Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes

Nagano, Minoru; Ishikawa, Toshiki; Ogawa, Yoshiaki; Iwabuchi, Mitsuru; Nakasone, Akari; Shimamoto, Ko; Uchimiya, Hirofumi; Kawai‐Yamada, Maki

doi:10.1007/s00425-014-2065-7

Cited by 48 publications

(27 citation statements)

References 56 publications

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“…Thus, BI-1 and FAH seem to coordinate the maintenance of 2-hydroxylation of sphingolipids in the context of defense responses to oxidative stress. Furthermore, it was recently shown that Arabidopsis BI-1 interacts with other sphingolipidmodifying enzymes and is involved in sphingolipid metabolism under cold stress (Nagano et al, 2014). In this study, we confirmed that AtBI-1 overexpression resulted in the accumulation of both the predominant 2-hydroxy VLCFA species, 20h:0, and the total amount of GlcCer (Fig.…”

Section: Discussionsupporting

confidence: 86%

Overexpression of BAX INHIBITOR-1 Links Plasma Membrane Microdomain Proteins to Stress

et al. 2015

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BAX INHIBITOR-1 (BI-1) is a cell death suppressor widely conserved in plants and animals. Overexpression of BI-1 enhances tolerance to stress-induced cell death in plant cells, although the molecular mechanism behind this enhancement is unclear. We recently found that Arabidopsis (Arabidopsis thaliana) BI-1 is involved in the metabolism of sphingolipids, such as the synthesis of 2-hydroxy fatty acids, suggesting the involvement of sphingolipids in the cell death regulatory mechanism downstream of BI-1. Here, we show that BI-1 affects cell death-associated components localized in sphingolipid-enriched microdomains of the plasma membrane in rice (Oryza sativa) cells. The amount of 2-hydroxy fatty acid-containing glucosylceramide increased in the detergent-resistant membrane (DRM; a biochemical counterpart of plasma membrane microdomains) fraction obtained from BI-1-overexpressing rice cells. Comparative proteomics analysis showed quantitative changes of DRM proteins in BI-1-overexpressing cells. In particular, the protein abundance of FLOTILLIN HOMOLOG (FLOT) and HYPERSENSITIVE-INDUCED REACTION PROTEIN3 (HIR3) markedly decreased in DRM of BI-1-overexpressing cells. Loss-of-function analysis demonstrated that FLOT and HIR3 are required for cell death by oxidative stress and salicylic acid, suggesting that the decreased levels of these proteins directly contribute to the stress-tolerant phenotypes in BI-1-overexpressing rice cells. These findings provide a novel biological implication of plant membrane microdomains in stress-induced cell death, which is negatively modulated by BI-1 overexpression via decreasing the abundance of a set of key proteins involved in cell death.

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Section: Discussionsupporting

confidence: 86%

Overexpression of BAX INHIBITOR-1 Links Plasma Membrane Microdomain Proteins to Stress

et al. 2015

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“…Analytical conditions described for Arabidopsis thaliana by Markham and Jaworski (2007) and Nagano et al (2014) were optimized for rice sphingolipid species. Chromatographic separation was performed using an XR-ODSII column (Shimadzu; 2.2 mm, 2.0 mm ID, 75 mm) held at 40°C with binary elution gradients consisting of THF/methanol/10 mM ammonium formate (3:2:5) containing 0.1% (v/v) formic acid as solvent A and THF/methanol/10 mM ammonium formate (7:2:1) containing 0.1% (v/v) formic acid as solvent B at a flow rate of 200 mL/min.…”

Section: Lc-ms/ms Analysis Of Sphingolipids and Sterolsmentioning

confidence: 99%

Plasma Membrane Microdomains Are Essential for Rac1-RbohB/H-Mediated Immunity in Rice

et al. 2016

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Numerous plant defense-related proteins are thought to congregate in plasma membrane microdomains, which consist mainly of sphingolipids and sterols. However, the extent to which microdomains contribute to defense responses in plants is unclear. To elucidate the relationship between microdomains and innate immunity in rice (Oryza sativa), we established lines in which the levels of sphingolipids containing 2-hydroxy fatty acids were decreased by knocking down two genes encoding fatty acid 2-hydroxylases (FAH1 and FAH2) and demonstrated that microdomains were less abundant in these lines. By testing these lines in a pathogen infection assay, we revealed that microdomains play an important role in the resistance to rice blast fungus infection. To illuminate the mechanism by which microdomains regulate immunity, we evaluated changes in protein composition, revealing that microdomains are required for the dynamics of the Rac/ROP small GTPase Rac1 and respiratory burst oxidase homologs (Rbohs) in response to chitin elicitor. Furthermore, FAHs are essential for the production of reactive oxygen species (ROS) after chitin treatment. Together with the observation that RbohB, a defense-related NADPH oxidase that interacts with Rac1, is localized in microdomains, our data indicate that microdomains are required for chitin-induced immunity through ROS signaling mediated by the Rac1-RbohB pathway.

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“…Total sphingolipids including GIPCs were prepared from calli of the wildtype plant and kjc1-1 and kjc2-1 mutants and analyzed by LC-MS/MS as described (Nagano et al, 2014). Peaks of GIPCs with different hexose numbers (Hex 0 , Hex 1 , and Hex 2 ) were assigned based on multiple reaction monitoring transitions (Mortimer et al, 2013).…”

Section: Gipc Analysismentioning

confidence: 99%

KONJAC1 and 2 Are Key Factors for GDP-Mannose Generation and Affect l-Ascorbic Acid and Glucomannan Biosynthesis in Arabidopsis

et al. 2015

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Humans are unable to synthesize L-ascorbic acid (AsA), yet it is required as a cofactor in many critical biochemical reactions. The majority of human dietary AsA is obtained from plants. In Arabidopsis thaliana, a GDP-mannose pyrophosphorylase (GMPP), VITAMIN C DEFECTIVE1 (VTC1), catalyzes a rate-limiting step in AsA synthesis: the formation of GDP-Man. In this study, we identified two nucleotide sugar pyrophosphorylase-like proteins, KONJAC1 (KJC1) and KJC2, which stimulate the activity of VTC1. The kjc1kjc2 double mutant exhibited severe dwarfism, indicating that KJC proteins are important for growth and development. The kjc1 mutation reduced GMPP activity to 10% of wild-type levels, leading to a 60% reduction in AsA levels. On the contrary, overexpression of KJC1 significantly increased GMPP activity. The kjc1 and kjc1kjc2 mutants also exhibited significantly reduced levels of glucomannan, which is also synthesized from GDP-Man. Recombinant KJC1 and KJC2 enhanced the GMPP activity of recombinant VTC1 in vitro, while KJCs did not show GMPP activity. Yeast two-hybrid assays suggested that the stimulation of GMPP activity occurs via interaction of KJCs with VTC1. These results suggest that KJCs are key factors for the generation of GDP-Man and affect AsA level and glucomannan accumulation through the stimulation of VTC1 GMPP activity.

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Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes

Cited by 48 publications

References 56 publications

Overexpression of BAX INHIBITOR-1 Links Plasma Membrane Microdomain Proteins to Stress

Overexpression of BAX INHIBITOR-1 Links Plasma Membrane Microdomain Proteins to Stress

Plasma Membrane Microdomains Are Essential for Rac1-RbohB/H-Mediated Immunity in Rice

KONJAC1 and 2 Are Key Factors for GDP-Mannose Generation and Affect l-Ascorbic Acid and Glucomannan Biosynthesis in Arabidopsis

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