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Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation

BACKGROUND: Microspore embryogenesis is an extraordinarily complicated process, comprehensively regulated by a composite network of physiological and molecular factors, among which hormone is one of the most crucial factors. Auxin is required for stress-induced microspore reprogramming, however, the...

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Autores principales: Wang, Chenggang, Zhang, Peiyu, He, Yun, Huang, Furong, Wang, Xu, Li, Hong, Yuan, Lingyun, Hou, Jinfeng, Chen, Guohu, Wang, Wenjie, Wu, Jianqiang, Tang, Xiaoyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10327361/
https://www.ncbi.nlm.nih.gov/pubmed/37415142
http://dx.doi.org/10.1186/s12864-023-09483-2
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author Wang, Chenggang
Zhang, Peiyu
He, Yun
Huang, Furong
Wang, Xu
Li, Hong
Yuan, Lingyun
Hou, Jinfeng
Chen, Guohu
Wang, Wenjie
Wu, Jianqiang
Tang, Xiaoyan
author_facet Wang, Chenggang
Zhang, Peiyu
He, Yun
Huang, Furong
Wang, Xu
Li, Hong
Yuan, Lingyun
Hou, Jinfeng
Chen, Guohu
Wang, Wenjie
Wu, Jianqiang
Tang, Xiaoyan
author_sort Wang, Chenggang
collection PubMed
description BACKGROUND: Microspore embryogenesis is an extraordinarily complicated process, comprehensively regulated by a composite network of physiological and molecular factors, among which hormone is one of the most crucial factors. Auxin is required for stress-induced microspore reprogramming, however, the mechanism of its regulation of microspore embryogenesis is still unclear. RESULTS: In this study, we found exogenously spraying 100 mg·L(− 1) IAA on the buds of Wucai significantly increased the rate of microspore embryogenesis, and moreover accelerated the process of embryogenesis. Physiological and biochemical tests showed that the contents of amino acids, soluble total sugar, soluble protein, and starch were significantly increased after IAA treatment. Furthermore, exogenously spraying 100 mg·L(− 1) IAA significantly enhanced IAA, GA(4), and GA(9) content, increased catalase (CAT) and malondialdehyde (MDA) activity, and reduced abscisic acid (ABA), MDA and soluble protopectin content, H(2)O(2) and O(2)·(−) production rate in the bud with the largest population of late-uninucleate-stage microspores. Transcriptome sequencing was performed on buds respectively treated with 100 mg·L(− 1) IAA and fresh water. A total of 2004 DEGs were identified, of which 79 were involved in micropores development, embryonic development and cell wall formation and modification, most of which were upregulated. KEGG and GO analysis revealed that 9.52% of DEGs were enriched in plant hormone synthesis and signal transduction pathways, pentose and glucuronic acid exchange pathways, and oxidative phosphorylation pathways. CONCLUSIONS: These findings indicated that exogenous IAA altered the contents of endogenous hormone content, total soluble sugar, amino acid, starch, soluble protein, MDA and protopectin, the activities of CAT and peroxidase (POD), and the production rate of H(2)O(2) and O(2)·(−). Combined with transcriptome analysis, it was found that most genes related to gibberellin (GA) and Auxin (IAA) synthesis and signal transduction, pectin methylase (PME) and polygalacturonase (PGs) genes and genes related to ATP synthesis and electron transport chain were upregulated, and genes related to ABA synthesis and signal transduction were downregulated. These results indicated that exogenous IAA treatment could change the balance of endogenous hormones, accelerate cell wall degradation, promote ATP synthesis and nutrient accumulation, inhibit ROS accumulation, which ultimately promote microspore embryogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09483-2.
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spelling pubmed-103273612023-07-08 Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation Wang, Chenggang Zhang, Peiyu He, Yun Huang, Furong Wang, Xu Li, Hong Yuan, Lingyun Hou, Jinfeng Chen, Guohu Wang, Wenjie Wu, Jianqiang Tang, Xiaoyan BMC Genomics Research BACKGROUND: Microspore embryogenesis is an extraordinarily complicated process, comprehensively regulated by a composite network of physiological and molecular factors, among which hormone is one of the most crucial factors. Auxin is required for stress-induced microspore reprogramming, however, the mechanism of its regulation of microspore embryogenesis is still unclear. RESULTS: In this study, we found exogenously spraying 100 mg·L(− 1) IAA on the buds of Wucai significantly increased the rate of microspore embryogenesis, and moreover accelerated the process of embryogenesis. Physiological and biochemical tests showed that the contents of amino acids, soluble total sugar, soluble protein, and starch were significantly increased after IAA treatment. Furthermore, exogenously spraying 100 mg·L(− 1) IAA significantly enhanced IAA, GA(4), and GA(9) content, increased catalase (CAT) and malondialdehyde (MDA) activity, and reduced abscisic acid (ABA), MDA and soluble protopectin content, H(2)O(2) and O(2)·(−) production rate in the bud with the largest population of late-uninucleate-stage microspores. Transcriptome sequencing was performed on buds respectively treated with 100 mg·L(− 1) IAA and fresh water. A total of 2004 DEGs were identified, of which 79 were involved in micropores development, embryonic development and cell wall formation and modification, most of which were upregulated. KEGG and GO analysis revealed that 9.52% of DEGs were enriched in plant hormone synthesis and signal transduction pathways, pentose and glucuronic acid exchange pathways, and oxidative phosphorylation pathways. CONCLUSIONS: These findings indicated that exogenous IAA altered the contents of endogenous hormone content, total soluble sugar, amino acid, starch, soluble protein, MDA and protopectin, the activities of CAT and peroxidase (POD), and the production rate of H(2)O(2) and O(2)·(−). Combined with transcriptome analysis, it was found that most genes related to gibberellin (GA) and Auxin (IAA) synthesis and signal transduction, pectin methylase (PME) and polygalacturonase (PGs) genes and genes related to ATP synthesis and electron transport chain were upregulated, and genes related to ABA synthesis and signal transduction were downregulated. These results indicated that exogenous IAA treatment could change the balance of endogenous hormones, accelerate cell wall degradation, promote ATP synthesis and nutrient accumulation, inhibit ROS accumulation, which ultimately promote microspore embryogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09483-2. BioMed Central 2023-07-06 /pmc/articles/PMC10327361/ /pubmed/37415142 http://dx.doi.org/10.1186/s12864-023-09483-2 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
Wang, Chenggang
Zhang, Peiyu
He, Yun
Huang, Furong
Wang, Xu
Li, Hong
Yuan, Lingyun
Hou, Jinfeng
Chen, Guohu
Wang, Wenjie
Wu, Jianqiang
Tang, Xiaoyan
Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title_full Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title_fullStr Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title_full_unstemmed Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title_short Exogenous spraying of IAA improved the efficiency of microspore embryogenesis in Wucai (Brassica campestris L.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
title_sort exogenous spraying of iaa improved the efficiency of microspore embryogenesis in wucai (brassica campestris l.) by affecting the balance of endogenous hormones, energy metabolism, and cell wall degradation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10327361/
https://www.ncbi.nlm.nih.gov/pubmed/37415142
http://dx.doi.org/10.1186/s12864-023-09483-2
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