Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis
Abstract
Glycosylinositol phosphorylceramides (GIPCs) are a class of glycosylated sphingolipids found in plants, fungi, and protozoa. These lipids are abundant in the plant plasma membrane, forming ~25% of total plasma membrane lipids. Little is known about the function of the glycosylated headgroup, but two recent studies have indicated that they play a key role in plant signaling and defense. Here, we show that a member of glycosyltransferase family 64, previously named ECTOPICALLY PARTING CELLS1, is likely a Golgi-localized GIPC-specific mannosyl-transferase, which we renamed GIPC MANNOSYL-TRANSFERASE1 (GMT1). Sphingolipid analysis revealed that the Arabidopsis thaliana gmt1 mutant almost completely lacks mannose-carrying GIPCs. Heterologous expression of GMT1 in Saccharomyces cerevisiae and tobacco (Nicotiana tabacum) cv Bright Yellow 2 resulted in the production of non-native mannosylated GIPCs. gmt1 displays a severe dwarfed phenotype and a constitutive hypersensitive response characterized by elevated salicylic acid and hydrogen peroxide levels, similar to that we previously reported for the Golgi-localized, GIPC-specific, GDP-Man transporter GONST1 (Mortimer et al., 2013). Unexpectedly, we show that gmt1 cell walls have a reduction in cellulose content, although other matrix polysaccharides are unchanged.
- Authors:
-
- Joint BioEnergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
- Saitama Univ. (Japan). Graduate School of Science and Engineering
- Univ. of California, Berkeley, CA (United States). Dept. of Chemical and Biomolecular Engineering
- Joint BioEnergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemical and Biomolecular Engineering
- RIKEN, Yokohama (Japan). Center for Sustainable Resource Science, Biomass Engineering Program; Nara Inst. of Science and Technology, Nara (Japan). Graduate School of Biological Sciences
- Joint BioEnergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1379600
- DOE Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article
- Journal Name:
- Plant Cell
- Additional Journal Information:
- Journal Volume: 28; Journal Issue: 12; Journal ID: ISSN 1040-4651
- Publisher:
- American Society of Plant Biologists
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Fang, Lin, Ishikawa, Toshiki, Rennie, Emilie A., Murawska, Gosia M., Lao, Jeemeng, Yan, Jingwei, Tsai, Alex Yi-Lin, Baidoo, Edward E. K., Xu, Jun, Keasling, Jay D., Demura, Taku, Kawai-Yamada, Maki, Scheller, Henrik V., and Mortimer, Jenny C. Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis. United States: N. p., 2016.
Web. doi:10.1105/tpc.16.00186.
Fang, Lin, Ishikawa, Toshiki, Rennie, Emilie A., Murawska, Gosia M., Lao, Jeemeng, Yan, Jingwei, Tsai, Alex Yi-Lin, Baidoo, Edward E. K., Xu, Jun, Keasling, Jay D., Demura, Taku, Kawai-Yamada, Maki, Scheller, Henrik V., & Mortimer, Jenny C. Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis. United States. https://doi.org/10.1105/tpc.16.00186
Fang, Lin, Ishikawa, Toshiki, Rennie, Emilie A., Murawska, Gosia M., Lao, Jeemeng, Yan, Jingwei, Tsai, Alex Yi-Lin, Baidoo, Edward E. K., Xu, Jun, Keasling, Jay D., Demura, Taku, Kawai-Yamada, Maki, Scheller, Henrik V., and Mortimer, Jenny C. 2016.
"Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis". United States. https://doi.org/10.1105/tpc.16.00186. https://www.osti.gov/servlets/purl/1379600.
@article{osti_1379600,
title = {Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis},
author = {Fang, Lin and Ishikawa, Toshiki and Rennie, Emilie A. and Murawska, Gosia M. and Lao, Jeemeng and Yan, Jingwei and Tsai, Alex Yi-Lin and Baidoo, Edward E. K. and Xu, Jun and Keasling, Jay D. and Demura, Taku and Kawai-Yamada, Maki and Scheller, Henrik V. and Mortimer, Jenny C.},
abstractNote = {Glycosylinositol phosphorylceramides (GIPCs) are a class of glycosylated sphingolipids found in plants, fungi, and protozoa. These lipids are abundant in the plant plasma membrane, forming ~25% of total plasma membrane lipids. Little is known about the function of the glycosylated headgroup, but two recent studies have indicated that they play a key role in plant signaling and defense. Here, we show that a member of glycosyltransferase family 64, previously named ECTOPICALLY PARTING CELLS1, is likely a Golgi-localized GIPC-specific mannosyl-transferase, which we renamed GIPC MANNOSYL-TRANSFERASE1 (GMT1). Sphingolipid analysis revealed that the Arabidopsis thaliana gmt1 mutant almost completely lacks mannose-carrying GIPCs. Heterologous expression of GMT1 in Saccharomyces cerevisiae and tobacco (Nicotiana tabacum) cv Bright Yellow 2 resulted in the production of non-native mannosylated GIPCs. gmt1 displays a severe dwarfed phenotype and a constitutive hypersensitive response characterized by elevated salicylic acid and hydrogen peroxide levels, similar to that we previously reported for the Golgi-localized, GIPC-specific, GDP-Man transporter GONST1 (Mortimer et al., 2013). Unexpectedly, we show that gmt1 cell walls have a reduction in cellulose content, although other matrix polysaccharides are unchanged.},
doi = {10.1105/tpc.16.00186},
url = {https://www.osti.gov/biblio/1379600},
journal = {Plant Cell},
issn = {1040-4651},
number = 12,
volume = 28,
place = {United States},
year = {Mon Nov 28 00:00:00 EST 2016},
month = {Mon Nov 28 00:00:00 EST 2016}
}
Works referenced in this record:
Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis
journal, January 2017
- Tartaglio, Virginia; Rennie, Emilie A.; Cahoon, Rebecca
- The Plant Journal, Vol. 89, Issue 2
Molecular characterization and targeted quantitative profiling of the sphingolipidome in rice
journal, September 2016
- Ishikawa, Toshiki; Ito, Yukihiro; Kawai-Yamada, Maki
- The Plant Journal, Vol. 88, Issue 4