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Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum

BACKGROUND: Dendrobium catenatum/D. officinale (here after D. catenatum), a well-known economically important traditional medicinal herb, produces a variety of bioactive metabolites including polysaccharides, alkaloids, and flavonoids with excellent pharmacological and clinical values. Although many...

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Autores principales: Wang, Zhicai, Zhao, Meili, Zhang, Xiaojie, Deng, Xuming, Li, Jian, Wang, Meina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9400273/
https://www.ncbi.nlm.nih.gov/pubmed/35999493
http://dx.doi.org/10.1186/s12864-022-08840-x
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author Wang, Zhicai
Zhao, Meili
Zhang, Xiaojie
Deng, Xuming
Li, Jian
Wang, Meina
author_facet Wang, Zhicai
Zhao, Meili
Zhang, Xiaojie
Deng, Xuming
Li, Jian
Wang, Meina
author_sort Wang, Zhicai
collection PubMed
description BACKGROUND: Dendrobium catenatum/D. officinale (here after D. catenatum), a well-known economically important traditional medicinal herb, produces a variety of bioactive metabolites including polysaccharides, alkaloids, and flavonoids with excellent pharmacological and clinical values. Although many genes associated with the biosynthesis of medicinal components have been cloned and characterized, the biosynthetic pathway, especially the downstream and regulatory pathway of major medicinal components in the herb, is far from clear. β-glucosidases (BGLUs) comprise a diverse group of enzymes that widely exist in plants and play essential functions in cell wall modification, defense response, phytohormone signaling, secondary metabolism, herbivore resistance, and scent release by hydrolyzing β-D-glycosidic bond from a carbohydrate moiety. The recent release of the chromosome-level reference genome of D. catenatum enables the characterization of gene families. Although the genome-wide analysis of the BGLU gene family has been successfully conducted in various plants, no systematic analysis is available for the D. catenatum. We previously isolated DcBGLU2 in the BGLU family as a key regulator for polysaccharide biosynthesis in D. catenatum. Yet, the exact number of DcBGLUs in the D. catenatum genome and their possible roles in bioactive compound production deserve more attention. RESULTS: To investigate the role of BGLUs in active metabolites production, 22 BGLUs (DcBGLU1-22) of the glycoside hydrolase family 1 (GH1) were identified from D. catenatum genome. Protein prediction showed that most of the DcBGLUs were acidic and phylogenetic analysis classified the family into four distinct clusters. The sequence alignments revealed several conserved motifs among the DcBGLU proteins and analyses of the putative signal peptides and N-glycosylation site revealed that the majority of DcBGLU members dually targeted to the vacuole and/or chloroplast. Organ-specific expression profiles and specific responses to MeJA and MF23 were also determined. Furthermore, four DcBGLUs were selected to test their involvement in metabolism regulation. Overexpression of DcBGLU2, 6, 8, and 13 significantly increased contents of flavonoid, reducing-polysaccharide, alkaloid and soluble-polysaccharide, respectively. CONCLUSION: The genome-wide systematic analysis identified candidate DcBGLU genes with possible roles in medicinal metabolites production and laid a theoretical foundation for further functional characterization and molecular breeding of D. catenatum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08840-x.
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spelling pubmed-94002732022-08-25 Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum Wang, Zhicai Zhao, Meili Zhang, Xiaojie Deng, Xuming Li, Jian Wang, Meina BMC Genomics Research BACKGROUND: Dendrobium catenatum/D. officinale (here after D. catenatum), a well-known economically important traditional medicinal herb, produces a variety of bioactive metabolites including polysaccharides, alkaloids, and flavonoids with excellent pharmacological and clinical values. Although many genes associated with the biosynthesis of medicinal components have been cloned and characterized, the biosynthetic pathway, especially the downstream and regulatory pathway of major medicinal components in the herb, is far from clear. β-glucosidases (BGLUs) comprise a diverse group of enzymes that widely exist in plants and play essential functions in cell wall modification, defense response, phytohormone signaling, secondary metabolism, herbivore resistance, and scent release by hydrolyzing β-D-glycosidic bond from a carbohydrate moiety. The recent release of the chromosome-level reference genome of D. catenatum enables the characterization of gene families. Although the genome-wide analysis of the BGLU gene family has been successfully conducted in various plants, no systematic analysis is available for the D. catenatum. We previously isolated DcBGLU2 in the BGLU family as a key regulator for polysaccharide biosynthesis in D. catenatum. Yet, the exact number of DcBGLUs in the D. catenatum genome and their possible roles in bioactive compound production deserve more attention. RESULTS: To investigate the role of BGLUs in active metabolites production, 22 BGLUs (DcBGLU1-22) of the glycoside hydrolase family 1 (GH1) were identified from D. catenatum genome. Protein prediction showed that most of the DcBGLUs were acidic and phylogenetic analysis classified the family into four distinct clusters. The sequence alignments revealed several conserved motifs among the DcBGLU proteins and analyses of the putative signal peptides and N-glycosylation site revealed that the majority of DcBGLU members dually targeted to the vacuole and/or chloroplast. Organ-specific expression profiles and specific responses to MeJA and MF23 were also determined. Furthermore, four DcBGLUs were selected to test their involvement in metabolism regulation. Overexpression of DcBGLU2, 6, 8, and 13 significantly increased contents of flavonoid, reducing-polysaccharide, alkaloid and soluble-polysaccharide, respectively. CONCLUSION: The genome-wide systematic analysis identified candidate DcBGLU genes with possible roles in medicinal metabolites production and laid a theoretical foundation for further functional characterization and molecular breeding of D. catenatum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08840-x. BioMed Central 2022-08-23 /pmc/articles/PMC9400273/ /pubmed/35999493 http://dx.doi.org/10.1186/s12864-022-08840-x 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
Wang, Zhicai
Zhao, Meili
Zhang, Xiaojie
Deng, Xuming
Li, Jian
Wang, Meina
Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title_full Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title_fullStr Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title_full_unstemmed Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title_short Genome-wide identification and characterization of active ingredients related β-Glucosidases in Dendrobium catenatum
title_sort genome-wide identification and characterization of active ingredients related β-glucosidases in dendrobium catenatum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9400273/
https://www.ncbi.nlm.nih.gov/pubmed/35999493
http://dx.doi.org/10.1186/s12864-022-08840-x
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