Frontiers in Plant Science (May 2021)

Subfunctionalization of Paralog Transcription Factors Contributes to Regulation of Alkaloid Pathway Branch Choice in Catharanthus roseus

  • Maite Colinas,
  • Maite Colinas,
  • Jacob Pollier,
  • Jacob Pollier,
  • Dries Vaneechoutte,
  • Dries Vaneechoutte,
  • Deniz G. Malat,
  • Deniz G. Malat,
  • Fabian Schweizer,
  • Fabian Schweizer,
  • Liesbeth De Milde,
  • Liesbeth De Milde,
  • Rebecca De Clercq,
  • Rebecca De Clercq,
  • Joana G. Guedes,
  • Joana G. Guedes,
  • Joana G. Guedes,
  • Teresa Martínez-Cortés,
  • Francisco J. Molina-Hidalgo,
  • Francisco J. Molina-Hidalgo,
  • Mariana Sottomayor,
  • Mariana Sottomayor,
  • Klaas Vandepoele,
  • Klaas Vandepoele,
  • Alain Goossens,
  • Alain Goossens

DOI
https://doi.org/10.3389/fpls.2021.687406
Journal volume & issue
Vol. 12

Abstract

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Catharanthus roseus produces a diverse range of specialized metabolites of the monoterpenoid indole alkaloid (MIA) class in a heavily branched pathway. Recent great progress in identification of MIA biosynthesis genes revealed that the different pathway branch genes are expressed in a highly cell type- and organ-specific and stress-dependent manner. This implies a complex control by specific transcription factors (TFs), only partly revealed today. We generated and mined a comprehensive compendium of publicly available C. roseus transcriptome data for MIA pathway branch-specific TFs. Functional analysis was performed through extensive comparative gene expression analysis and profiling of over 40 MIA metabolites in the C. roseus flower petal expression system. We identified additional members of the known BIS and ORCA regulators. Further detailed study of the ORCA TFs suggests subfunctionalization of ORCA paralogs in terms of target gene-specific regulation and synergistic activity with the central jasmonate response regulator MYC2. Moreover, we identified specific amino acid residues within the ORCA DNA-binding domains that contribute to the differential regulation of some MIA pathway branches. Our results advance our understanding of TF paralog specificity for which, despite the common occurrence of closely related paralogs in many species, comparative studies are scarce.

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