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Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)

Lotus (Nelumbo nucifera) is a large aquatic plant that accumulates pharmacologically significant benzylisoquinoline alkaloids (BIAs). However, little is known about their biosynthesis and regulation. Here, we show that the two group III WRKY transcription factors (TFs), NnWRKY70a and NnWRKY70b, posi...

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Autores principales: Li, Jing, Li, Yi, Dang, Mingjing, Li, Shang, Chen, Simeng, Liu, Ruizhen, Zhang, Zeyu, Li, Guoqian, Zhang, Minghua, Yang, Dong, Yang, Mei, Liu, Yanling, Tian, Daike, Deng, Xianbao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9240598/
https://www.ncbi.nlm.nih.gov/pubmed/35783938
http://dx.doi.org/10.3389/fpls.2022.862915
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author Li, Jing
Li, Yi
Dang, Mingjing
Li, Shang
Chen, Simeng
Liu, Ruizhen
Zhang, Zeyu
Li, Guoqian
Zhang, Minghua
Yang, Dong
Yang, Mei
Liu, Yanling
Tian, Daike
Deng, Xianbao
author_facet Li, Jing
Li, Yi
Dang, Mingjing
Li, Shang
Chen, Simeng
Liu, Ruizhen
Zhang, Zeyu
Li, Guoqian
Zhang, Minghua
Yang, Dong
Yang, Mei
Liu, Yanling
Tian, Daike
Deng, Xianbao
author_sort Li, Jing
collection PubMed
description Lotus (Nelumbo nucifera) is a large aquatic plant that accumulates pharmacologically significant benzylisoquinoline alkaloids (BIAs). However, little is known about their biosynthesis and regulation. Here, we show that the two group III WRKY transcription factors (TFs), NnWRKY70a and NnWRKY70b, positively regulate the BIA biosynthesis in lotus. Both NnWRKY70s are jasmonic acid (JA) responsive, with their expression profiles highly correlated to the BIA concentration and BIA pathway gene expression. A dual-luciferase assay showed that NnWRKY70a could transactivate the NnTYDC promoter, whereas NnWRKY70b could activate promoters of the three BIA structural genes, including NnTYDC, NnCYP80G, and Nn7OMT. In addition, the transient overexpression of NnWRKY70a and NnWRKY70b in lotus petals significantly elevated the BIA alkaloid concentrations. Notably, NnWRKY70b seems to be a stronger BIA biosynthesis regulator, because it dramatically induced more BIA structural gene expressions and BIA accumulation than NnWRKY70a. A yeast two-hybrid assay further revealed that NnWRKY70b physically interacted with NnJAZ1 and two other group III WRKY TFs (NnWRKY53b and NnWRKY70a), suggesting that it may cooperate with the other group III WRKYs to adjust the lotus BIA biosynthesis via the JA-signaling pathway. To illustrate the mechanism underlying NnWRKY70b-mediated BIA regulation in the lotus, a simplified model is proposed. Our study provides useful insights into the regulatory roles of WRKY TFs in the biosynthesis of secondary metabolites.
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spelling pubmed-92405982022-06-30 Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera) Li, Jing Li, Yi Dang, Mingjing Li, Shang Chen, Simeng Liu, Ruizhen Zhang, Zeyu Li, Guoqian Zhang, Minghua Yang, Dong Yang, Mei Liu, Yanling Tian, Daike Deng, Xianbao Front Plant Sci Plant Science Lotus (Nelumbo nucifera) is a large aquatic plant that accumulates pharmacologically significant benzylisoquinoline alkaloids (BIAs). However, little is known about their biosynthesis and regulation. Here, we show that the two group III WRKY transcription factors (TFs), NnWRKY70a and NnWRKY70b, positively regulate the BIA biosynthesis in lotus. Both NnWRKY70s are jasmonic acid (JA) responsive, with their expression profiles highly correlated to the BIA concentration and BIA pathway gene expression. A dual-luciferase assay showed that NnWRKY70a could transactivate the NnTYDC promoter, whereas NnWRKY70b could activate promoters of the three BIA structural genes, including NnTYDC, NnCYP80G, and Nn7OMT. In addition, the transient overexpression of NnWRKY70a and NnWRKY70b in lotus petals significantly elevated the BIA alkaloid concentrations. Notably, NnWRKY70b seems to be a stronger BIA biosynthesis regulator, because it dramatically induced more BIA structural gene expressions and BIA accumulation than NnWRKY70a. A yeast two-hybrid assay further revealed that NnWRKY70b physically interacted with NnJAZ1 and two other group III WRKY TFs (NnWRKY53b and NnWRKY70a), suggesting that it may cooperate with the other group III WRKYs to adjust the lotus BIA biosynthesis via the JA-signaling pathway. To illustrate the mechanism underlying NnWRKY70b-mediated BIA regulation in the lotus, a simplified model is proposed. Our study provides useful insights into the regulatory roles of WRKY TFs in the biosynthesis of secondary metabolites. Frontiers Media S.A. 2022-06-15 /pmc/articles/PMC9240598/ /pubmed/35783938 http://dx.doi.org/10.3389/fpls.2022.862915 Text en Copyright © 2022 Li, Li, Dang, Li, Chen, Liu, Zhang, Li, Zhang, Yang, Yang, Liu, Tian and Deng. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Li, Jing
Li, Yi
Dang, Mingjing
Li, Shang
Chen, Simeng
Liu, Ruizhen
Zhang, Zeyu
Li, Guoqian
Zhang, Minghua
Yang, Dong
Yang, Mei
Liu, Yanling
Tian, Daike
Deng, Xianbao
Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title_full Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title_fullStr Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title_full_unstemmed Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title_short Jasmonate-Responsive Transcription Factors NnWRKY70a and NnWRKY70b Positively Regulate Benzylisoquinoline Alkaloid Biosynthesis in Lotus (Nelumbo nucifera)
title_sort jasmonate-responsive transcription factors nnwrky70a and nnwrky70b positively regulate benzylisoquinoline alkaloid biosynthesis in lotus (nelumbo nucifera)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9240598/
https://www.ncbi.nlm.nih.gov/pubmed/35783938
http://dx.doi.org/10.3389/fpls.2022.862915
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