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Iridoid synthase activity is common among the plant progesterone 5β-reductase family

Munkert, Jennifer; Pollier, Jacob; Miettinen, Karel; Van Moerkercke, Alex LU ; Payne, Richard J.; Müller-Uri, Frieder; Burlat, Vincent; O'Connor, Sarah E; Memelink, Johan and Kreis, Wolfgang, et al. (2015) In Molecular Plant 8(1). p.136-152
Abstract

Catharanthus roseus, the Madagascar periwinkle, synthesizes bioactive monoterpenoid indole alkaloids, including the anti-cancer drugs vinblastine and vincristine. The monoterpenoid branch of the alkaloid pathway leads to the secoiridoid secologanin and involves the enzyme iridoid synthase (IS), a member of the progesterone 5β-reductase (P5βR) family. IS reduces 8-oxogeranial to iridodial. Through transcriptome mining, we show that IS belongs to a family of six C. roseus P5βR genes. Characterization of recombinant CrP5βR proteins demonstrates that all but CrP5βR3 can reduce progesterone and thus can be classified as P5βRs. Three of them, namely CrP5βR1, CrP5βR2, and CrP5βR4, can also reduce 8-oxogeranial, pointing to a possible... (More)

Catharanthus roseus, the Madagascar periwinkle, synthesizes bioactive monoterpenoid indole alkaloids, including the anti-cancer drugs vinblastine and vincristine. The monoterpenoid branch of the alkaloid pathway leads to the secoiridoid secologanin and involves the enzyme iridoid synthase (IS), a member of the progesterone 5β-reductase (P5βR) family. IS reduces 8-oxogeranial to iridodial. Through transcriptome mining, we show that IS belongs to a family of six C. roseus P5βR genes. Characterization of recombinant CrP5βR proteins demonstrates that all but CrP5βR3 can reduce progesterone and thus can be classified as P5βRs. Three of them, namely CrP5βR1, CrP5βR2, and CrP5βR4, can also reduce 8-oxogeranial, pointing to a possible redundancy with IS (corresponding to CrP5βR5) in secoiridoid synthesis. In-depth functional analysis by subcellular protein localization, gene expression analysis, in situ hybridization, and virus-induced gene silencing indicate that besides IS, CrP5βR4 may also participate in secoiridoid biosynthesis. We cloned a set of P5βR genes from angiosperm plant species not known to produce iridoids and demonstrate that the corresponding recombinant proteins are also capable of using 8-oxogeranial as a substrate. This suggests that IS activity is intrinsic to angiosperm P5βR proteins and has evolved early during evolution.

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published
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keywords
Catharanthus, Gene Expression Regulation, Plant, Iridoids, Molecular Sequence Data, Plant Proteins, Progesterone Reductase, Journal Article, Research Support, Non-U.S. Gov't
in
Molecular Plant
volume
8
issue
1
pages
17 pages
publisher
Oxford University Press
external identifiers
  • scopus:84925059997
ISSN
1752-9867
DOI
10.1016/j.molp.2014.11.005
language
English
LU publication?
no
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37768b3f-4ece-45db-8da9-1b29d7a02837
date added to LUP
2017-11-06 11:30:39
date last changed
2018-05-13 04:36:29
@article{37768b3f-4ece-45db-8da9-1b29d7a02837,
  abstract     = {<p>Catharanthus roseus, the Madagascar periwinkle, synthesizes bioactive monoterpenoid indole alkaloids, including the anti-cancer drugs vinblastine and vincristine. The monoterpenoid branch of the alkaloid pathway leads to the secoiridoid secologanin and involves the enzyme iridoid synthase (IS), a member of the progesterone 5β-reductase (P5βR) family. IS reduces 8-oxogeranial to iridodial. Through transcriptome mining, we show that IS belongs to a family of six C. roseus P5βR genes. Characterization of recombinant CrP5βR proteins demonstrates that all but CrP5βR3 can reduce progesterone and thus can be classified as P5βRs. Three of them, namely CrP5βR1, CrP5βR2, and CrP5βR4, can also reduce 8-oxogeranial, pointing to a possible redundancy with IS (corresponding to CrP5βR5) in secoiridoid synthesis. In-depth functional analysis by subcellular protein localization, gene expression analysis, in situ hybridization, and virus-induced gene silencing indicate that besides IS, CrP5βR4 may also participate in secoiridoid biosynthesis. We cloned a set of P5βR genes from angiosperm plant species not known to produce iridoids and demonstrate that the corresponding recombinant proteins are also capable of using 8-oxogeranial as a substrate. This suggests that IS activity is intrinsic to angiosperm P5βR proteins and has evolved early during evolution.</p>},
  author       = {Munkert, Jennifer and Pollier, Jacob and Miettinen, Karel and Van Moerkercke, Alex and Payne, Richard J. and Müller-Uri, Frieder and Burlat, Vincent and O'Connor, Sarah E and Memelink, Johan and Kreis, Wolfgang and Goossens, Alain},
  issn         = {1752-9867},
  keyword      = {Catharanthus,Gene Expression Regulation, Plant,Iridoids,Molecular Sequence Data,Plant Proteins,Progesterone Reductase,Journal Article,Research Support, Non-U.S. Gov't},
  language     = {eng},
  number       = {1},
  pages        = {136--152},
  publisher    = {Oxford University Press},
  series       = {Molecular Plant},
  title        = {Iridoid synthase activity is common among the plant progesterone 5β-reductase family},
  url          = {http://dx.doi.org/10.1016/j.molp.2014.11.005},
  volume       = {8},
  year         = {2015},
}