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References

  1. Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. 1996. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch. Microbiol. 165: 377-386.
    Pubmed CrossRef
  2. Alvarez HM, Pucci OH, Steinbüchel A. 1997. Lipid storage compounds in marine bacteria. Appl. Microbiol. Biotechnol. 47: 132-139.
    CrossRef
  3. Beja O, Suzuki MT, Koonin EV, Aravind L, Hadd A, Nguyen LP, et al. 2000. Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2: 516-529.
    Pubmed CrossRef
  4. Brady SF, Chao CJ, Handelsman J, Clardy J. 2001. Cloning and heterologous expression of a natural product biosynthetic gene cluster from cDNA. Org. Lett. 3: 1981-1984.
    Pubmed CrossRef
  5. Bredemeier R, Hulsch R, Metzger JO, Berthe-Corti L. 2003. Submersed culture production of extracellular wax esters by the marine bacterium Fundibacter jadensis. Mar. Biotechnol. 52: 579-583.
  6. Bryn K, Jantzen E, Bovre K. 1977. Occurrence and patterns of waxes in Neisseriaceae. J. Gen. Microbiol. 102: 33-43.
    Pubmed CrossRef
  7. Cases S, Stone SJ, Zhou P, Yen E, Tow B, Lardizabal KD, et al. 2001. Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members. J. Biol. Chem. 276: 38870-38876.
    Pubmed CrossRef
  8. Chung EJ, Lim HK, Kim JC, Choi GJ, Park EJ, Lee MH, et al. 2008. Forest soil metagenome gene cluster involved in antifungal activity expression in Escherichia coli. Appl. Environ. Microbiol. 74: 723-730.
    Pubmed PMC CrossRef
  9. Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, et al. 2003. Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl. Environ. Microbiol. 69: 49-55.
    Pubmed PMC CrossRef
  10. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, et al. 2000. Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl. Acad. Sci. USA 97: 6487-6492.
    Pubmed PMC CrossRef
  11. El-Komy MH. 2014. Comparative analysis of defense response in chocolate spot-resistant and -susceptible faba bean (Vicia faba) cultivars following infection by the necrotrophic fungus Botrytis fabae. Plant Pathol. J. 30: 355-366.
    Pubmed PMC CrossRef
  12. Elend C, Schmeisser C, Leggewie C, Babiak P, Carballeira JD, Steele HL, et al. 2006. Isolation and biochemical characterization of two novel metagenome derived esterases. Appl. Environ. Microbiol. 72: 3637-3645.
    Pubmed PMC CrossRef
  13. Garton NJ, Christensen H, Minnikin DE, Adegbola RA, Barer MR. 2002. Intracellular lipophilic inclusions of mycobacteria in vitro and in sputum. Microbiology 148: 2951-2958.
    Pubmed CrossRef
  14. Gunawan ER, Basri M, Rahmani MB, Salleh AB, Rahman RNZ. 2004. Lipase-catalyzed synthesis of palm-based wax ester. J. Oleo Sci. 53: 417-477.
    CrossRef
  15. Handelsman J, Rondon MR, Brady SP, Clady J, Goodman RM. 1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5: R245-R249.
    CrossRef
  16. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
    Pubmed PMC CrossRef
  17. Heilmann M, Iven T, Ahmann K, Homung E, Stymne S, Feussner I. 2012. Production of wax esters in plant seed oils by oleosomal cotargeting of biosynthetic enzymes. J. Lipid Res. 53: 2153-2161.
    Pubmed PMC CrossRef
  18. Holder JW, Ulrich JC, DeBono AC, Godfrey PA, Desjardins CA, Zucker J, et al. 2011. Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. PLoS Genet. 7: e1002219.
    Pubmed PMC CrossRef
  19. Holloway PJ. 1995. Waxes: chemistry, molecular biology and functions. Phytochemistry 39: 953-956.
    CrossRef
  20. Holtzapple E, Schmidt-Dannert C. 2007. Biosynthesis of isoprenoid wax ester in Marinobacter hydrocarbonoclasticus DSM 8798: identification and characterization of isoprenoid coenzyme A synthetase and wax ester synthases. J. Bacteriol. 189: 3804-3812.
    Pubmed PMC CrossRef
  21. Hong KS, Lim HK, Chung EJ, Park EJ, Lee MH, Kim JC, et al. 2007. Selection and characterization of forest soil metagenome genes encoding lipolytic enzymes. J. Microbiol. Biotechnol. 17: 1655-1660.
    Pubmed
  22. Jaeger KE, Dijkstra BW, Reetz MT. 1999. Bacterial biocatalysts:molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu. Rev. Microbiol. 53: 315-351.
    Pubmed CrossRef
  23. Jaeger KE, Egger T. 2002. Lipases for biotechnology. Curr. Opin. Biotechnol. 13: 390-397.
    CrossRef
  24. Kalscheuer R, Steinbüchel A. 2003. A novel bifunctional wax ester synthase/acyl-CoA: diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J. Biol. Chem. 278: 8075-8082.
    Pubmed CrossRef
  25. Kalscheuer R, Stöveken T, Luftmann H, Malkus U, Reichelt R, Steinbüchel A. 2006. Neutral lipid biosynthesis in engineered Escherichia coli: jojoba oil-like wax esters and fatty acid butyl esters. Appl. Environ. Microbiol. 72: 1373-1379.
    Pubmed PMC CrossRef
  26. Kim JS, Lim HK, Lee MH, Park J-H, Hwang EC, Moon BJ, Lee SW. 2009. Production of porphyrin intermediates in Escherichia coli carrying soil metagenome genes. FEMS Microbiol. Lett. 295: 42-49.
    Pubmed CrossRef
  27. Lee MH, Hong KS, Malhotra S, Park JH, Hwang EC, Choi HK, et al. 2010. A new esterase3 EstD2 isolated from plant rhizosphere soil metagenome. Appl. Microbiol. Biotechnol. 88:1125-1134.
    Pubmed CrossRef
  28. Lee MH, Lee SW. 2013. Bioprospecting potential of the soil metagenome: novel enzymes and bioactivities. Genomics Inform. 11: 114-120.
    Pubmed PMC CrossRef
  29. Lee SW, Won K, Lim HK, Kim JC, Choi GJ, Cho KY. 2004. Screening for novel lipolytic enzymes from uncultured soil microorganisms. Appl. Microbiol. Biotechnol. 65: 720-726.
    Pubmed CrossRef
  30. Reiser S, Somerville C. 1997. Isolation of mutants of Acinetobacter calcoaceticus deficient in wax ester synthesis and complementation of one mutation with a gene encoding a fatty acyl coenzyme A reductase. J. Bacteriol. 179: 2969-2975.
    Pubmed PMC
  31. Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, et al. 2000. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66:2541-2547.
    Pubmed PMC CrossRef
  32. Rontani JF, Bonin PC, Volkman JK. 1999. Production of wax esters during aerobic growth of marine bacteria on isoprenoid compounds. Appl. Environ. Microbiol. 65: 221-230.
    Pubmed PMC
  33. Russel NJ, Volkman JK. 1980. The effect of growth temperature and wax ester compositions in the psychrophilic bacterium Micrococcus cryophilus ATCC 15174. J. Gen. Microbiol. 118:131-141.
    CrossRef
  34. Sambrook J, Fritsch EF, Maniatis TA. 1989. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Habor Laboratory Press, Cold Spring Habor, NY.
  35. Sandager L, Gustavsson MH, Stahl U, Dahlqvist A, Wiber E, Banas A, et al. 2002. Storage lipid synthesis is non-essential in yeast. J. Biol. Chem. 277: 6478-6482.
    Pubmed CrossRef
  36. Simon C, Daniel R. 2011. Metagenomic analysis: past and future trends. Appl. Environ. Microbiol. 77: 1153-1161.
    Pubmed PMC CrossRef
  37. Sirakova TD, Dubey VS, Deb C, Daniel J, Korotkova TA, Abomoelak B, Kolattukudy PE. 2006. Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152: 2717-2725.
    Pubmed PMC CrossRef
  38. Steinbüchel A. 2001. Perspectives for biotechnological production and utilization of biopolymers: metabolic engineering of polyhydroxyalkanoate biosynthesis pathways as a successful example. Macromol. Biosci. 1: 1-24.
    CrossRef
  39. Stöveken T, Kalscheuer R, Malkus U, Reichelt R, Steinbüchel A. 2005. The wax ester synthase/acyl coenzyme A:diacylglycerol acyltransferase from Acinetobacter sp. strain ADP1: characterization of a novel type of acyltransferase. J. Bacteriol. 187: 1369-1376.
    Pubmed PMC CrossRef
  40. Tao W, Lee MH, Yoon M-Y, Kim JC, Malhotra S, Wu J, et al. 2011. Characterization of two metagenome-derived esterase that reactivate chloramphenicol by counteracting chloramphenicol acetyltrasnferase. J. Microbiol. Biotechnol. 21: 1203-1210.
    Pubmed CrossRef
  41. Tsujita T, Sumiyoshi M, Okuda H. 1999. Wax ester synthesizing activity of lipase. Lipids 34: 1159-1166.
    Pubmed CrossRef
  42. Wältermann M, Hinz A, Robenek H, Troyer D, Reichelt R, Malkus U, et al. 2005. Mechanism of lipid-body formation in prokaryotes: how bacteria fatten up. Mol. Microbiol. 55: 750-763.
    Pubmed CrossRef
  43. Wältermann M, Steinbüchel A. 2005. Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J. Bacteriol. 187:3607-3619.
    Pubmed PMC CrossRef
  44. Wu LF, Lam X, Bird PD, Zheng H, Samuels L, Jetter R, Kunst L. 2008. Identification of the wax ester synthase/acyl-coenzyme A:diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol. 148: 97-107.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(2): 248-254

Published online February 28, 2016 https://doi.org/10.4014/jmb.1507.07029

Copyright © The Korean Society for Microbiology and Biotechnology.

Characterization of a Soil Metagenome-Derived Gene Encoding Wax Ester Synthase

Nam Hee Kim 1, Ji-Hye Park 1, Eunsook Chung 1, Hyun-Ah So 1, Myung Hwan Lee 1, Jin-Cheol Kim 2, Eul Chul Hwang 1 and Seon-Woo Lee 1*

1Department of Applied Bioscience, Dong-A University, Busan 49315, Republic of Korea, 2Department of Agricultural Chemistry, Chonnam National University, Gwangju 61186, Republic of Korea

Received: July 7, 2015; Accepted: October 28, 2015

Abstract

A soil metagenome contains the genomes of all microbes included in a soil sample, including
those that cannot be cultured. In this study, soil metagenome libraries were searched for
microbial genes exhibiting lipolytic activity and those involved in potential lipid metabolism
that could yield valuable products in microorganisms. One of the subclones derived from the
original fosmid clone, pELP120, was selected for further analysis. A subclone spanning a
3.3 kb DNA fragment was found to encode for lipase/esterase and contained an additional
partial open reading frame encoding a wax ester synthase (WES) motif. Consequently, both
pELP120 and the full length of the gene potentially encoding WES were sequenced. To
determine if the wes gene encoded a functioning WES protein that produced wax esters, gas
chromatography-mass spectroscopy was conducted using ethyl acetate extract from an
Escherichia coli strain that expressed the wes gene and was grown with hexadecanol. The ethyl
acetate extract from this E. coli strain did indeed produce wax ester compounds of various
carbon-chain lengths. DNA sequence analysis of the full-length gene revealed that the gene
cluster may be derived from a member of Proteobacteria, whereas the clone does not contain
any clear phylogenetic markers. These results suggest that the wes gene discovered in this
study encodes a functional protein in E. coli and produces wax esters through a heterologous
expression system.

Keywords: Lipid metabolism, soil metagenome, wax ester synthase, wes

References

  1. Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. 1996. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch. Microbiol. 165: 377-386.
    Pubmed CrossRef
  2. Alvarez HM, Pucci OH, Steinbüchel A. 1997. Lipid storage compounds in marine bacteria. Appl. Microbiol. Biotechnol. 47: 132-139.
    CrossRef
  3. Beja O, Suzuki MT, Koonin EV, Aravind L, Hadd A, Nguyen LP, et al. 2000. Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2: 516-529.
    Pubmed CrossRef
  4. Brady SF, Chao CJ, Handelsman J, Clardy J. 2001. Cloning and heterologous expression of a natural product biosynthetic gene cluster from cDNA. Org. Lett. 3: 1981-1984.
    Pubmed CrossRef
  5. Bredemeier R, Hulsch R, Metzger JO, Berthe-Corti L. 2003. Submersed culture production of extracellular wax esters by the marine bacterium Fundibacter jadensis. Mar. Biotechnol. 52: 579-583.
  6. Bryn K, Jantzen E, Bovre K. 1977. Occurrence and patterns of waxes in Neisseriaceae. J. Gen. Microbiol. 102: 33-43.
    Pubmed CrossRef
  7. Cases S, Stone SJ, Zhou P, Yen E, Tow B, Lardizabal KD, et al. 2001. Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members. J. Biol. Chem. 276: 38870-38876.
    Pubmed CrossRef
  8. Chung EJ, Lim HK, Kim JC, Choi GJ, Park EJ, Lee MH, et al. 2008. Forest soil metagenome gene cluster involved in antifungal activity expression in Escherichia coli. Appl. Environ. Microbiol. 74: 723-730.
    Pubmed KoreaMed CrossRef
  9. Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, et al. 2003. Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl. Environ. Microbiol. 69: 49-55.
    Pubmed KoreaMed CrossRef
  10. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, et al. 2000. Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl. Acad. Sci. USA 97: 6487-6492.
    Pubmed KoreaMed CrossRef
  11. El-Komy MH. 2014. Comparative analysis of defense response in chocolate spot-resistant and -susceptible faba bean (Vicia faba) cultivars following infection by the necrotrophic fungus Botrytis fabae. Plant Pathol. J. 30: 355-366.
    Pubmed KoreaMed CrossRef
  12. Elend C, Schmeisser C, Leggewie C, Babiak P, Carballeira JD, Steele HL, et al. 2006. Isolation and biochemical characterization of two novel metagenome derived esterases. Appl. Environ. Microbiol. 72: 3637-3645.
    Pubmed KoreaMed CrossRef
  13. Garton NJ, Christensen H, Minnikin DE, Adegbola RA, Barer MR. 2002. Intracellular lipophilic inclusions of mycobacteria in vitro and in sputum. Microbiology 148: 2951-2958.
    Pubmed CrossRef
  14. Gunawan ER, Basri M, Rahmani MB, Salleh AB, Rahman RNZ. 2004. Lipase-catalyzed synthesis of palm-based wax ester. J. Oleo Sci. 53: 417-477.
    CrossRef
  15. Handelsman J, Rondon MR, Brady SP, Clady J, Goodman RM. 1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5: R245-R249.
    CrossRef
  16. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
    Pubmed KoreaMed CrossRef
  17. Heilmann M, Iven T, Ahmann K, Homung E, Stymne S, Feussner I. 2012. Production of wax esters in plant seed oils by oleosomal cotargeting of biosynthetic enzymes. J. Lipid Res. 53: 2153-2161.
    Pubmed KoreaMed CrossRef
  18. Holder JW, Ulrich JC, DeBono AC, Godfrey PA, Desjardins CA, Zucker J, et al. 2011. Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. PLoS Genet. 7: e1002219.
    Pubmed KoreaMed CrossRef
  19. Holloway PJ. 1995. Waxes: chemistry, molecular biology and functions. Phytochemistry 39: 953-956.
    CrossRef
  20. Holtzapple E, Schmidt-Dannert C. 2007. Biosynthesis of isoprenoid wax ester in Marinobacter hydrocarbonoclasticus DSM 8798: identification and characterization of isoprenoid coenzyme A synthetase and wax ester synthases. J. Bacteriol. 189: 3804-3812.
    Pubmed KoreaMed CrossRef
  21. Hong KS, Lim HK, Chung EJ, Park EJ, Lee MH, Kim JC, et al. 2007. Selection and characterization of forest soil metagenome genes encoding lipolytic enzymes. J. Microbiol. Biotechnol. 17: 1655-1660.
    Pubmed
  22. Jaeger KE, Dijkstra BW, Reetz MT. 1999. Bacterial biocatalysts:molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu. Rev. Microbiol. 53: 315-351.
    Pubmed CrossRef
  23. Jaeger KE, Egger T. 2002. Lipases for biotechnology. Curr. Opin. Biotechnol. 13: 390-397.
    CrossRef
  24. Kalscheuer R, Steinbüchel A. 2003. A novel bifunctional wax ester synthase/acyl-CoA: diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J. Biol. Chem. 278: 8075-8082.
    Pubmed CrossRef
  25. Kalscheuer R, Stöveken T, Luftmann H, Malkus U, Reichelt R, Steinbüchel A. 2006. Neutral lipid biosynthesis in engineered Escherichia coli: jojoba oil-like wax esters and fatty acid butyl esters. Appl. Environ. Microbiol. 72: 1373-1379.
    Pubmed KoreaMed CrossRef
  26. Kim JS, Lim HK, Lee MH, Park J-H, Hwang EC, Moon BJ, Lee SW. 2009. Production of porphyrin intermediates in Escherichia coli carrying soil metagenome genes. FEMS Microbiol. Lett. 295: 42-49.
    Pubmed CrossRef
  27. Lee MH, Hong KS, Malhotra S, Park JH, Hwang EC, Choi HK, et al. 2010. A new esterase3 EstD2 isolated from plant rhizosphere soil metagenome. Appl. Microbiol. Biotechnol. 88:1125-1134.
    Pubmed CrossRef
  28. Lee MH, Lee SW. 2013. Bioprospecting potential of the soil metagenome: novel enzymes and bioactivities. Genomics Inform. 11: 114-120.
    Pubmed KoreaMed CrossRef
  29. Lee SW, Won K, Lim HK, Kim JC, Choi GJ, Cho KY. 2004. Screening for novel lipolytic enzymes from uncultured soil microorganisms. Appl. Microbiol. Biotechnol. 65: 720-726.
    Pubmed CrossRef
  30. Reiser S, Somerville C. 1997. Isolation of mutants of Acinetobacter calcoaceticus deficient in wax ester synthesis and complementation of one mutation with a gene encoding a fatty acyl coenzyme A reductase. J. Bacteriol. 179: 2969-2975.
    Pubmed KoreaMed
  31. Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, et al. 2000. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66:2541-2547.
    Pubmed KoreaMed CrossRef
  32. Rontani JF, Bonin PC, Volkman JK. 1999. Production of wax esters during aerobic growth of marine bacteria on isoprenoid compounds. Appl. Environ. Microbiol. 65: 221-230.
    Pubmed KoreaMed
  33. Russel NJ, Volkman JK. 1980. The effect of growth temperature and wax ester compositions in the psychrophilic bacterium Micrococcus cryophilus ATCC 15174. J. Gen. Microbiol. 118:131-141.
    CrossRef
  34. Sambrook J, Fritsch EF, Maniatis TA. 1989. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Habor Laboratory Press, Cold Spring Habor, NY.
  35. Sandager L, Gustavsson MH, Stahl U, Dahlqvist A, Wiber E, Banas A, et al. 2002. Storage lipid synthesis is non-essential in yeast. J. Biol. Chem. 277: 6478-6482.
    Pubmed CrossRef
  36. Simon C, Daniel R. 2011. Metagenomic analysis: past and future trends. Appl. Environ. Microbiol. 77: 1153-1161.
    Pubmed KoreaMed CrossRef
  37. Sirakova TD, Dubey VS, Deb C, Daniel J, Korotkova TA, Abomoelak B, Kolattukudy PE. 2006. Identification of a diacylglycerol acyltransferase gene involved in accumulation of triacylglycerol in Mycobacterium tuberculosis under stress. Microbiology 152: 2717-2725.
    Pubmed KoreaMed CrossRef
  38. Steinbüchel A. 2001. Perspectives for biotechnological production and utilization of biopolymers: metabolic engineering of polyhydroxyalkanoate biosynthesis pathways as a successful example. Macromol. Biosci. 1: 1-24.
    CrossRef
  39. Stöveken T, Kalscheuer R, Malkus U, Reichelt R, Steinbüchel A. 2005. The wax ester synthase/acyl coenzyme A:diacylglycerol acyltransferase from Acinetobacter sp. strain ADP1: characterization of a novel type of acyltransferase. J. Bacteriol. 187: 1369-1376.
    Pubmed KoreaMed CrossRef
  40. Tao W, Lee MH, Yoon M-Y, Kim JC, Malhotra S, Wu J, et al. 2011. Characterization of two metagenome-derived esterase that reactivate chloramphenicol by counteracting chloramphenicol acetyltrasnferase. J. Microbiol. Biotechnol. 21: 1203-1210.
    Pubmed CrossRef
  41. Tsujita T, Sumiyoshi M, Okuda H. 1999. Wax ester synthesizing activity of lipase. Lipids 34: 1159-1166.
    Pubmed CrossRef
  42. Wältermann M, Hinz A, Robenek H, Troyer D, Reichelt R, Malkus U, et al. 2005. Mechanism of lipid-body formation in prokaryotes: how bacteria fatten up. Mol. Microbiol. 55: 750-763.
    Pubmed CrossRef
  43. Wältermann M, Steinbüchel A. 2005. Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J. Bacteriol. 187:3607-3619.
    Pubmed KoreaMed CrossRef
  44. Wu LF, Lam X, Bird PD, Zheng H, Samuels L, Jetter R, Kunst L. 2008. Identification of the wax ester synthase/acyl-coenzyme A:diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol. 148: 97-107.
    Pubmed KoreaMed CrossRef