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Journal of Plant Research

, Volume 132, Issue 1, pp 131–143 | Cite as

Arabidopsis Bax inhibitor-1 interacts with enzymes related to very-long-chain fatty acid synthesis

  • Minoru NaganoEmail author
  • Chikako Kakuta
  • Yoichiro Fukao
  • Masayuki Fujiwara
  • Hirofumi Uchimiya
  • Maki Kawai-Yamada
Regular Paper
  • 171 Downloads

Abstract

Bax inhibitor-1 (BI-1) is a widely conserved cell death regulator that confers resistance to environmental stress in plants. Previous studies suggest that Arabidopsis thaliana BI-1 (AtBI-1) modifies sphingolipids by interacting with cytochrome b5 (AtCb5), an electron-transfer protein. To reveal how AtBI-1 regulates sphingolipid synthesis, we screened yeast sphingolipid-deficient mutants and identified yeast ELO2 and ELO3 as novel enzymes that are essential for AtBI-1 function. ELO2 and ELO3 are condensing enzymes that synthesize very-long-chain fatty acids (VLCFAs), major fatty acids in plant sphingolipids. In Arabidopsis, we identified four ELO homologs (AtELO1–AtELO4), localized in the endoplasmic reticulum membrane. Of those AtELOs, AtELO1 and AtELO2 had a characteristic histidine motif and were bound to AtCb5-B. This result suggests that AtBI-1 interacts with AtELO1 and AtELO2 through AtCb5. AtELO2 and AtCb5-B also interact with KCR1, PAS2, and CER10, which are essential for the synthesis of VLCFAs. Therefore, AtELO2 may participate in VLCFA synthesis with AtCb5 in Arabidopsis. In addition, our co-immunoprecipitation/mass spectrometry analysis demonstrated that AtBI-1 forms a complex with AtELO2, KCR1, PAS2, CER10, and AtCb5-D. Furthermore, AtBI-1 contributes to the rapid synthesis of 2-hydroxylated VLCFAs in response to oxidative stress. These results indicate that AtBI-1 regulates VLCFA synthesis by interacting with VLCFA-synthesizing enzymes.

Keywords

Bax inhibitor-1 Oxidative stress Sphingolipid Very-long-chain fatty acid 

Notes

Acknowledgements

Plasmids and strains used for cell death assays in yeast were kindly provided by Dr. John C. Reed (The Burnham Institute, La Jolla, CA). Plasmids and strains used for the suY2H system were generously provided by Dr. Ralph Panstruga (Max-Planck Institute, Saabruecken, Germany) and Dr. Imre E. Somssich (Max-Planck Institute). Plasmids used for the BiFC assay were kindly provided by Dr. Tsuyoshi Nakagawa (Shimane University, Japan). We appreciate Dr. Noriko Inada (Nara Institute of Science and Technology, Japan) for technical advice of confocal laser microscopy and FRET analysis. This research was supported by a Grant-in-Aid for Japan Society for the Promotion of Science (JSPS) Fellows Grant Numbers 07J03838 and 11J08349 to M. N.; a Grant in-Aid to C. K. for Scientific Research for Plant Graduate Student from Nara Institute Science and Technology; JSPS KAKENHI Grant Numbers 26850232 and 17K15412 to M. N; 26292190 to M. K-Y..

Supplementary material

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Supplementary material 1 (PDF 1178 KB)

References

  1. Bach L, Faure JD (2010) Role of very-long-chain fatty acids in plant development, when chain length does matter. C R Biol 333:361–370Google Scholar
  2. De BDA Granrut, Cacas JL (2016) How very-long-chain fatty acids could signal stressful conditions in plants? Front Plant Sci 7:1490Google Scholar
  3. Denic V, Weissman JS (2007) A molecular caliper mechanism for determining very long-chain fatty acid length. Cell 130:663–677Google Scholar
  4. Dickson RC, Lester RL (2002) Sphingolipid functions in Saccharomyces cerevisiae. Biochim Biophys Acta 1583:13–25Google Scholar
  5. Dickson RC, Sumanasekera C, Lester RL (2006) Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45:447–465Google Scholar
  6. Earley KW, Haag JR, Ontes O, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629Google Scholar
  7. Eiamsa-Ard P, Kanjana-Opas A, Cahoon EB, Chodok P, Kaewsuwan S (2013) Two novel Physcomitrella patens fatty acid elongases (ELOs): identification and functional characterization. Appl Microbiol Biotechnol 97:3485–3497Google Scholar
  8. Eichmann R, Schultheiss H, Kogel KH, Huckelhoven R (2004) The barley apoptosis suppressor homologue BAX inhibitor-1compromises nonhost penetration resistance of barley to the inappropriate pathogen Blumeria graminis f. sp. tritici. Mol Plant Microbe Interact 17:484–490Google Scholar
  9. Fox BG, Shanklin J, Somerville C, Munck E (1993) Stearoyl-acyl carrier protein delta 9 desaturase from Ricinus communis is a diiron-oxo protein. Proc Natl Acad Sci USA 90:2486–2490Google Scholar
  10. Haslam TM, Kunst L (2013) Extending the story of very-long-chain fatty acid elongation. Plant Sci 210:93–107Google Scholar
  11. Ihara-Ohori Y, Nagano M, Muto S, Uchimiya H, Kawai-Yamada M (2007) Cell death suppressor, Arabidopsis BI-1, is associated with calmodulin-binding and ion homeostasis. Plant Physiol 143:650–660Google Scholar
  12. Imai H, Yamamoto K, Shibahara A, Miyatani S, Nakayama T (2000) Determining double-bond positions in monenoic 2-hydroxy fatty acids of glucosylceramides by gas chromatography-mass spectrometry. Lipids 35:233–236Google Scholar
  13. Imari J, Baltruschat H, Stein E, Jia G, Vogelsberg J, Kogel KH, Huckelhoven R (2006) Expression of barley BAX Inhibitor-1 in carrots confers resistance to Botrytis cinerea. Mol Plant Pathol 7:279–284Google Scholar
  14. Isbat M, Zeba N, Kim SR, Hong CB (2009) A Bax inhibitor-1 gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. Plant Physiol 166:1685–1693Google Scholar
  15. Ishikawa T, Takahara K, Hirabayashi T, Matsumura H, Fujisawa S, Terauchi R, Uchimiya H, Kawai-Yamada M (2010) Metabolome analysis of response to oxidative stress in rice suspension cells overexpressing cell death suppressor Bax inhibitor-1. Plant Cell Physiol 51:9–20Google Scholar
  16. Ishikawa T, Watanabe N, Nagano M, Kawai-Yamada M, Lam E (2011) Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor. Cell Death Differ 18:1271–1278Google Scholar
  17. Ishikawa T, Aki T, Yanagisawa S, Uchimiya H, Kawai-Yamada M (2015) Overexpression of BAX INHIBITOR-1 lings plasma membrane microdomain proteins to stress. Plant Physiol 169:1333–1343Google Scholar
  18. Joubes J, Raffaele S, Bourdenx B, Garcia C, Laroche-Traineau J, Moreau P, Domergue F, Lessire R (2008) The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modelling and expression profiling. Plant Mol Biol 67:547–566Google Scholar
  19. Kajikawa M, Yamaoka S, Yamato KT, Kanamaru H, Sakuradani E, Shimizu S, Fukuzawa H, Sakai Y, Ohyama K (2003a) Functional analysis of a beta-ketoacyl-CoA synthase gene MpFAE2, by gene silencing in the liverwort Marchantia polymorpha L. Biosci Biotechnol Biochem 67:605–612Google Scholar
  20. Kajikawa M, Yamato KT, Kanamaru H, Sakuradani E, Shimizu S, Fukuzawa H, Sakai Y, Ohyama K (2003b) MpFAE3, a beta-ketoacyl-CoA synthase gene in the liverwort Marchantia polymorpha L., is preferentially involved in elongation of palmitic acid to stearic acid. Biosci Biotechnol Biochem 67:1667–1674Google Scholar
  21. Kajikawa M, Yamato KT, Kohzu Y, Nojiri M, Sakuradani E, Shimizu S, Sakai Y, Fukuzawa H, Ohyama K (2004) Isolation and characterization of delta(6)-desaturase, an ELO-like enzyme and delta(5)-desaturase form the liverwort Marchantia polymorpha and production of arachidonic and eicosapentaenoic acids in the methylotraphic yeast Pichia pastoris. Plant Mol Biol 54:335–352Google Scholar
  22. Kajikawa M, Yamato KT, Sakai Y, Fukuzawa H, Ohyama K, Kohchi T (2006) Isolation and functional characterization of fatty acid delta5-elongase gene form the liverwort Marchantia polymorpha L. FEBS lett 580:149–154Google Scholar
  23. Kawai M, Pan L, Reed JC, Uchimiya H (1999) Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett 31:143–147Google Scholar
  24. Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300Google Scholar
  25. Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax Inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16:21–32Google Scholar
  26. Kawai-Yamada M, Hori Z, Ihara-Ohori Y, Tamura K, Nagano M, Ishikawa T, Uchimiya H (2009) Loss of calmodulin binding to Bax inhibitor-1 affects Pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana. J Biol Chem 28:27998–28003Google Scholar
  27. Kim J, Jung JH, Lee SB, Go YS, Kim HJ, Cahoon R, Markham JE, Cahoon EB, Suh MC (2013) Involved in the synthesis of tetracosanoic acids as precursors of cuticular waxes, suberins, sphingolipids, and phospholipids. Plant Phhysiol 162:567–580Google Scholar
  28. Leonard AE, Pereira SL, Sprecher H, Huang YS (2005) Elongation of long-chain fatty acids. Prog Lipid Res 43:36–54Google Scholar
  29. Luttgeharm KD, Kimberlin NA, Cahoon EB (2016) Plant sphingolipid metabolism and function. Subcell Biochem 86:249–286Google Scholar
  30. Markham JE, Jaworski JG (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 21:1304–1314Google Scholar
  31. Meyer A, Kirsch H, Domergue F, Abbadi A, Sperling P, Bauer J, Cirpus P, Zank TK, Moreau H, Roscoe TJ, Zahringer U, Heinz E (2004) Novel fatty acid elongases and their use for the reconstitution docosahexaenoic acid biosynthesis. J Lipid Res 45:1899–1909Google Scholar
  32. Mitchell AG, Martin CE (1997) Fah1p, a Saccharomyces cerevisiae cytochrome b 5 fusion protein, and its Arabidopsis thaliana homolog that lacks the cytochrome b 5 domain both function in the alpha-hydroxylation of sphingolipid-associated very long chain fatty acids. J Biol Chem 272:28281–28288Google Scholar
  33. Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663Google Scholar
  34. Nagano M, Ihara-Ohori Y, Imai H, Inada N, Fujimoto M, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2009) Functional association of cell death suppressor, Arabidopsis Bax inhibitor-1, with fatty acid 2-hydroxylation through cytochrome b 5. Plant J 17:122–134Google Scholar
  35. Nagano M, Takahara K, Fujimoto M, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2012) Arabidopsis sphingolipid fatty acid 2-hydroxylases (AtFAH1 and AtFAH2) are functionally differentiated in fatty acid 2-hydroxylation and stress responses. Plant Physiol 159:1138–1148Google Scholar
  36. Nagano M, Ishikawa T, Ogawa Y, Iwabuchi M, Nakasone A, Shimamoto K, Uchimiya H, Kawai-Yamada M (2014) Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes. Planta 240:77–89Google Scholar
  37. Nagano M, Ishikawa T, Fujiwara M, Fukao Y, Kawano Y, Kawai-Yamada M, Shimamoto K (2016) Plasma membrane microdomains are essential for Rac1-RbohB/H-mediated immunity in rice. Plant Cell 28:1966–1983Google Scholar
  38. Nakagawa T, Suzuki T, Nakamura S, Hino T, Maeo K, Tabata T, Kawai T, Tanaka K, Niwa Y, Watanabe K, Kimura T, Ishiguro S (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71:2091–2100Google Scholar
  39. Oh CS, Toke DA, Mandala S, Martin CE (1997) ELO2 and ELO3, homologues of the Saccharomyces cerevisiae ELO1 gene, function in fatty acid elongation and are required for sphingolipid formation. J Biol Chem 272:17376–17384Google Scholar
  40. Quist TM, Sokolchik I, Shi H, Joly RJ, Bressan RA, Maggio A, Narsimhan M, Li X (2009) HOS3, and ELO-like gene, inhibits effects of ABA and implicates S-1-P/ceramide control system for abiotic stress responses in Arabidopsis thaliana. Mol Plant 2:138–151Google Scholar
  41. Raffaele S, Leger A, Roby D (2009) Very long chain fatty acid and lipid signaling in the response of plants to pathogens. Plant Signal Behav 4:94–99Google Scholar
  42. Ramiro DA, Melotto-Passarin DM, Barbosa Mde A, Santos FD, Gomez SG, Massola Junior NS, Lam E, Carrer H (2016) Expression of Arabidopsis Bax Inhibitor-1 in transgenic sugarcane confers drought tolerance. Plant Biotechnol J 14:1826–1837Google Scholar
  43. Revardel E, Bonneau M, Durrens P, Aigle M (1995) Characterization of a new gene family developing pleiotropic phenotypes upon mutation in Saccharomyces cerevisiae. Biochim Biophys Acta 1263:261–265Google Scholar
  44. Sawai H, Okamoto Y, Luberto C, Mao C, Bielawska A, Domae N, Hannun YA (2000) Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275:39793–39798Google Scholar
  45. Schenkman JB, Jansson I (2003) The many roles of cytochrome b 5. Pharmacol Ther 97:139–152Google Scholar
  46. Scotton DC, Azevedo MD, Sestari I, Da Silva JS, Souza LA, Peres LE, Leal GA Jr, Figueira A (2016) Expression of the Theobroma cacao Bax-inhibitor-1 gene in tomato reduces infection by the hemibiotrophic pathogen Moniliophthora perniciosa. Mol Plant Pathol.  https://doi.org/10.1111/mpp.12463 Google Scholar
  47. Silve S, Leplatois P, Josse A, Dupuy PH, Lanau C, Kaghad M, Dhers C, Picard C, Rahier A, Taton M, Fur G, Caput D, Ferrara P, Loison G (1996) The immunosuppressant SR 31747 blocks cell proliferation by inhibiting a steroid isomerase in Saccharomyces cerevisiae. Mol Cell Biol 16:2719–2727Google Scholar
  48. Simon-Plas F, Perraki A, Bayer E, Gerbeau-Pissot P, Mongrand S (2011) An update on plant membrane rafts. Curr Opin Plant Biol 14:642–649Google Scholar
  49. Wang X, Tang C, Huang X, Li F, Chen X, Zhang G, Sun Y, Han D, Kang Z (2012) Wheat BAX inhibitor-1 contributes to wheat resistance to Puccinia striiformis. J Exp Bot 63:4571–4584Google Scholar
  50. Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894Google Scholar
  51. Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283:3200–3210Google Scholar
  52. Wattelet-Boyer V, Brocard L, Jonsson K, Esnay N, Joubes J, Domergue F, Mongrand S, Raikhel N, Bhalerao RP, Moreau P, Boutte Y (2016) Enrichment of hydroxylated C24- and C26-anyl-chain sphingolipids mediated PIN2 apical sorting at trans-Golgi network subdomains. Nat Commun 7:12788Google Scholar
  53. Wittke S, Lewke N, Muller S, Johnsson N (1999) Probing the molecular environmental of membrane proteins in vivo. Mol Biol Cell 10:2519–2530Google Scholar
  54. Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apopotic suppressor identified by the functional screening in yeasts. Mol Cell 1:337–346Google Scholar
  55. Yoshinaga K, Arimura SI, Niwa Y, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2005) Mitochondrial behavior in the early stages of ROS stress leading to cell death in Arabidopsis thaliana. Ann Bot 96:337–342Google Scholar
  56. Zank TK, Zahringer U, Beckmann C, Pohnert G, Boland W, Holtorf H, Reski R, Lerchl J, Heinz E (2002) Cloning and functional characterization of an enzyme involved in the elongation of Delta6-polyunsaturated fatty acids from the moss Physcomitrella patens. Plant J 31:255–268Google Scholar
  57. Zhang K, Kniazeva M, Han M, Li W, Yu Z, Yang Z, Li Y, Metzker ML, Allikmets R, Zack DJ, Kakuk LE, Lagali PS, Wong PW, MacDonald IM, Sieving PA, Figueroa DJ, Austin CP, Gould RJ, Ayyagari R, Petrukhin K (2001) A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat Genet 27:89–93Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Minoru Nagano
    • 1
    Email author
  • Chikako Kakuta
    • 2
  • Yoichiro Fukao
    • 1
  • Masayuki Fujiwara
    • 3
    • 4
  • Hirofumi Uchimiya
    • 2
    • 5
  • Maki Kawai-Yamada
    • 5
  1. 1.Graduate School of Life SciencesRitsumeikan UniversityKusatsuJapan
  2. 2.Institute of Molecular and Cellular BiosciencesUniversity of TokyoTokyoJapan
  3. 3.Institute of Advanced BiosciencesKeio UniversityTsuruokaJapan
  4. 4.YANMAR Co., LtdOsakaJapan
  5. 5.Graduate School of Science and EngineeringSaitama UniversitySakurakuJapan

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