The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development

Liên Bach, Louise V. Michaelson, Richard Haslam, Yannick Bellec, Lionel Gissot, Jessica Marion, Marco Da Costa, Jean Pierre Boutin, Martine Miquel, Frédérique Tellier, Frederic Domergue, Jonathan E Markham, Frederic Beaudoin, Johnathan A. Napier, Jean Denis Faure

Research output: Contribution to journalArticle

125 Citations (Scopus)

Abstract

Very-long-chain fatty acids (VLCFAs) are synthesized as acyl-CoAs by the endoplasmic reticulum-localized elongase multiprotein complex. Two Arabidopsis genes are putative homologues of the recently identified yeast 3-hydroxy-acyl-CoA dehydratase (PHS1), the third enzyme of the elongase complex. We showed that Arabidopsis PASTICCINO2 (PAS2) was able to restore phs1 cytokinesis defects and sphingolipid long chain base overaccumulation. Conversely, the expression of PHS1 was able to complement the developmental defects and the accumulation of long chain bases of the pas2-1 mutant. The pas2-1 mutant was characterized by a general reduction of VLCFA pools in seed storage triacylglycerols, cuticular waxes, and complex sphingolipids. Most strikingly, the defective elongation cycle resulted in the accumulation of 3-hydroxy-acyl-CoA intermediates, indicating premature termination of fatty acid elongation and confirming the role of PAS2 in this process. We demonstrated by in vivo bimolecular fluorescence complementation that PAS2 was specifically associated in the endoplasmic reticulum with the enoyl-CoA reductase CER10, the fourth enzyme of the elongase complex. Finally, complete loss of PAS2 function is embryo lethal, and the ectopic expression of PHS1 led to enhanced levels of VLCFAs associated with severe developmental defects. Altogether these results demonstrate that the plant 3-hydroxy-acyl-CoA dehydratase PASTICCINO2 is an essential and limiting enzyme in VLCFA synthesis but also that PAS2-derived VLCFA homeostasis is required for specific developmental processes.

Original languageEnglish (US)
Pages (from-to)14727-14731
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume105
Issue number38
DOIs
StatePublished - Sep 23 2008
Externally publishedYes

Fingerprint

Hydro-Lyases
Acyl Coenzyme A
Plant Development
Fatty Acids
Sphingolipids
Arabidopsis
Endoplasmic Reticulum
Enzymes
Fatty Acid Desaturases
Multiprotein Complexes
Cytokinesis
Waxes
Seeds
Triglycerides
Homeostasis
Embryonic Structures
Yeasts
Fluorescence
Genes

Keywords

  • Cuticular wax
  • Elongase
  • Leaf development
  • Sphingolipid
  • Triacylglycerol

ASJC Scopus subject areas

  • General

Cite this

The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. / Bach, Liên; Michaelson, Louise V.; Haslam, Richard; Bellec, Yannick; Gissot, Lionel; Marion, Jessica; Da Costa, Marco; Boutin, Jean Pierre; Miquel, Martine; Tellier, Frédérique; Domergue, Frederic; Markham, Jonathan E; Beaudoin, Frederic; Napier, Johnathan A.; Faure, Jean Denis.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 105, No. 38, 23.09.2008, p. 14727-14731.

Research output: Contribution to journalArticle

Bach, L, Michaelson, LV, Haslam, R, Bellec, Y, Gissot, L, Marion, J, Da Costa, M, Boutin, JP, Miquel, M, Tellier, F, Domergue, F, Markham, JE, Beaudoin, F, Napier, JA & Faure, JD 2008, 'The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development', Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 38, pp. 14727-14731. https://doi.org/10.1073/pnas.0805089105
Bach, Liên ; Michaelson, Louise V. ; Haslam, Richard ; Bellec, Yannick ; Gissot, Lionel ; Marion, Jessica ; Da Costa, Marco ; Boutin, Jean Pierre ; Miquel, Martine ; Tellier, Frédérique ; Domergue, Frederic ; Markham, Jonathan E ; Beaudoin, Frederic ; Napier, Johnathan A. ; Faure, Jean Denis. / The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. In: Proceedings of the National Academy of Sciences of the United States of America. 2008 ; Vol. 105, No. 38. pp. 14727-14731.
@article{895c15b98c5e4367b55c62de7706ae53,
title = "The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development",
abstract = "Very-long-chain fatty acids (VLCFAs) are synthesized as acyl-CoAs by the endoplasmic reticulum-localized elongase multiprotein complex. Two Arabidopsis genes are putative homologues of the recently identified yeast 3-hydroxy-acyl-CoA dehydratase (PHS1), the third enzyme of the elongase complex. We showed that Arabidopsis PASTICCINO2 (PAS2) was able to restore phs1 cytokinesis defects and sphingolipid long chain base overaccumulation. Conversely, the expression of PHS1 was able to complement the developmental defects and the accumulation of long chain bases of the pas2-1 mutant. The pas2-1 mutant was characterized by a general reduction of VLCFA pools in seed storage triacylglycerols, cuticular waxes, and complex sphingolipids. Most strikingly, the defective elongation cycle resulted in the accumulation of 3-hydroxy-acyl-CoA intermediates, indicating premature termination of fatty acid elongation and confirming the role of PAS2 in this process. We demonstrated by in vivo bimolecular fluorescence complementation that PAS2 was specifically associated in the endoplasmic reticulum with the enoyl-CoA reductase CER10, the fourth enzyme of the elongase complex. Finally, complete loss of PAS2 function is embryo lethal, and the ectopic expression of PHS1 led to enhanced levels of VLCFAs associated with severe developmental defects. Altogether these results demonstrate that the plant 3-hydroxy-acyl-CoA dehydratase PASTICCINO2 is an essential and limiting enzyme in VLCFA synthesis but also that PAS2-derived VLCFA homeostasis is required for specific developmental processes.",
keywords = "Cuticular wax, Elongase, Leaf development, Sphingolipid, Triacylglycerol",
author = "Li{\^e}n Bach and Michaelson, {Louise V.} and Richard Haslam and Yannick Bellec and Lionel Gissot and Jessica Marion and {Da Costa}, Marco and Boutin, {Jean Pierre} and Martine Miquel and Fr{\'e}d{\'e}rique Tellier and Frederic Domergue and Markham, {Jonathan E} and Frederic Beaudoin and Napier, {Johnathan A.} and Faure, {Jean Denis}",
year = "2008",
month = "9",
day = "23",
doi = "10.1073/pnas.0805089105",
language = "English (US)",
volume = "105",
pages = "14727--14731",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "38",

}

TY - JOUR

T1 - The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development

AU - Bach, Liên

AU - Michaelson, Louise V.

AU - Haslam, Richard

AU - Bellec, Yannick

AU - Gissot, Lionel

AU - Marion, Jessica

AU - Da Costa, Marco

AU - Boutin, Jean Pierre

AU - Miquel, Martine

AU - Tellier, Frédérique

AU - Domergue, Frederic

AU - Markham, Jonathan E

AU - Beaudoin, Frederic

AU - Napier, Johnathan A.

AU - Faure, Jean Denis

PY - 2008/9/23

Y1 - 2008/9/23

N2 - Very-long-chain fatty acids (VLCFAs) are synthesized as acyl-CoAs by the endoplasmic reticulum-localized elongase multiprotein complex. Two Arabidopsis genes are putative homologues of the recently identified yeast 3-hydroxy-acyl-CoA dehydratase (PHS1), the third enzyme of the elongase complex. We showed that Arabidopsis PASTICCINO2 (PAS2) was able to restore phs1 cytokinesis defects and sphingolipid long chain base overaccumulation. Conversely, the expression of PHS1 was able to complement the developmental defects and the accumulation of long chain bases of the pas2-1 mutant. The pas2-1 mutant was characterized by a general reduction of VLCFA pools in seed storage triacylglycerols, cuticular waxes, and complex sphingolipids. Most strikingly, the defective elongation cycle resulted in the accumulation of 3-hydroxy-acyl-CoA intermediates, indicating premature termination of fatty acid elongation and confirming the role of PAS2 in this process. We demonstrated by in vivo bimolecular fluorescence complementation that PAS2 was specifically associated in the endoplasmic reticulum with the enoyl-CoA reductase CER10, the fourth enzyme of the elongase complex. Finally, complete loss of PAS2 function is embryo lethal, and the ectopic expression of PHS1 led to enhanced levels of VLCFAs associated with severe developmental defects. Altogether these results demonstrate that the plant 3-hydroxy-acyl-CoA dehydratase PASTICCINO2 is an essential and limiting enzyme in VLCFA synthesis but also that PAS2-derived VLCFA homeostasis is required for specific developmental processes.

AB - Very-long-chain fatty acids (VLCFAs) are synthesized as acyl-CoAs by the endoplasmic reticulum-localized elongase multiprotein complex. Two Arabidopsis genes are putative homologues of the recently identified yeast 3-hydroxy-acyl-CoA dehydratase (PHS1), the third enzyme of the elongase complex. We showed that Arabidopsis PASTICCINO2 (PAS2) was able to restore phs1 cytokinesis defects and sphingolipid long chain base overaccumulation. Conversely, the expression of PHS1 was able to complement the developmental defects and the accumulation of long chain bases of the pas2-1 mutant. The pas2-1 mutant was characterized by a general reduction of VLCFA pools in seed storage triacylglycerols, cuticular waxes, and complex sphingolipids. Most strikingly, the defective elongation cycle resulted in the accumulation of 3-hydroxy-acyl-CoA intermediates, indicating premature termination of fatty acid elongation and confirming the role of PAS2 in this process. We demonstrated by in vivo bimolecular fluorescence complementation that PAS2 was specifically associated in the endoplasmic reticulum with the enoyl-CoA reductase CER10, the fourth enzyme of the elongase complex. Finally, complete loss of PAS2 function is embryo lethal, and the ectopic expression of PHS1 led to enhanced levels of VLCFAs associated with severe developmental defects. Altogether these results demonstrate that the plant 3-hydroxy-acyl-CoA dehydratase PASTICCINO2 is an essential and limiting enzyme in VLCFA synthesis but also that PAS2-derived VLCFA homeostasis is required for specific developmental processes.

KW - Cuticular wax

KW - Elongase

KW - Leaf development

KW - Sphingolipid

KW - Triacylglycerol

UR - http://www.scopus.com/inward/record.url?scp=55749095402&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=55749095402&partnerID=8YFLogxK

U2 - 10.1073/pnas.0805089105

DO - 10.1073/pnas.0805089105

M3 - Article

VL - 105

SP - 14727

EP - 14731

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 38

ER -