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The basic helix-loop-helix transcription factor BIS2 is essential for monoterpenoid indole alkaloid production in the medicinal plant Catharanthus roseus

Van Moerkercke, Alex LU ; Steensma, Priscille ; Gariboldi, Ivo ; Espoz, Javiera ; Purnama, Purin C ; Schweizer, Fabian ; Miettinen, Karel ; Vanden Bossche, Robin ; De Clercq, Rebecca and Memelink, Johan , et al. (2016) In Plant Journal 88(1). p.3-12
Abstract

Monoterpenoid indole alkaloids (MIAs) are produced as plant defence compounds. In the medicinal plant Catharanthus roseus, they comprise the anticancer compounds vinblastine and vincristine. The iridoid (monoterpenoid) pathway forms one of the two branches that feed MIA biosynthesis and its activation is regulated by the transcription factor (TF) basic helix-loop-helix (bHLH) iridoid synthesis 1 (BIS1). Here, we describe the identification and characterisation of BIS2, a jasmonate (JA)-responsive bHLH TF expressed preferentially in internal phloem-associated parenchyma cells, which transactivates promoters of iridoid biosynthesis genes and can homodimerise or form heterodimers with BIS1. Stable overexpression of BIS2 in C. roseus... (More)

Monoterpenoid indole alkaloids (MIAs) are produced as plant defence compounds. In the medicinal plant Catharanthus roseus, they comprise the anticancer compounds vinblastine and vincristine. The iridoid (monoterpenoid) pathway forms one of the two branches that feed MIA biosynthesis and its activation is regulated by the transcription factor (TF) basic helix-loop-helix (bHLH) iridoid synthesis 1 (BIS1). Here, we describe the identification and characterisation of BIS2, a jasmonate (JA)-responsive bHLH TF expressed preferentially in internal phloem-associated parenchyma cells, which transactivates promoters of iridoid biosynthesis genes and can homodimerise or form heterodimers with BIS1. Stable overexpression of BIS2 in C. roseus suspension cells and transient ectopic expression of BIS2 in C. roseus petal limbs resulted in increased transcript accumulation of methylerythritol-4-phosphate and iridoid pathway genes, but not of other MIA genes or triterpenoid genes. Transcript profiling also indicated that BIS2 expression is part of an amplification loop, as it is induced by overexpression of either BIS1 or BIS2. Accordingly, silencing of BIS2 in C. roseus suspension cells completely abolished the JA-induced upregulation of the iridoid pathway genes and subsequent MIA accumulation, despite the presence of induced BIS1, indicating that BIS2 is essential for MIA production in C. roseus.

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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Basic Helix-Loop-Helix Transcription Factors, Catharanthus, Gene Expression Regulation, Plant, Indole Alkaloids, Plant Proteins, Plants, Medicinal, Journal Article
in
Plant Journal
volume
88
issue
1
pages
10 pages
publisher
Wiley-Blackwell
external identifiers
  • pmid:27342401
  • scopus:84982085352
ISSN
1365-313X
DOI
10.1111/tpj.13230
language
English
LU publication?
no
id
f0ea991f-6634-4dba-b857-58dad234308a
date added to LUP
2017-11-06 11:28:12
date last changed
2024-06-11 05:31:28
@article{f0ea991f-6634-4dba-b857-58dad234308a,
  abstract     = {{<p>Monoterpenoid indole alkaloids (MIAs) are produced as plant defence compounds. In the medicinal plant Catharanthus roseus, they comprise the anticancer compounds vinblastine and vincristine. The iridoid (monoterpenoid) pathway forms one of the two branches that feed MIA biosynthesis and its activation is regulated by the transcription factor (TF) basic helix-loop-helix (bHLH) iridoid synthesis 1 (BIS1). Here, we describe the identification and characterisation of BIS2, a jasmonate (JA)-responsive bHLH TF expressed preferentially in internal phloem-associated parenchyma cells, which transactivates promoters of iridoid biosynthesis genes and can homodimerise or form heterodimers with BIS1. Stable overexpression of BIS2 in C. roseus suspension cells and transient ectopic expression of BIS2 in C. roseus petal limbs resulted in increased transcript accumulation of methylerythritol-4-phosphate and iridoid pathway genes, but not of other MIA genes or triterpenoid genes. Transcript profiling also indicated that BIS2 expression is part of an amplification loop, as it is induced by overexpression of either BIS1 or BIS2. Accordingly, silencing of BIS2 in C. roseus suspension cells completely abolished the JA-induced upregulation of the iridoid pathway genes and subsequent MIA accumulation, despite the presence of induced BIS1, indicating that BIS2 is essential for MIA production in C. roseus.</p>}},
  author       = {{Van Moerkercke, Alex and Steensma, Priscille and Gariboldi, Ivo and Espoz, Javiera and Purnama, Purin C and Schweizer, Fabian and Miettinen, Karel and Vanden Bossche, Robin and De Clercq, Rebecca and Memelink, Johan and Goossens, Alain}},
  issn         = {{1365-313X}},
  keywords     = {{Basic Helix-Loop-Helix Transcription Factors; Catharanthus; Gene Expression Regulation, Plant; Indole Alkaloids; Plant Proteins; Plants, Medicinal; Journal Article}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{3--12}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Plant Journal}},
  title        = {{The basic helix-loop-helix transcription factor BIS2 is essential for monoterpenoid indole alkaloid production in the medicinal plant Catharanthus roseus}},
  url          = {{http://dx.doi.org/10.1111/tpj.13230}},
  doi          = {{10.1111/tpj.13230}},
  volume       = {{88}},
  year         = {{2016}},
}