Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis

Joseph Msanne, Ming Chen, Kyle D. Luttgeharm, Amanda M. Bradley, Elizabeth S. Mays, Janet M. Paper, Daniel L. Boyle, Rebecca E. Cahoon, Kathrin Schrick, Edgar B Cahoon

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Glucosylceramides (GlcCer), glucose-conjugated sphingolipids, are major components of the endomembrane system and plasma membrane in most eukaryotic cells. Yet the quantitative significance and cellular functions of GlcCer are not well characterized in plants and other multi-organ eukaryotes. To address this, we examined Arabidopsis lines that were lacking or deficient in GlcCer by insertional disruption or by RNA interference (RNAi) suppression of the single gene for GlcCer synthase (GCS, At2g19880), the enzyme that catalyzes GlcCer synthesis. Null mutants for GCS (designated 'gcs-1') were viable as seedlings, albeit strongly reduced in size, and failed to develop beyond the seedling stage. Heterozygous plants harboring the insertion allele exhibited reduced transmission through the male gametophyte. Undifferentiated calli generated from gcs-1 seedlings and lacking GlcCer proliferated in a manner similar to calli from wild-type plants. However, gcs-1 calli, in contrast to wild-type calli, were unable to develop organs on differentiation media. Consistent with a role for GlcCer in organ-specific cell differentiation, calli from gcs-1 mutants formed roots and leaves on media supplemented with the glucosylated sphingosine glucopsychosine, which was readily converted to GlcCer independent of GCS. Underlying these phenotypes, gcs-1 cells had altered Golgi morphology and fewer cisternae per Golgi apparatus relative to wild-type cells, indicative of protein trafficking defects. Despite seedling lethality in the null mutant, GCS RNAi suppression lines with ≤2% of wild-type GlcCer levels were viable and fertile. Collectively, these results indicate that GlcCer are essential for cell-type differentiation and organogenesis, and plant cells produce amounts of GlcCer in excess of that required for normal development.

Original languageEnglish (US)
Pages (from-to)188-201
Number of pages14
JournalPlant Journal
Volume84
Issue number1
DOIs
StatePublished - Oct 1 2015

Fingerprint

Glucosylceramides
Organogenesis
organogenesis
Arabidopsis
cell viability
Cell Differentiation
Cell Survival
callus
Bony Callus
seedlings
RNA interference
Seedlings
mutants
cells
eukaryotic cells
endomembrane system
sphingosine
sphingolipids
protein transport
ceramide glucosyltransferase

Keywords

  • Arabidopsis
  • ceramide
  • differentiation
  • glucosylceramide
  • Glucosylceramide synthase
  • sphingolipids

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology
  • Genetics

Cite this

Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis. / Msanne, Joseph; Chen, Ming; Luttgeharm, Kyle D.; Bradley, Amanda M.; Mays, Elizabeth S.; Paper, Janet M.; Boyle, Daniel L.; Cahoon, Rebecca E.; Schrick, Kathrin; Cahoon, Edgar B.

In: Plant Journal, Vol. 84, No. 1, 01.10.2015, p. 188-201.

Research output: Contribution to journalArticle

Msanne, J, Chen, M, Luttgeharm, KD, Bradley, AM, Mays, ES, Paper, JM, Boyle, DL, Cahoon, RE, Schrick, K & Cahoon, EB 2015, 'Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis', Plant Journal, vol. 84, no. 1, pp. 188-201. https://doi.org/10.1111/tpj.13000
Msanne, Joseph ; Chen, Ming ; Luttgeharm, Kyle D. ; Bradley, Amanda M. ; Mays, Elizabeth S. ; Paper, Janet M. ; Boyle, Daniel L. ; Cahoon, Rebecca E. ; Schrick, Kathrin ; Cahoon, Edgar B. / Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis. In: Plant Journal. 2015 ; Vol. 84, No. 1. pp. 188-201.
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