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Clade IVa Basic Helix-Loop-Helix Transcription Factors Form Part of a Conserved Jasmonate Signaling Circuit for the Regulation of Bioactive Plant Terpenoid Biosynthesis

Mertens, Jan ; Van Moerkercke, Alex LU ; Vanden Bossche, Robin ; Pollier, Jacob and Goossens, Alain (2016) In Plant and Cell Physiology 57(12). p.2564-2575
Abstract

Plants produce many bioactive, specialized metabolites to defend themselves when facing various stress situations. Their biosynthesis is directed by a tightly controlled regulatory circuit that is elicited by phytohormones such as jasmonate (JA). The basic helix-loop-helix (bHLH) transcription factors (TFs) bHLH iridoid synthesis 1 (BIS1) and Triterpene Saponin Activating Regulator (TSAR) 1 and 2, from Catharanthus roseus and Medicago truncatula, respectively, all belong to clade IVa of the bHLH protein family and activate distinct terpenoid pathways, thereby mediating monoterpenoid indole alkaloid (MIA) and triterpene saponin (TS) accumulation, respectively, in these two species. In this study, we report that promoters of the genes... (More)

Plants produce many bioactive, specialized metabolites to defend themselves when facing various stress situations. Their biosynthesis is directed by a tightly controlled regulatory circuit that is elicited by phytohormones such as jasmonate (JA). The basic helix-loop-helix (bHLH) transcription factors (TFs) bHLH iridoid synthesis 1 (BIS1) and Triterpene Saponin Activating Regulator (TSAR) 1 and 2, from Catharanthus roseus and Medicago truncatula, respectively, all belong to clade IVa of the bHLH protein family and activate distinct terpenoid pathways, thereby mediating monoterpenoid indole alkaloid (MIA) and triterpene saponin (TS) accumulation, respectively, in these two species. In this study, we report that promoters of the genes encoding the enzymes involved in the specific terpenoid pathway of one of these species can be transactivated by the orthologous bHLH factor from the other species through recognition of the same cis-regulatory elements. Accordingly, ectopic expression of CrBIS1 in M. truncatula hairy roots up-regulated the expression of all genes required for soyasaponin production, resulting in strongly increased levels of soyasaponins in the transformed roots. Likewise, transient expression of MtTSAR1 and MtTSAR2 in C. roseus petals led to up-regulation of the genes involved in the iridoid branch of the MIA pathway. Together, our data illustrate the functional similarity of these JA-inducible TFs and indicate that recruitment of defined cis-regulatory elements constitutes an important aspect of the evolution of conserved regulatory modules for the activation of species-specific terpenoid biosynthesis pathways by common signals such as the JA phytohormones.

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author
; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Alkaloids, Basic Helix-Loop-Helix Transcription Factors, Catharanthus, Cyclopentanes, Flowers, Gene Expression Regulation, Plant, Medicago truncatula, Oxylipins, Plant Growth Regulators, Plant Proteins, Plant Roots, Plants, Genetically Modified, Promoter Regions, Genetic, Saponins, Signal Transduction, Terpenes, Up-Regulation, Journal Article
in
Plant and Cell Physiology
volume
57
issue
12
pages
12 pages
publisher
Oxford University Press
external identifiers
  • scopus:85014183882
  • pmid:27694525
ISSN
1471-9053
DOI
10.1093/pcp/pcw168
language
English
LU publication?
no
id
0c8e7b44-d773-4c76-a7dd-69bffe00097f
date added to LUP
2017-11-06 11:29:11
date last changed
2024-03-17 22:15:24
@article{0c8e7b44-d773-4c76-a7dd-69bffe00097f,
  abstract     = {{<p>Plants produce many bioactive, specialized metabolites to defend themselves when facing various stress situations. Their biosynthesis is directed by a tightly controlled regulatory circuit that is elicited by phytohormones such as jasmonate (JA). The basic helix-loop-helix (bHLH) transcription factors (TFs) bHLH iridoid synthesis 1 (BIS1) and Triterpene Saponin Activating Regulator (TSAR) 1 and 2, from Catharanthus roseus and Medicago truncatula, respectively, all belong to clade IVa of the bHLH protein family and activate distinct terpenoid pathways, thereby mediating monoterpenoid indole alkaloid (MIA) and triterpene saponin (TS) accumulation, respectively, in these two species. In this study, we report that promoters of the genes encoding the enzymes involved in the specific terpenoid pathway of one of these species can be transactivated by the orthologous bHLH factor from the other species through recognition of the same cis-regulatory elements. Accordingly, ectopic expression of CrBIS1 in M. truncatula hairy roots up-regulated the expression of all genes required for soyasaponin production, resulting in strongly increased levels of soyasaponins in the transformed roots. Likewise, transient expression of MtTSAR1 and MtTSAR2 in C. roseus petals led to up-regulation of the genes involved in the iridoid branch of the MIA pathway. Together, our data illustrate the functional similarity of these JA-inducible TFs and indicate that recruitment of defined cis-regulatory elements constitutes an important aspect of the evolution of conserved regulatory modules for the activation of species-specific terpenoid biosynthesis pathways by common signals such as the JA phytohormones.</p>}},
  author       = {{Mertens, Jan and Van Moerkercke, Alex and Vanden Bossche, Robin and Pollier, Jacob and Goossens, Alain}},
  issn         = {{1471-9053}},
  keywords     = {{Alkaloids; Basic Helix-Loop-Helix Transcription Factors; Catharanthus; Cyclopentanes; Flowers; Gene Expression Regulation, Plant; Medicago truncatula; Oxylipins; Plant Growth Regulators; Plant Proteins; Plant Roots; Plants, Genetically Modified; Promoter Regions, Genetic; Saponins; Signal Transduction; Terpenes; Up-Regulation; Journal Article}},
  language     = {{eng}},
  number       = {{12}},
  pages        = {{2564--2575}},
  publisher    = {{Oxford University Press}},
  series       = {{Plant and Cell Physiology}},
  title        = {{Clade IVa Basic Helix-Loop-Helix Transcription Factors Form Part of a Conserved Jasmonate Signaling Circuit for the Regulation of Bioactive Plant Terpenoid Biosynthesis}},
  url          = {{http://dx.doi.org/10.1093/pcp/pcw168}},
  doi          = {{10.1093/pcp/pcw168}},
  volume       = {{57}},
  year         = {{2016}},
}