Plant Cell Reports

, Volume 34, Issue 4, pp 557–572 | Cite as

Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species

  • Saet Buyl Lee
  • Mi Chung SuhEmail author


The aerial parts of plants are covered with a cuticle, a hydrophobic layer consisting of cutin polyester and cuticular waxes that protects them from various environmental stresses. Cuticular waxes mainly comprise very long chain fatty acids and their derivatives such as aldehydes, alkanes, secondary alcohols, ketones, primary alcohols, and wax esters that are also important raw materials for the production of lubricants, adhesives, cosmetics, and biofuels. The major function of cuticular waxes is to control non-stomatal water loss and gas exchange. In recent years, the in planta roles of many genes involved in cuticular wax biosynthesis have been characterized not only from model organisms like Arabidopsis thaliana and saltwater cress (Eutrema salsugineum), but also crop plants including maize, rice, wheat, tomato, petunia, Medicago sativa, Medicago truncatula, rapeseed, and Camelina sativa through genetic, biochemical, molecular, genomic, and cell biological approaches. In this review, we discuss recent advances in the understanding of the biological functions of genes involved in cuticular wax biosynthesis, transport, and regulation of wax deposition from Arabidopsis and crop species, provide information on cuticular wax amounts and composition in various organs of nine representative plant species, and suggest the important issues that need to be investigated in this field of study.


Arabidopsis thaliana Crop Cuticle Plant Stress Wax 



ATP binding cassette


Acyl-CoA binding protein


Acetyl-CoA carboxylase


Enoyl-CoA reductase


Fatty acids elongase


Fatty acyl-CoA reductase




β-Hydroxyacyl-CoA dehydratase


β-Ketoacyl-CoA reductase


β-Ketoacyl-CoA synthase


Long chain acyl-CoA synthase


Lipid transfer proteins


Midchain alkane hydroxylase


Very long chain fatty acid


Bifunctional wax synthase/acyl-CoA:diacylglycerol acyltransferase



We would like to express our sincere gratitude to Ljerka Kunst (University of British Columbia) for her critical review. This work was supported by grants from the Next-Generation BioGreen 21 Program (PJ0110522015) of the Rural Development Administration, Republic of Korea, and the National Research Foundation (2013R1A2A2A01015672) of Korea.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aarts MG, Keijzer CJ, Stiekema WJ et al (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127PubMedCentralPubMedGoogle Scholar
  2. Aharoni A, Dixit S, Jetter R et al (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16:2463–2480PubMedCentralPubMedGoogle Scholar
  3. Avato P, Mikkelsen JD, von Wettstein-Knowles P (1982) Synthesis of epicuticular primary alcohols and intracellular fatty acids by tissue slices from cer-j59 barley leaves. Carlsberg Res Commun 47:377–390Google Scholar
  4. Avato P, Bianchi G, Nayak A et al (1987) Epicuticular waxes of maize as affected by the interaction of mutant gl8 with gl3, gl4 and gl15. Lipids 22:11–16Google Scholar
  5. Bach L, Faure J-D (2010) Role of very-long-chain fatty acids in plant development, when chain length does matter. C R Biol 333:361–370PubMedGoogle Scholar
  6. Bach L, Michaelson LV, Haslam R et al (2008) The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proc Natl Acad Sci USA 105:14727–14731PubMedCentralPubMedGoogle Scholar
  7. Barthlott W, Neinhuis C, Cutler D et al (1998) Classification and terminology of plant epicuticular waxes. Bot J Linn Soc 126:237–260Google Scholar
  8. Beaudoin F, Wu X, Li F et al (2009) Functional characterization of the Arabidopsis β-ketoacyl-coenzyme A reductase candidates of the fatty acid elongase. Plant Physiol 150:1174–1191PubMedCentralPubMedGoogle Scholar
  9. Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15:329–337PubMedGoogle Scholar
  10. Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52:110–129PubMedGoogle Scholar
  11. Bernard A, Domergue F, Pascal S et al (2012) Reconstitution of plant alkane biosynthesis in yeast demonstrates that Arabidopsis ECERIFERUM1 and ECERIFERUM3 are core components of a very-long-chain alkane synthesis complex. Plant Cell 24:3106–3118PubMedCentralPubMedGoogle Scholar
  12. Bianchi G, Avato P, Salamini F (1979) The absence of fatty acid aldehydes in gl1 gl2 waxes. Maize Gen Coop Newsletter 53:103Google Scholar
  13. Bianchi A, Bianchi G, Avato P et al (1985) Biosynthetic pathways of epicuticular wax of maize as assessed by mutation, light, plant age and inhibitor studies. Maydica 30:179–198Google Scholar
  14. Bird D, Beisson F, Brigham A et al (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52:485–498PubMedGoogle Scholar
  15. Bonaventure B, Salas JJ, Pollard MR et al (2003) Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 15:1020–1033PubMedCentralPubMedGoogle Scholar
  16. Bourdenx B, Bernard A, Domergue F et al (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156:29–45PubMedCentralPubMedGoogle Scholar
  17. Broun P, Poindexter P, Osborne E et al (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101:4706–4711PubMedCentralPubMedGoogle Scholar
  18. Buschhaus C, Jetter R (2011) Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces? J Exp Bot 62:841–853PubMedGoogle Scholar
  19. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183PubMedCentralPubMedGoogle Scholar
  20. Carrasco S, Meyer T (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80:973–1000PubMedCentralPubMedGoogle Scholar
  21. Chen XB, Goodwin SM, Boroff VL et al (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15:1170–1185PubMedCentralPubMedGoogle Scholar
  22. Chen X, Goodwin SM, Liu X et al (2005) Mutation of the RESURRECTION1 locus of Arabidopsis reveals an association of cuticular wax with embryo development 1. Plant Physiol 139:909–919PubMedCentralPubMedGoogle Scholar
  23. DeBono A, Yeats TH, Rose JKC et al (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21:1230–1238PubMedCentralPubMedGoogle Scholar
  24. Dietrich CR, Perera MADN, Yandeau-Nelson DM et al (2005) Characterization of two GL8 paralogs reveals that the 3-ketoacyl reductase component of fatty acid elongase is essential for maize (Zea mays L.) development. Plant J 42:844–861PubMedGoogle Scholar
  25. Dubos C, Stracke R, Grotewold E et al (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581PubMedGoogle Scholar
  26. Dunn TM, Lynch DV, Michaelson LV et al (2004) A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann Bot 93:483–497PubMedCentralPubMedGoogle Scholar
  27. Fiebig A, Mayfield JA, Miley NL et al (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12:2001–2008PubMedCentralPubMedGoogle Scholar
  28. Franke R, Höfer R, Briesen I et al (2009) The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. Plant J 57:80–95PubMedGoogle Scholar
  29. Go YS, Kim H, Kim HJ et al (2014) Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. Plant Cell 26:1666–1680PubMedCentralPubMedGoogle Scholar
  30. Graham LE (1993) Origin of land plants. Wiley, New YorkGoogle Scholar
  31. Greer S, Wen M, Bird D et al (2007) The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol 145:653–667PubMedCentralPubMedGoogle Scholar
  32. Guo L, Yang H, Zhang X et al (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767PubMedCentralPubMedGoogle Scholar
  33. Hannoufa A, McNevin J, Lemieux B (1993) Epicuticular wax of eceriferum mutants of Arabidopsis thaliana. Phytochemistry 33:851–855Google Scholar
  34. Hansen JD, Pyee J, Xia Y et al (1997) The glossy1 locus of maize and an epidermis-specific cDNA from Klenia odora define a class of receptor-like proteins required for the normal accumulation of cuticular waxes. Plant Physiol 113:1091–1100PubMedCentralPubMedGoogle Scholar
  35. Haslam TM, Kunst L (2013) Extending the story of very-long-chain fatty acid elongation. Plant Sci 210:93–107PubMedGoogle Scholar
  36. Haslam TM, Manas-Fernandez A, Zhao L et al (2012) Arabidopsis ECERIFERUM2 is a component of the fatty acid elongation machinery required for fatty acid extension to exceptional lengths. Plant Physiol 160:1164–1174PubMedCentralPubMedGoogle Scholar
  37. Haslam T, Haslam RP, Thoraval D et al (2015) CER2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiol. (pii: pp.114.253195) [Epub ahead of print]Google Scholar
  38. Hooker TS, Millar AA, Kunst L (2002) Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol 129:1568–1580PubMedCentralPubMedGoogle Scholar
  39. Hooker TS, Lam P, Zheng H et al (2007) A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19:904–913PubMedCentralPubMedGoogle Scholar
  40. Isaacson T, Kosma DK, Matas AJ et al (2009) Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J 60:363–377PubMedGoogle Scholar
  41. Islam MA, Du H, Ning J et al (2009) Characterization of Glossy1-homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Mol Biol 70:443–456PubMedGoogle Scholar
  42. Ito Y, Kimura F, Hirakata K et al (2011) Fatty acid elongase is required for shoot development in rice. Plant J 66:680–688PubMedGoogle Scholar
  43. James DW, Lim E, Keller J et al (1995) Directed tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon activator. Plant Cell 7:309–319PubMedCentralPubMedGoogle Scholar
  44. Javelle M, Vernoud V, Depege-Fargeix N et al (2010) Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiol 154:273–286PubMedCentralPubMedGoogle Scholar
  45. Jenks MA, Rich PJ, Peters PJ et al (1992) Epicuticular wax morphology of bloomless (bm) mutants in Sorghum bicolor. Int J Plant Sci 153:311–319Google Scholar
  46. Jenks MA, Tuttle HA, Eigenbrode SD et al (1995) Leaf epicuticular waxes of the eceriferum mutants in Arabidopsis. Plant Physiol 108:369–377PubMedCentralPubMedGoogle Scholar
  47. Jessen D, Olbrich A, Knüfer J et al (2011) Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis. Plant J 68:715–726PubMedGoogle Scholar
  48. Jetter R, Kunst L (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J 54:670–683PubMedGoogle Scholar
  49. Jetter R, Kunst L, Samuels AL (2007) Composition of plant cuticular waxes. In: Riederer M, Müller C (eds) Biology of the plant cuticle, vol 23. Blackwell, Oxford, pp 145–181Google Scholar
  50. Jung KH, Han MJ, Dy Lee et al (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18:3015–3032PubMedCentralPubMedGoogle Scholar
  51. Kagale S, Koh C, Nixon J et al (2014) The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Commun 5:3706PubMedCentralPubMedGoogle Scholar
  52. Kannangara R, Branigan C, Liu Y et al (2007) The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19:1278–1294PubMedCentralPubMedGoogle Scholar
  53. Kim H, Lee SB, Kim HJ et al (2012) Characterization of glycosylphosphatidylinositol-anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. Plant Cell Physiol 53:1391–1403PubMedGoogle Scholar
  54. Kim J, Jung JH, Lee SB et al (2013) Arabidopsis 3-ketoacyl-coenzyme A synthase9 is involved in the synthesis of tetracosanoic acids as precursors of cuticular waxes, suberins, sphingolipids, and phospholipids. Plant Physiol 162:567–580PubMedCentralPubMedGoogle Scholar
  55. Kim S, Park M, Yeom SI et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278PubMedGoogle Scholar
  56. Koornneef M, Hanhart CJ, Thiel F (1989) A genetic and phenotypic description of eceriferum (cer) mutants in Arabidopsis thaliana. J Hered 80:118–122Google Scholar
  57. Kosma DK, Jenks MA (2007) Eco-physiological and molecular-genetic determinants of plant cuticle function in drought and salt stress tolerance. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in Molecular Breeding toward Drought and Salt Tolerant Crops. Springer, Dordrecht, pp 91–120Google Scholar
  58. Kosma DK, Bourdenx B, Bernard A et al (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151:1918–1929PubMedCentralPubMedGoogle Scholar
  59. Kosma DK, Parsons EP, Isaacson T et al (2010) Fruit cuticle lipid composition during development in tomato ripening mutants. Physiol Plant 139:107–117PubMedGoogle Scholar
  60. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42:51–80PubMedGoogle Scholar
  61. Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12:721–727PubMedGoogle Scholar
  62. Kunst L, Taylor DC, Underhill EW (1992) Fatty-acid elongation in developing seeds of Arabidopsis thaliana. Plant Physiol Biochem 30:425–434Google Scholar
  63. Lam P, Zhao L, McFarlane HE et al (2012) RDR1 and SGS3, components of RNA-mediated gene silencing, are required for the regulation of cuticular wax biosynthesis in developing inflorescence stems of Arabidopsis. Plant Physiol 159:1385–1395PubMedCentralPubMedGoogle Scholar
  64. Lam P, Zhao L, Eveleigh N et al (2014) The exosome and trans-acting small interfering RNAs regulate cuticular wax biosynthesis during Arabidopsis inflorescence stem development. Plant Physiol 167:323–336PubMedGoogle Scholar
  65. Lee SB, Suh MC (2013) Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol Plant 6:246–249PubMedGoogle Scholar
  66. Lee SB, Suh MC (2014) Cuticular wax biosynthesis is up-regulated by the MYB94 transcription factor in Arabidopsis. Plant Cell Physiol 56:48–60PubMedGoogle Scholar
  67. Lee SB, Go YS, Bae HJ et al (2009a) Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol 150:42–54PubMedCentralPubMedGoogle Scholar
  68. Lee SB, Jung SJ, Go YS et al (2009b) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60:462–475PubMedGoogle Scholar
  69. Lee SB, Kim H, Kim RJ et al (2014) Overexpression of Arabidopsis MYB96 confers drought resistance in Camelina sativa via cuticular wax accumulation. Plant Cell Rep 33:1535–1546PubMedGoogle Scholar
  70. Leide J, Hildebrandt U, Reussing K et al (2007) The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in β-ketoacyl-coenzyme a synthase (LeCER6). Plant Physiol 144:1667–1679PubMedCentralPubMedGoogle Scholar
  71. Leide J, Hildebrandt U, Vogg G et al (2011) The positional sterile (ps) mutation affects cuticular transpiration and wax biosynthesis of tomato fruits. J Plant Physiol 168:871–877PubMedGoogle Scholar
  72. Lemieux B (1996) Molecular genetics of epicuticular waxes biosynthesis. Trends Plant Sci 1:312–318Google Scholar
  73. Li YH, Beisson F, Ohlrogge J et al (2007) Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin-associated acyltransferase. Plant Physiol 144:1267–1277PubMedCentralPubMedGoogle Scholar
  74. Li F, Wu X, Lam P et al (2008) Identification of the wax ester synthase/acyl-coenzyme A: diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol 148:97–107PubMedCentralPubMedGoogle Scholar
  75. Li L, Li D, Liu S et al (2013) The maize glossy13 gene, cloned via BSR-Seq and Seq-Walking encodes a putative ABC transporter required for the normal accumulation of epicuticular waxes. PLoS One 8:e82333PubMedCentralPubMedGoogle Scholar
  76. Li-Beisson Y, Shorrosh B, Beisson F et al (2013) Acyl-Lipid metabolism. Arabidopsis Book 11:e0161. doi: 10.1199/tab.0161 PubMedCentralPubMedGoogle Scholar
  77. Liu S, Dietrich CR, Schnable PS (2009) DLA-based strategies for cloning insertion mutants: cloning the gl4 locus of maize using Mu transposon tagged alleles. Genetics 183:1215–1225PubMedCentralPubMedGoogle Scholar
  78. Liu S, Yeh C-T, Tang HM et al (2012) Gene mapping via bulked segregant RNA-Seq (BSR-Seq). PLoS One 7:e36406. doi: 10.1371/journal.pone.0036406 PubMedCentralPubMedGoogle Scholar
  79. Lü S, Song T, Kosma DK et al (2009) Arabidopsis CER8 encodes long-chain acyl CoA synthetase 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59:553–564PubMedGoogle Scholar
  80. Lü S, Zhao H, Parsons EP et al (2011) The glossyhead1 allele of ACC1 reveals a principal role for multidomain acetyl-coenzyme A carboxylase in the biosynthesis of cuticular waxes by Arabidopsis. Plant Physiol 157:1079–1092PubMedCentralPubMedGoogle Scholar
  81. Lü S, Zhao H, Des Marais DL et al (2012) Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol 159:930–944PubMedCentralPubMedGoogle Scholar
  82. Luo B, Xue XY, Hu WL et al (2007) An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol 48:1790–1802PubMedGoogle Scholar
  83. Mao B, Cheng Z, Lei C et al (2012) Wax crystal-sparse leaf2, a rice homologue of WAX2/GL1, is involved in synthesis of leaf cuticular wax. Planta 235:39–52PubMedGoogle Scholar
  84. McFarlane HE, Shin JJH, Bird DA et al (2010) Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22:3066–3075PubMedCentralPubMedGoogle Scholar
  85. McFarlane HE, Watanabe Y, Yang W et al (2014) Golgi- and trans-Golgi network-mediated vesicle trafficking is required for wax secretion from epidermal cells. Plant Physiol 164:1250–1260PubMedCentralPubMedGoogle Scholar
  86. McNevin JP, Woodward W, Hannoufa A et al (1993) Isolation and characterization of eceriferum (cer) mutants induced by T-DNA insertions in Arabidopsis thaliana. Genome 36:610–618PubMedGoogle Scholar
  87. Ménard R, Verdier G, Ors M et al (2014) Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant Cell Physiol 55:455–466PubMedGoogle Scholar
  88. Millar AA, Kunst L (1997) Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. Plant J 12:121–131PubMedGoogle Scholar
  89. Millar AA, Clemens S, Zachgo S et al (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11:825–838PubMedCentralPubMedGoogle Scholar
  90. Nadakuduti SS, Pollard M, Kosma DK et al (2012) Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiol 159:945–960PubMedCentralPubMedGoogle Scholar
  91. Nawrath C, Schreiber L, Franke RB et al (2013) Apoplastic diffusion barriers in arabidopsis. Arabidopsis Book 11:e0167. doi: 10.1199/tab.0167 PubMedCentralPubMedGoogle Scholar
  92. O’Toole JC, Cruz RT (1983) Genotypic variation in epicuticular wax of rice. Crop Sci 23:392–400Google Scholar
  93. Oshima Y, ShikataM Koyama T et al (2013) MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25:1609–1624PubMedCentralPubMedGoogle Scholar
  94. Ouyang S, Zhu W, Hamilton J et al (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:883–887Google Scholar
  95. Panikashvili D, Savaldi-Goldstein S, Mandel T et al (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345–1360PubMedCentralPubMedGoogle Scholar
  96. Panikashvili D, Shi JX, Bocobza S et al (2010) The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant 3:563–575PubMedGoogle Scholar
  97. Panikashvili D, Shi JX, Schreiber L et al (2011) The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol 190:113–124PubMedGoogle Scholar
  98. Parsons EP, Popopvsky S, Lohrey GT et al (2013) Fruit cuticle lipid composition and water loss in a diverse collection of pepper (Capsicum). Physiol Plant 149:160–174PubMedGoogle Scholar
  99. Pascal S, Bernard A, Sorel M et al (2013) The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very-long-chain fatty acid elongation process. Plant J 73:733–746PubMedGoogle Scholar
  100. Pighin JA, Zheng HQ, Balakshin LJ et al (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704PubMedGoogle Scholar
  101. Pollard M, Beisson F, Li Y et al (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246PubMedGoogle Scholar
  102. Pruitt RE, Vielle-Calzada JP, Ploense SE et al (2000) FIDDLEHEAD a gene required to suppress epidermal cell interactions in Arabidopsis encodes a putative lipid biosynthetic enzyme. Proc Natl Acad Sci USA 97:1311–1316PubMedCentralPubMedGoogle Scholar
  103. Pu YY, Gao J, Guo YL et al (2013) A novel dominant glossy mutation causes suppression of wax biosynthesis pathway and deficiency of cuticular wax in Brassica napus. BMC Plant Biol 13:215PubMedCentralPubMedGoogle Scholar
  104. Qin BX, Tang D, Huang J et al (2011) Rice OsGL1-1 is involved in leaf cuticular wax and cuticle membrane. Mol Plant 4:985–995PubMedGoogle Scholar
  105. Quist TM, Sokolchik I, Shi H et al (2009) HOS3, an ELO-like gene, inhibits effects of ABA and implicates a S-1-P/ceramide control system for abiotic stress responses in Arabidopsis thaliana. Mol Plant 2:138–151PubMedCentralPubMedGoogle Scholar
  106. Raffaele S, Vailleau F, Léger A et al (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20:752–767PubMedCentralPubMedGoogle Scholar
  107. Rashotte AM, Jenks MA, Nguyen TD et al (1997) Epicuticular wax variation in ecotypes of Arabidopsis thaliana. Phytochemistry 45:251–255PubMedGoogle Scholar
  108. Razeq FM, Kosma DK, Rowland O et al (2014) Extracellular lipids of Camelina sativa: characterization of chloroform-extractable waxes from aerial and subterranean surfaces. Phytochemistry 106:188–196PubMedGoogle Scholar
  109. Roudier F, Gissot L, Beaudoin F et al (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375PubMedCentralPubMedGoogle Scholar
  110. Rowland O, Zheng H, Hepworth SR et al (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142:866–877PubMedCentralPubMedGoogle Scholar
  111. Rowland O, Lee R, Franke R et al (2007) The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett 581:3538–3544PubMedGoogle Scholar
  112. Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Ann Rev Plant Biol 59:683–707Google Scholar
  113. Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629–642PubMedCentralPubMedGoogle Scholar
  114. Seo PJ, Lee SB, Suh MC et al (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152PubMedCentralPubMedGoogle Scholar
  115. Shepherd T, Robertson GW, Griffiths DW et al (1995) Effects of environment on the composition of epicuticular wax from Kale and Swede. Phytochemistry 40:407–417Google Scholar
  116. Shephered T, Griffiths DW (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499Google Scholar
  117. Smirnova A, Leide J, Riederer M (2013) Deficiency in a very-long-chain fatty acid β-ketoacyl-CoA synthase (SlCER6) of tomato impairs microgametogenesis and causes floral organ fusion. Plant Physiol 161:196–209PubMedCentralPubMedGoogle Scholar
  118. Steinmüller D, Tevini M (1985) Action of ultraviolet radiation (UV-B) upon cuticular waxes in some crop plants. Planta 164:557–564PubMedGoogle Scholar
  119. Sturaro M, Hartings H, Schmelzer E et al (2005) Cloning and characterization of GLOSSY1, a maize gene involved in cuticle membrane and wax production. Plant Physiol 138:478–489PubMedCentralPubMedGoogle Scholar
  120. Suh MC, Samuels AL, Jetter R et al (2005) Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol 139:1649–1665PubMedCentralPubMedGoogle Scholar
  121. Todd J, Post-Beittenmiller D, Jaworski JG (1999) KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. Plant J 17:119–130PubMedGoogle Scholar
  122. Velasco R, Korfhage C, Salamini A et al (2002) Expression of the glossy2 gene of maize during plant development. Maydica 47:71–81Google Scholar
  123. Vogg G, Fischer S, Leide J et al (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid β-ketoacyl-CoA synthase. J Exp Bot 55:1401–1410PubMedGoogle Scholar
  124. von Wettstein-Knowles P (1971) The molecular phenotypes of the eceriferum mutants. In: Nilan RA (ed) Barley genetics II. Washington State University Press, Pulman, pp 146–193Google Scholar
  125. von Wettstein-Knowles P (1979) Genetics and biosynthesis of plant epicuticular waxes. In Advances in the Biochemistry and Physiology of Plant Lipids. In: Liljenberg C (ed) Appelqvist LA. Elsevier North-Holland Biornedical Press, Amsterdam, pp 1–26Google Scholar
  126. Wang Z, Guhling O, Yao R et al (2011) Two oxidosqualene cyclases responsible for biosynthesis of tomato fruit cuticular triterpenoids. Plant Physiol 155:540–552PubMedCentralPubMedGoogle Scholar
  127. Wang YH, Wan LY, Zhang LX et al (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78:275–288PubMedGoogle Scholar
  128. Weng H, Molina I, Shockey J et al (2010) Organ fusion and defective cuticle function in a lacs1 lacs2 double mutant of Arabidopsis. Planta 231:1089–1100PubMedGoogle Scholar
  129. Wu R, Li S, He S et al (2011) CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell 23:3392–3411PubMedCentralPubMedGoogle Scholar
  130. Xia Y, Nikolau BJ, Schnable PS (1996) Cloning and characterization of CER2, an Arabidopsis gene that affects cuticular wax accumulation. Plant Cell 8:1291–1304PubMedCentralPubMedGoogle Scholar
  131. Xu X, Dietrich CR, Delledonne M et al (1997) Sequence analysis of the cloned GLOSSY8 gene of maize suggests that it may code for a beta-ketoacyl reductase required for the biosynthesis of cuticular waxes. Plant Physiol 115:501–510PubMedCentralPubMedGoogle Scholar
  132. Xu X, Feng J, Lü S et al (2014) Leaf cuticular lipids on the Shandong and Yukon ecotypes of saltwater cress, Eutrema salsugineum, and their response to water deficiency and impact on cuticle permeability. Physiol Plant 151:446–458PubMedGoogle Scholar
  133. Xue Y, Xiao S, Kim J et al (2014) Arabidopsis membrane-associated acyl-CoA-binding protein ACBP1 is involved in stem cuticle formation. J Exp Bot 65:5473–5483PubMedCentralPubMedGoogle Scholar
  134. Yang M, Yang Q, Fu T et al (2011) Overexpression of the Brassica napus BnLAS gene in Arabidopsis affects plant development and increases drought tolerance. Plant Cell Rep 30:373–388PubMedGoogle Scholar
  135. Yeats TH, Rose JKC (2013) The formation and function of plant cuticles. Plant Physiol 163:5–29PubMedCentralPubMedGoogle Scholar
  136. Yu D, Ranathunge K, Huang H et al (2008) Wax Crystal-Sparse Leaf1 encodes a β-ketoacyl CoA synthase involved in biosynthesis of cuticular waxes on rice leaf. Planta 228:675–685PubMedGoogle Scholar
  137. Zhang J-Y, Broeckling CD, Blancaflor EB et al (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707PubMedGoogle Scholar
  138. Zhang J-Y, Broeckling CD, Sumner LW et al (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64:265–278PubMedGoogle Scholar
  139. Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17:1467–1481PubMedCentralPubMedGoogle Scholar
  140. Zhou LY, Ni ED, Yang JW et al (2013) Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance. PLoS One 8:e65139. doi: 10.1371/journal.pone.0065139 PubMedCentralPubMedGoogle Scholar
  141. Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice. Proc Natl Acad Sci USA 110:17790–17795PubMedCentralPubMedGoogle Scholar
  142. Zhu L, Guo J, Zhu J et al (2014) Enhanced expression of EsWAX1 improves drought tolerance with increased accumulation of cuticular wax and ascorbic acid in transgenic Arabidopsis. Plant Physiol Biochem 75:24–35PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Bioenergy Science and TechnologyChonnam National UniversityGwangjuKorea

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