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Title: Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis

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:
ORCiD logo [1] ;  [2] ;  [1] ; ORCiD logo [1] ;  [1] ;  [1] ;  [1] ;  [1] ; ORCiD logo [3] ; ORCiD logo [4] ;  [5] ;  [2] ; ORCiD logo [6] ; ORCiD logo [4]
  1. Joint BioEnergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
  2. Saitama Univ. (Japan). Graduate School of Science and Engineering
  3. Univ. of California, Berkeley, CA (United States). Dept. of Chemical and Biomolecular Engineering
  4. 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
  5. RIKEN, Yokohama (Japan). Center for Sustainable Resource Science, Biomass Engineering Program; Nara Inst. of Science and Technology, Nara (Japan). Graduate School of Biological Sciences
  6. 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:
Grant/Contract Number:
AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Plant Cell
Additional Journal Information:
Journal Volume: 28; Journal Issue: 12; Journal ID: ISSN 1040-4651
Publisher:
American Society of Plant Biologists
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES
OSTI Identifier:
1379600

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., 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. 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., and Mortimer, Jenny C.. 2016. "Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis". United States. doi: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},
journal = {Plant Cell},
number = 12,
volume = 28,
place = {United States},
year = {2016},
month = {11}
}