitrant genotypes. RESULTS: Here, we demonstrated that exogenous application of PSK effectively inhibited PEM browning during suspension culture in a recalcitrant genotype of C. lanceolata. Comparative time-series transcriptome profiling showed that redox homeostasis underwent drastic fluctuations when PEMs were cultured in liquid medium, while additional PSK treatment helped to maintain a relatively stable redox homeostasis. Interestingly, PSK seemed to have a dual effect on peroxidases (PRXs), with PSK simultaneously transcriptionally repressing ROS-producing PRXs and activating ROS-scavenging PRXs. Furthermore, determination of H(2)O(2) and MDA content, as well as cell viability, showed that exogenous PSK treatment inhibited PEM browning and safeguarded PEM suspension culture by decreasing the H(2)O(2) level and increasing PEM activity. CONCLUSIONS: Collectively, these findings provide a valuable tool for the future establishment of large-scale C. lanceolata PEM suspension culture without genotype limitations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04496-1.
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spelling pubmed-105614722023-10-10 Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis Hao, Zhaodong Shi, Jinyu Wu, Hua Yan, Yiqing Xing, Kaifei Zheng, Renhua Shi, Jisen Chen, Jinhui BMC Plant Biol Research BACKGROUND: Suspension culture is widely used in the establishment of efficient plant regeneration systems, as well as in the mass production of plant secondary metabolites. However, the establishment of a suspension culture system of Cunninghamia lanceolata is genotype-dependent given that proembryogenic masses (PEMs) are prone to browning during this process in recalcitrant genotypes. Previously, we reported that the plant peptide hormone phytosulfokine (PSK) can tremendously decrease the hydrogen peroxide (H(2)O(2)) level and help to initiate somatic embryogenesis (SE) in recalcitrant C. lanceolata genotypes. However, to date, no studies have revealed whether or how PSK may contribute to the establishment of a suspension culture system in these recalcitrant genotypes. RESULTS: Here, we demonstrated that exogenous application of PSK effectively inhibited PEM browning during suspension culture in a recalcitrant genotype of C. lanceolata. Comparative time-series transcriptome profiling showed that redox homeostasis underwent drastic fluctuations when PEMs were cultured in liquid medium, while additional PSK treatment helped to maintain a relatively stable redox homeostasis. Interestingly, PSK seemed to have a dual effect on peroxidases (PRXs), with PSK simultaneously transcriptionally repressing ROS-producing PRXs and activating ROS-scavenging PRXs. Furthermore, determination of H(2)O(2) and MDA content, as well as cell viability, showed that exogenous PSK treatment inhibited PEM browning and safeguarded PEM suspension culture by decreasing the H(2)O(2) level and increasing PEM activity. CONCLUSIONS: Collectively, these findings provide a valuable tool for the future establishment of large-scale C. lanceolata PEM suspension culture without genotype limitations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04496-1. BioMed Central 2023-10-09 /pmc/articles/PMC10561472/ /pubmed/37814230 http://dx.doi.org/10.1186/s12870-023-04496-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Hao, Zhaodong
Shi, Jinyu
Wu, Hua
Yan, Yiqing
Xing, Kaifei
Zheng, Renhua
Shi, Jisen
Chen, Jinhui
Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title_full Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title_fullStr Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title_full_unstemmed Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title_short Phytosulfokine contributes to suspension culture of Cunninghamia lanceolata through its impact on redox homeostasis
title_sort phytosulfokine contributes to suspension culture of cunninghamia lanceolata through its impact on redox homeostasis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561472/
https://www.ncbi.nlm.nih.gov/pubmed/37814230
http://dx.doi.org/10.1186/s12870-023-04496-1
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