Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus

Summary Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors contr...

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Published inPlant biotechnology journal Vol. 19; no. 4; pp. 671 - 688
Main Authors Zhao, Chenning, Liu, Xiaojuan, Gong, Qin, Cao, Jinping, Shen, Wanxia, Yin, Xueren, Grierson, Donald, Zhang, Bo, Xu, Changjie, Li, Xian, Chen, Kunsong, Sun, Chongde
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.04.2021
John Wiley and Sons Inc
Subjects
Accumulation
Arabidopsis
Binding
Bioactive compounds
Biosynthesis
biotechnology
catalytic activity
chalcone
Chalcone isomerase
Chalcone synthase
Citrus
Citrus - genetics
Citrus - metabolism
Citrus fruits
Dehydration
DREB
Enzymes
flavanone
flavone
Flavones
Flavonoids
Fruits
Gene expression
Gene Expression Regulation, Plant
Genomes
Intramolecular Lyases
Naringenin
naringenin-chalcone synthase
Phylogenetics
Plant Proteins - genetics
Plant Proteins - metabolism
Proteins
RAV
Regulatory sequences
RNA
RNA-mediated interference
Substrates
transcription (genetics)
Transcription factors
type IV chalcone isomerase
flavanone
DREB
type IV chalcone isomerase
RAV
flavone
citrus
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Abstract Summary Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to (2S)‐naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference‐induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration‐responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB‐RAV transcriptional complex regulating flavonoid production.
AbstractList Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to (2S)‐naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference‐induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration‐responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB‐RAV transcriptional complex regulating flavonoid production.
Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to (2S)-naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference-induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration-responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB-RAV transcriptional complex regulating flavonoid production.Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to (2S)-naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference-induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration-responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB-RAV transcriptional complex regulating flavonoid production.
Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to ( 2S )‐naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference‐induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration‐responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB‐RAV transcriptional complex regulating flavonoid production.
Summary Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone isomerase (CHI) family proteins play essential roles in flavonoid biosynthesis but little are known about the transcription factors controlling their gene expression. Here, we identified a type IV CHI (designated as CitCHIL1) from citrus which enhances the accumulation of citrus flavanones and flavones (CFLs). CitCHIL1 participates in a CFL biosynthetic metabolon and assists the cyclization of naringenin chalcone to (2S)‐naringenin, which leads to the efficient influx of substrates to chalcone synthase (CHS) and improves the catalytic efficiency of CHS. Overexpressing CitCHIL1 in Citrus and Arabidopsis significantly increased flavonoid content and RNA interference‐induced silencing of CitCHIL1 in citrus led to a 43% reduction in CFL content. Three AP2/ERF transcription factors were identified as positive regulators of the CitCHIL1 expression. Of these, two dehydration‐responsive element binding (DREB) proteins, CitERF32 and CitERF33, activated the transcription by directly binding to the CGCCGC motif in the promoter, while CitRAV1 (RAV: related to ABI3/VP1) formed a transcription complex with CitERF33 that strongly enhanced the activation efficiency and flavonoid accumulation. These results not only illustrate the specific function that CitCHIL1 executes in CFL biosynthesis but also reveal a new DREB‐RAV transcriptional complex regulating flavonoid production.
Author Shen, Wanxia
Chen, Kunsong
Li, Xian
Zhang, Bo
Gong, Qin
Zhao, Chenning
Yin, Xueren
Sun, Chongde
Liu, Xiaojuan
Xu, Changjie
Grierson, Donald
Cao, Jinping
AuthorAffiliation 2 Citrus Research Institute Southwest University/Chinese Academy of Agricultural Sciences Chongqing China
1 Laboratory of Fruit Quality Biology/Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology/The State Agriculture Ministry Laboratory of Horticultural Plant Growth Development and Quality Improvement Zhejiang University Hangzhou China
3 Division of Plant and Crop Sciences School of Biosciences University of Nottingham Loughborough UK
AuthorAffiliation_xml – name: 1 Laboratory of Fruit Quality Biology/Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology/The State Agriculture Ministry Laboratory of Horticultural Plant Growth Development and Quality Improvement Zhejiang University Hangzhou China
– name: 3 Division of Plant and Crop Sciences School of Biosciences University of Nottingham Loughborough UK
– name: 2 Citrus Research Institute Southwest University/Chinese Academy of Agricultural Sciences Chongqing China
Author_xml – sequence: 1
  givenname: Chenning
  surname: Zhao
  fullname: Zhao, Chenning
  organization: Zhejiang University
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  fullname: Liu, Xiaojuan
  organization: Zhejiang University
– sequence: 3
  givenname: Qin
  surname: Gong
  fullname: Gong, Qin
  organization: Zhejiang University
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  surname: Cao
  fullname: Cao, Jinping
  organization: Zhejiang University
– sequence: 5
  givenname: Wanxia
  surname: Shen
  fullname: Shen, Wanxia
  organization: Southwest University/Chinese Academy of Agricultural Sciences
– sequence: 6
  givenname: Xueren
  orcidid: 0000-0002-1282-4432
  surname: Yin
  fullname: Yin, Xueren
  organization: Zhejiang University
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  surname: Grierson
  fullname: Grierson, Donald
  organization: University of Nottingham
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  surname: Zhang
  fullname: Zhang, Bo
  organization: Zhejiang University
– sequence: 9
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  orcidid: 0000-0001-6284-6878
  surname: Xu
  fullname: Xu, Changjie
  organization: Zhejiang University
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  givenname: Xian
  surname: Li
  fullname: Li, Xian
  organization: Zhejiang University
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  givenname: Chongde
  orcidid: 0000-0002-2874-0292
  surname: Sun
  fullname: Sun, Chongde
  email: adesun2006@zju.edu.cn
  organization: Zhejiang University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33089636$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2020 The Authors. Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2020 The Authors. Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
– notice: 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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DocumentTitleAlternate CitCHIL1 and three TFs enhance flavonoid synthesis
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Issue 4
Keywords flavanone
DREB
type IV chalcone isomerase
RAV
flavone
citrus
Language English
License Attribution
2020 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet Summary Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive....
Flavanones and flavones are excellent source of bioactive compounds but the molecular basis of their highly efficient production remains elusive. Chalcone...
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SubjectTerms Accumulation
Arabidopsis
Binding
Bioactive compounds
Biosynthesis
biotechnology
catalytic activity
chalcone
Chalcone isomerase
Chalcone synthase
Citrus
Citrus - genetics
Citrus - metabolism
Citrus fruits
Dehydration
DREB
Enzymes
flavanone
flavone
Flavones
Flavonoids
Fruits
Gene expression
Gene Expression Regulation, Plant
Genomes
Intramolecular Lyases
Naringenin
naringenin-chalcone synthase
Phylogenetics
Plant Proteins - genetics
Plant Proteins - metabolism
Proteins
RAV
Regulatory sequences
RNA
RNA-mediated interference
Substrates
transcription (genetics)
Transcription factors
type IV chalcone isomerase
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Title Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.13494
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Volume 19
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