Clade IVa Basic Helix-Loop-Helix Transcription Factors Form Part of a Conserved Jasmonate Signaling Circuit for the Regulation of Bioactive Plant Terpenoid Biosynthesis.
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.
Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium.|These authors contributed equally to this work.
Jan
J
Mertens
Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium.|These authors contributed equally to this work.
Alex
A
Van Moerkercke
Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium.
Robin
R
Vanden Bossche
Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium.|Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium.
Jacob
J
Pollier
Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium algoo@psb.vib-ugent.be.|Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium.
Alain
A
Goossens
D000470:Alkaloids / Q000378:metabolism; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics / Q000378:metabolism*; D030008:Catharanthus / Q000235:genetics* / Q000502:physiology; D003517:Cyclopentanes / Q000378:metabolism*; D035264:Flowers / Q000235:genetics / Q000502:physiology; D018506:Gene Expression Regulation, Plant; D046913:Medicago truncatula / Q000235:genetics* / Q000502:physiology; D054883:Oxylipins / Q000378:metabolism*; D010937:Plant Growth Regulators / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000235:genetics / Q000502:physiology; D030821:Plants, Genetically Modified; D011401:Promoter Regions, Genetic / Q000235:genetics; D012503:Saponins / Q000378:metabolism; D015398:Signal Transduction; D013729:Terpenes / Q000378:metabolism*; D015854:Up-Regulation
D000470:Alkaloids; D051792:Basic Helix-Loop-Helix Proteins; D003517:Cyclopentanes; D054883:Oxylipins; D010937:Plant Growth Regulators; D010940:Plant Proteins; D012503:Saponins; D013729:Terpenes; C011006:jasmonic acid
Catharanthus roseus; Jasmonate; Medicago truncatula; Monoterpenoid indole alkaloids; Triterpene saponins; bHLH transcription factors