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Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis

Elena Babiychuk UGent, Pierrette Bouvier-Navé, Vincent Compagnon, Masashi Suzuki, Toshiya Muranaka, Marc Van Montagu UGent, Sergei Kushnir UGent and Hubert Schaller (2008) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 105(8). p.3163-3168
abstract
Sterols have multiple functions in all eukaryotes. In plants, sterol biosynthesis is initiated by the enzymatic conversion of 2,3-oxidosqualene to cycloartenol. This reaction is catalyzed by cycloartenol synthase 1 (CAS1), which belongs to a family of 13 2,3-oxidosqualene cyclases in Arabidopsis thaliana. To understand the full scope of sterol biological functions in plants, we characterized allelic series of cas1 mutations. Plants carrying the weak mutant allele cas1-1 were viable but developed albino inflorescence shoots because of photooxidation of plastids in stems that contained low amounts of carotenoids and chlorophylls. Consistent with the CAS1 catalyzed reaction, mutant tissues accumulated 2,3-oxidosqualene. This triterpenoid precursor did not increase at the expense of the pathway end products. Two strong mutations, cas1-2 and cas1-3, were not transmissible through the male gametes, suggesting a role for CAS1 in male gametophyte function. To validate these findings, we analyzed a conditional CRE/loxP recombination-dependent cas1-2 mutant allele. The albino phenotype of growing leaf tissues was a typical defect observed shortly after the CRE/ loxP-induced onset of CAS1 loss of function. In the induced casl-2 seedlings, terminal phenotypes included arrest of meristematic activity, followed by necrotic death. Mutant tissues accumulated 2,3-oxidosqualene and contained low amounts of sterols. The vital role of sterols in membrane functioning most probably explains the requirement of CAS1 for plant cell viability. The observed impact of cas1 mutations on a chloroplastic function implies a previously unrecognized role of sterols or triterpenoid metabolites in plastid biogenesis.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
sterols, albinism, triterpenoid metabolites, 2, 3-oxidosqualene, ISOPRENOID BIOSYNTHESIS, ENDOPLASMIC-RETICULUM, PLANT TRANSFORMATION, LANOSTEROL SYNTHASE, THALIANA, STEROLS, EXPRESSION, TRITERPENE, GENE, REDUCTASE
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
105
issue
8
pages
3163 - 3168
Web of Science type
Article
Web of Science id
000253567900074
ISSN
0027-8424
DOI
10.1073/pnas.0712190105
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
439465
handle
http://hdl.handle.net/1854/LU-439465
date created
2008-11-12 13:57:00
date last changed
2012-12-05 17:22:19
@article{439465,
  abstract     = {Sterols have multiple functions in all eukaryotes. In plants, sterol biosynthesis is initiated by the enzymatic conversion of 2,3-oxidosqualene to cycloartenol. This reaction is catalyzed by cycloartenol synthase 1 (CAS1), which belongs to a family of 13 2,3-oxidosqualene cyclases in Arabidopsis thaliana. To understand the full scope of sterol biological functions in plants, we characterized allelic series of cas1 mutations. Plants carrying the weak mutant allele cas1-1 were viable but developed albino inflorescence shoots because of photooxidation of plastids in stems that contained low amounts of carotenoids and chlorophylls. Consistent with the CAS1 catalyzed reaction, mutant tissues accumulated 2,3-oxidosqualene. This triterpenoid precursor did not increase at the expense of the pathway end products. Two strong mutations, cas1-2 and cas1-3, were not transmissible through the male gametes, suggesting a role for CAS1 in male gametophyte function. To validate these findings, we analyzed a conditional CRE/loxP recombination-dependent cas1-2 mutant allele. The albino phenotype of growing leaf tissues was a typical defect observed shortly after the CRE/ loxP-induced onset of CAS1 loss of function. In the induced casl-2 seedlings, terminal phenotypes included arrest of meristematic activity, followed by necrotic death. Mutant tissues accumulated 2,3-oxidosqualene and contained low amounts of sterols. The vital role of sterols in membrane functioning most probably explains the requirement of CAS1 for plant cell viability. The observed impact of cas1 mutations on a chloroplastic function implies a previously unrecognized role of sterols or triterpenoid metabolites in plastid biogenesis.},
  author       = {Babiychuk, Elena and Bouvier-Nav{\'e}, Pierrette and Compagnon, Vincent and Suzuki, Masashi and Muranaka, Toshiya and Van Montagu, Marc and Kushnir, Sergei and Schaller, Hubert},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {sterols,albinism,triterpenoid metabolites,2,3-oxidosqualene,ISOPRENOID BIOSYNTHESIS,ENDOPLASMIC-RETICULUM,PLANT TRANSFORMATION,LANOSTEROL SYNTHASE,THALIANA,STEROLS,EXPRESSION,TRITERPENE,GENE,REDUCTASE},
  language     = {eng},
  number       = {8},
  pages        = {3163--3168},
  title        = {Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis},
  url          = {http://dx.doi.org/10.1073/pnas.0712190105},
  volume       = {105},
  year         = {2008},
}

Chicago
Babiychuk, Elena, Pierrette Bouvier-Navé, Vincent Compagnon, Masashi Suzuki, Toshiya Muranaka, Marc Van Montagu, Sergei Kushnir, and Hubert Schaller. 2008. “Allelic Mutant Series Reveal Distinct Functions for Arabidopsis Cycloartenol Synthase 1 in Cell Viability and Plastid Biogenesis.” Proceedings of the National Academy of Sciences of the United States of America 105 (8): 3163–3168.
APA
Babiychuk, E., Bouvier-Navé, P., Compagnon, V., Suzuki, M., Muranaka, T., Van Montagu, M., Kushnir, S., et al. (2008). Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 105(8), 3163–3168.
Vancouver
1.
Babiychuk E, Bouvier-Navé P, Compagnon V, Suzuki M, Muranaka T, Van Montagu M, et al. Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2008;105(8):3163–8.
MLA
Babiychuk, Elena, Pierrette Bouvier-Navé, Vincent Compagnon, et al. “Allelic Mutant Series Reveal Distinct Functions for Arabidopsis Cycloartenol Synthase 1 in Cell Viability and Plastid Biogenesis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 105.8 (2008): 3163–3168. Print.