Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis

Virginia Tartaglio, Emilie A. Rennie, Rebecca Cahoon, George Wang, Edward Baidoo, Jennifer C. Mortimer, Edgar B. Cahoon, Henrik V. Scheller

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Sphingolipids are a major component of plant plasma membranes and endomembranes, and mediate a diverse range of biological processes. Study of the highly glycosylated glycosyl inositol phosphorylceramide (GIPC) sphingolipids has been slow as a result of challenges associated with the extractability of GIPCs, and their functions in the plant remain poorly characterized. We recently discovered an Arabidopsis GIPC glucuronosyltransferase, INOSITOL PHOSPHORYLCERAMIDE GLUCURONOSYLTRANSFERASE 1 (IPUT1), which is the first enzyme in the GIPC glycosylation pathway. Plants homozygous for the iput1 loss-of-function mutation were unobtainable, and so the developmental effects of reduced GIPC glucuronosylation could not be analyzed in planta. Using a pollen-specific rescue construct, we have here isolated homozygous iput1 mutants. The iput1 mutants show severe dwarfism, compromised pollen tube guidance, and constitutive activation of salicyclic acid-mediated defense pathways. The mutants also possess reduced GIPCs, increased ceramides, and an increased incorporation of short-chain fatty acids and dihydroxylated bases into inositol phosphorylceramides and GIPCs. The assignment of a direct role for GIPC glycan head groups in the impaired processes in iput1 mutants is complicated by the vast compensatory changes in the sphingolipidome; however, our results reveal that the glycosylation steps of GIPC biosynthesis are important regulated components of sphingolipid metabolism. This study corroborates previously suggested roles for GIPC glycans in plant growth and defense, suggests important roles for them in reproduction and demonstrates that the entire sphingolipidome is sensitive to their status.

Original languageEnglish (US)
Pages (from-to)278-290
Number of pages13
JournalPlant Journal
Volume89
Issue number2
DOIs
StatePublished - Jan 1 2017

Fingerprint

sphingolipids
Sphingolipids
Inositol
glycosylation
Glycosylation
Arabidopsis
Reproduction
Growth
mutants
Pollen Tube
Biological Phenomena
Plant Structures
Dwarfism
Glucuronosyltransferase
polysaccharides
Volatile Fatty Acids
Ceramides
group process
Pollen
inositols

Keywords

  • Arabidopsis thaliana
  • IPUT1
  • glucuronosyltransferase
  • glycosyl inositol phosphorylceramides
  • pollen tube growth
  • sphingolipid

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Tartaglio, V., Rennie, E. A., Cahoon, R., Wang, G., Baidoo, E., Mortimer, J. C., ... Scheller, H. V. (2017). Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis. Plant Journal, 89(2), 278-290. https://doi.org/10.1111/tpj.13382

Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis. / Tartaglio, Virginia; Rennie, Emilie A.; Cahoon, Rebecca; Wang, George; Baidoo, Edward; Mortimer, Jennifer C.; Cahoon, Edgar B.; Scheller, Henrik V.

In: Plant Journal, Vol. 89, No. 2, 01.01.2017, p. 278-290.

Research output: Contribution to journalArticle

Tartaglio, V, Rennie, EA, Cahoon, R, Wang, G, Baidoo, E, Mortimer, JC, Cahoon, EB & Scheller, HV 2017, 'Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis', Plant Journal, vol. 89, no. 2, pp. 278-290. https://doi.org/10.1111/tpj.13382
Tartaglio, Virginia ; Rennie, Emilie A. ; Cahoon, Rebecca ; Wang, George ; Baidoo, Edward ; Mortimer, Jennifer C. ; Cahoon, Edgar B. ; Scheller, Henrik V. / Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis. In: Plant Journal. 2017 ; Vol. 89, No. 2. pp. 278-290.
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