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Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua

MicroRNAs (miRNAs) play crucial roles in plant development and secondary metabolism through different modes of sequence‐specific interaction with their targets. Artemisinin biosynthesis is extensively regulated by phytohormones. However, the function of phytohormone‐responsive miRNAs in artemisinin...

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Autores principales: Guo, Zhiying, Hao, Kai, Lv, Zongyou, Yu, Luyao, Bu, Qitao, Ren, Junze, Zhang, Henan, Chen, Ruibing, Zhang, Lei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946145/
https://www.ncbi.nlm.nih.gov/pubmed/36478140
http://dx.doi.org/10.1111/pbi.13974
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author Guo, Zhiying
Hao, Kai
Lv, Zongyou
Yu, Luyao
Bu, Qitao
Ren, Junze
Zhang, Henan
Chen, Ruibing
Zhang, Lei
author_facet Guo, Zhiying
Hao, Kai
Lv, Zongyou
Yu, Luyao
Bu, Qitao
Ren, Junze
Zhang, Henan
Chen, Ruibing
Zhang, Lei
author_sort Guo, Zhiying
collection PubMed
description MicroRNAs (miRNAs) play crucial roles in plant development and secondary metabolism through different modes of sequence‐specific interaction with their targets. Artemisinin biosynthesis is extensively regulated by phytohormones. However, the function of phytohormone‐responsive miRNAs in artemisinin biosynthesis remains enigmatic. Thus, we combined the analysis of transcriptomics, small RNAs, and the degradome to generate a comprehensive resource for identifying key miRNA‐target circuits involved in the phytohormone‐induced process of artemisinin biosynthesis in Artemisia annua. In total, 151 conserved and 52 novel miRNAs and their 4132 targets were determined. Based on the differential expression analysis, miR160 was selected as a potential miRNA involved in artemisinin synthesis. Overexpressing MIR160 significantly impaired glandular trichome formation and suppressed artemisinin biosynthesis in A. annua, while repressing its expression resulted in the opposite effect, indicating that miR160 negatively regulates glandular trichome development and artemisinin biosynthesis. RNA ligase‐mediated 5′ RACE and transient transformation assays showed that miR160 mediates the RNA cleavage of Auxin Response Factor 1 (ARF1) in A. annua. Furthermore, ARF1 was shown to increase artemisinin synthesis by activating AaDBR2 expression. Taken together, our results reveal the intrinsic link between the miR160‐ARF1 module and artemisinin biosynthesis, and may expedite the innovation of metabolic engineering approaches for high and stable production of artemisinin in the future.
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spelling pubmed-99461452023-02-23 Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua Guo, Zhiying Hao, Kai Lv, Zongyou Yu, Luyao Bu, Qitao Ren, Junze Zhang, Henan Chen, Ruibing Zhang, Lei Plant Biotechnol J Research Articles MicroRNAs (miRNAs) play crucial roles in plant development and secondary metabolism through different modes of sequence‐specific interaction with their targets. Artemisinin biosynthesis is extensively regulated by phytohormones. However, the function of phytohormone‐responsive miRNAs in artemisinin biosynthesis remains enigmatic. Thus, we combined the analysis of transcriptomics, small RNAs, and the degradome to generate a comprehensive resource for identifying key miRNA‐target circuits involved in the phytohormone‐induced process of artemisinin biosynthesis in Artemisia annua. In total, 151 conserved and 52 novel miRNAs and their 4132 targets were determined. Based on the differential expression analysis, miR160 was selected as a potential miRNA involved in artemisinin synthesis. Overexpressing MIR160 significantly impaired glandular trichome formation and suppressed artemisinin biosynthesis in A. annua, while repressing its expression resulted in the opposite effect, indicating that miR160 negatively regulates glandular trichome development and artemisinin biosynthesis. RNA ligase‐mediated 5′ RACE and transient transformation assays showed that miR160 mediates the RNA cleavage of Auxin Response Factor 1 (ARF1) in A. annua. Furthermore, ARF1 was shown to increase artemisinin synthesis by activating AaDBR2 expression. Taken together, our results reveal the intrinsic link between the miR160‐ARF1 module and artemisinin biosynthesis, and may expedite the innovation of metabolic engineering approaches for high and stable production of artemisinin in the future. John Wiley and Sons Inc. 2022-12-20 2023-03 /pmc/articles/PMC9946145/ /pubmed/36478140 http://dx.doi.org/10.1111/pbi.13974 Text en © 2022 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Guo, Zhiying
Hao, Kai
Lv, Zongyou
Yu, Luyao
Bu, Qitao
Ren, Junze
Zhang, Henan
Chen, Ruibing
Zhang, Lei
Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title_full Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title_fullStr Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title_full_unstemmed Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title_short Profiling of phytohormone‐specific microRNAs and characterization of the miR160‐ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua
title_sort profiling of phytohormone‐specific micrornas and characterization of the mir160‐arf1 module involved in glandular trichome development and artemisinin biosynthesis in artemisia annua
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946145/
https://www.ncbi.nlm.nih.gov/pubmed/36478140
http://dx.doi.org/10.1111/pbi.13974
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