Advertisement

Planta

, Volume 248, Issue 3, pp 715–727 | Cite as

Evolutionarily conserved function of the sacred lotus (Nelumbo nucifera Gaertn.) CER2-LIKE family in very-long-chain fatty acid elongation

  • Xianpeng Yang
  • Zhouya Wang
  • Tao Feng
  • Juanjuan Li
  • Longyu Huang
  • Baiming Yang
  • Huayan Zhao
  • Matthew A. Jenks
  • Pingfang Yang
  • Shiyou Lü
Original Article

Abstract

Main conclusion

Identification of NnCER2 and NnCER2-LIKE from Nelumbo nucifera, which are required for the very-long-chain fatty acid elongation, provides new evidence that CER2 proteins are evolutionarily conserved across the eudicots.

CER2-LIKE family proteins have been described as core components of the fatty acid elongase complex in Arabidopsis, maize, and rice, having specific function in synthesis of the C30 to C34 fatty acyl-CoA precursors of cuticular waxes. Little is known about the functional conservation in this gene family across species. In this study, two CER2-LIKE family proteins, NnCER2 and NnCER2-LIKE, were characterized from sacred lotus (Nelumbo nucifera), which is an ancient basal eudicot. The transcriptional expression of NnCER2 and NnCER2-LIKE was found in floating leaf blades, emergent petioles and vertical leaves, petals, and anthers. The NnCER2 and NnCER2-LIKE proteins were localized to the endoplasmic reticulum and nucleus. Overexpressing NnCER2 and NnCER2-LIKE in Arabidopsis led to alteration of cuticle wax structure in inflorescence stems, and this was associated with elevated 30, 32, and 34 carbon length wax compounds, and their derivatives. The different substrate specificities of NnCER2 and NnCER2-LIKE were explored using co-expression with AtCER6 in yeast cells. These findings provide clear evidence that the function of CER2 family proteins in producing VLCFAs is highly conserved across the eudicots.

Keywords

Arabidopsis thaliana CER2-LIKE proteins Cuticular wax Evolution Fatty acid elongase Localization Nelumbo nucifera NnCER2 Phylogeny 

Abbreviations

FAE

Fatty acid elongase

FAME

Fatty acid methyl ester

KCS

3-Ketoacyl-CoA synthase

VLCFA

Very-long-chain fatty acid

Notes

Acknowledgements

We thank Dr. Ljerka Kunst (University of British Columbia, Canada) for providing p42X yeast expressing vectors; Dr. Tao Feng for phylogenetic analysis and Chang Du (Wuhan Botanical Garden, Chinese Academy of Sciences) assistance of scanning electron microscopy and confocal imaging. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31570186 and 31770377).

Supplementary material

425_2018_2934_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1155 kb)
425_2018_2934_MOESM2_ESM.pdf (29 kb)
Supplementary material 2 (PDF 28 kb)
425_2018_2934_MOESM3_ESM.pdf (34 kb)
Supplementary material 3 (PDF 34 kb)
425_2018_2934_MOESM4_ESM.pdf (9 kb)
Supplementary material 4 (PDF 9 kb)

References

  1. Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7(12):2115–2127.  https://doi.org/10.1105/tpc.7.12.2115 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE T Automat Contr 19(6):716–723.  https://doi.org/10.1109/TAC.1974.1100705 CrossRefGoogle Scholar
  3. Barthlott W, Neinhuis C (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202(1):1–8.  https://doi.org/10.1007/s004250050096 CrossRefGoogle Scholar
  4. Barthlott W, Neinhuis C, Jetter R, Bourauel T, Riederer M (1996) Waterlily, poppy, or sycamore: on the systematic position of Nelumbo. Flora 191(2):169–174CrossRefGoogle Scholar
  5. Baudin A, Ozier-Kalogeropoulos O, Denouel A, Lacroute F, Cullin C (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21(14):3329–3330.  https://doi.org/10.1093/nar/21.14.3329 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52(1):110–129.  https://doi.org/10.1016/j.plipres.2012.10.002 CrossRefPubMedGoogle Scholar
  7. Bernard A, Domergue F, Pascal S, Jetter R, Renne C 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(7):3106–3118.  https://doi.org/10.1105/tpc.112.099796 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bourdenx B, Bernard A, Domergue F, Pascal S, Leger A 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(1):29–45.  https://doi.org/10.1104/pp.111.172320 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boyer JS, Wong SC, Farquhar GD (1997) CO2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiol 114(1):185–191.  https://doi.org/10.1104/pp.114.1.185 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brown JW, Walker JF, Smith SA (2017) Phyx: phylogenetic tools for unix. Bioinformatics 33(12):1886–1888.  https://doi.org/10.1093/bioinformatics/btx063 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Buda GJ, Barnes WJ, Fich EA, Park S, Yeats TH et al (2013) An ATP binding cassette transporter is required for cuticular wax deposition and desiccation tolerance in the moss Physcomitrella patens. Plant Cell 25(10):4000–4013.  https://doi.org/10.1105/tpc.113.117648 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Byng JW, Chase MW, Christenhusz MJM, Fay MF, Judd WS et al (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181(1):1–20.  https://doi.org/10.1111/boj.12385 CrossRefGoogle Scholar
  13. Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15(5):1170–1185.  https://doi.org/10.1105/tpc.010926 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743.  https://doi.org/10.1046/j.1365-313x.1998.00343.x CrossRefPubMedGoogle Scholar
  15. Dickson RC, Lester RL (1999) Yeast sphingolipids. Biochim Biophys Acta 1426(2):347–357.  https://doi.org/10.1016/S0304-4165(98)00135-4 CrossRefPubMedGoogle Scholar
  16. Edwards D (1993) Cells and tissues in the vegetative sporophytes of early land plants. New Phytol 125(2):225–247.  https://doi.org/10.1111/j.1469-8137.1993.tb03879.x CrossRefGoogle Scholar
  17. Ensikat HJ, Ditsche-Kuru P, Neinhuis C, Barthlott W (2011) Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Beilstein J Nanotechnol 2:152–161CrossRefGoogle Scholar
  18. Funato K, Vallee B, Riezman H (2002) Biosynthesis and trafficking of sphingolipids in the yeast Saccharomyces cerevisiae. Biochemistry 41(51):15105–15114.  https://doi.org/10.1021/bi026616d CrossRefPubMedGoogle Scholar
  19. Gietz RD, Schiestl RH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2(1):31–34.  https://doi.org/10.1038/nprot.2007.13 CrossRefPubMedGoogle Scholar
  20. Greer S, Wen M, Bird D, Wu X, Samuels L 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(3):653–667.  https://doi.org/10.1104/pp.107.107300 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Haslam TM, Kunst L (2013) Extending the story of very-long-chain fatty acid elongation. Plant Sci 210:93–107.  https://doi.org/10.1016/j.plantsci.2013.05.008 CrossRefPubMedGoogle Scholar
  22. Haslam TM, Manas-Fernandez A, Zhao L, Kunst L (2012) Arabidopsis ECERIFERUM2 is a component of the fatty acid elongation machinery required for fatty acid extension to exceptional lengths. Plant Physiol 160(3):1164–1174.  https://doi.org/10.1104/pp.112.201640 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Haslam TM, Haslam R, Thoraval D, Pascal S, Delude C et al (2015) ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiol 167(3):682–692.  https://doi.org/10.1104/pp.114.253195 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Haslam TM, Gerelle WK, Graham SW, Kunst L (2017) The unique role of the ECERIFERUM2-LIKE clade of the BAHD acyltransferase superfamily in cuticular wax metabolism. Plants (Basel).  https://doi.org/10.3390/plants6020023 CrossRefGoogle Scholar
  25. Hegebarth D, Buschhaus C, Joubès J, Thoraval D, Bird D et al (2017) Arabidopsis ketoacyl-CoA synthase 16 (KCS16) forms C36/C38 acyl precursors for leaf trichome and pavement surface wax. Plant Cell Environ 40(9):1761–1776.  https://doi.org/10.1111/pce.12981 CrossRefPubMedGoogle Scholar
  26. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Le SV (2017) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol.  https://doi.org/10.1093/molbev/msx281 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hulskamp M, Kopczak SD, Horejsi TF, Kihl BK, Pruitt RE (1995) Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J 8(5):703–714.  https://doi.org/10.1046/j.1365-313X.1995.08050703.x CrossRefPubMedGoogle Scholar
  28. Jetter R, Kunst L (2008) Plant surface lipid biosynthetic pathways and their utility for metabolic engineering of waxes and hydrocarbon biofuels. Plant J 54(4):670–683.  https://doi.org/10.1111/j.1365-313X.2008.03467.x CrossRefPubMedGoogle Scholar
  29. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al (2008) NCBI BLAST: a better web interface. Nucleic Acids Res.  https://doi.org/10.1093/nar/gkn201 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Joubès J, Raffaele S, Bourdenx B, Garcia C, Laroche-Traineau J et al (2008) The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modelling and expression profiling. Plant Mol Biol 67(5):547–566.  https://doi.org/10.1007/s11103-008-9339-z CrossRefPubMedGoogle Scholar
  31. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589.  https://doi.org/10.1038/nmeth.4285 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780.  https://doi.org/10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kim J, Jung JH, Lee SB, Go YS, Kim HJ 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(2):567–580.  https://doi.org/10.1104/pp.112.210450 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kondo S, Hori K, Sasaki-Sekimoto Y, Kobayashi A, Kato T et al (2016) Primitive extracellular lipid components on the surface of the charophytic alga Klebsormidium flaccidum and their possible biosynthetic pathways as deduced from the genome sequence. Front Plant Sci 7:952.  https://doi.org/10.3389/fpls.2016.00952 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12(6):721–727.  https://doi.org/10.1016/j.pbi.2009.09.009 CrossRefPubMedGoogle Scholar
  36. Lee SB, Suh MC (2015) Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species. Plant Cell Rep 34(4):557–572.  https://doi.org/10.1007/s00299-015-1772-2 CrossRefPubMedGoogle Scholar
  37. Lee SB, Jung SJ, Go YS, Kim HU, Kim JK et al (2009) 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(3):462–475.  https://doi.org/10.1111/j.1365-313X.2009.03973.x CrossRefPubMedGoogle Scholar
  38. Li F, Wu X, Lam P, Bird D, Zheng H 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(1):97–107.  https://doi.org/10.1104/pp.108.123471 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Li Y, Svetlana P, Yao JX, Li CS (2014) A review on the taxonomic, evolutionary and phytogeographic studies of the lotus plant (Nelumbonaceae: Nelumbo). Acta Geol Sin-Engl 88(4):1252–1261.  https://doi.org/10.1111/1755-6724.12287 CrossRefGoogle Scholar
  40. Lü S, Zhao H, Parsons EP, Xu C, Kosma DK 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(3):1079–1092.  https://doi.org/10.1104/pp.111.185132 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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(1):121–131.  https://doi.org/10.1046/j.1365-313X.1997.12010121.x CrossRefPubMedGoogle Scholar
  42. Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC 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(5):825–838.  https://doi.org/10.1105/tpc.11.5.825 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ming R, VanBuren R, Liu Y, Yang M, Han Y et al (2013) Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 14(5):R41.  https://doi.org/10.1186/gb-2013-14-5-r41 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mitchell AG, Martin CE (1997) Fah1p, a Saccharomyces cerevisiae cytochrome b5 fusion protein, and its Arabidopsis thaliana homolog that lacks the cytochrome b5 domain both function in the alpha-hydroxylation of sphingolipid-associated very long chain fatty acids. J Biol Chem 272(45):28281–28288.  https://doi.org/10.1074/jbc.272.45.28281 CrossRefPubMedGoogle Scholar
  45. Moon H, Chowrira G, Rowland O, Blacklock BJ, Smith MA et al (2004) A root-specific condensing enzyme from Lesquerella fendleri that elongates very-long-chain saturated fatty acids. Plant Mol Biol 56(6):917–927.  https://doi.org/10.1007/s11103-004-6235-z CrossRefPubMedGoogle Scholar
  46. Muhlhausen S, Kollmar M (2013) Whole genome duplication events in plant evolution reconstructed and predicted using myosin motor proteins. BMC Evol Biol 13:202.  https://doi.org/10.1186/1471-2148-13-202 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51(6):1126–1136.  https://doi.org/10.1111/j.1365-313X.2007.03212.x CrossRefPubMedGoogle Scholar
  48. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274.  https://doi.org/10.1093/molbev/msu300 CrossRefPubMedGoogle Scholar
  49. Pascal S, Bernard A, Sorel M, Pervent M, Vile D 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(5):733–746.  https://doi.org/10.1111/tpj.12060 CrossRefPubMedGoogle Scholar
  50. Preuss D, Lemieux B, Yen G, Davis RW (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Gene Dev 7(6):974–985.  https://doi.org/10.1101/gad.7.6.974 CrossRefPubMedGoogle Scholar
  51. Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490.  https://doi.org/10.1371/journal.pone.0009490 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Qin BX, Tang D, Huang J, Li M, Wu XR et al (2011) Rice OsGL1-1 is involved in leaf cuticular wax and cuticle membrane. Mol Plant 4(6):985–995.  https://doi.org/10.1093/mp/ssr028 CrossRefPubMedGoogle Scholar
  53. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69.  https://doi.org/10.1126/science.1150646 CrossRefPubMedGoogle Scholar
  54. Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 52(363):2023–2032.  https://doi.org/10.1093/jexbot/52.363.2023 CrossRefPubMedGoogle Scholar
  55. Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R et al (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142(3):866–877.  https://doi.org/10.1104/pp.106.086785 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rowland O, Lee R, Franke R, Schreiber L, Kunst L (2007) The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett 581(18):3538–3544.  https://doi.org/10.1016/j.febslet.2007.06.065 CrossRefPubMedGoogle Scholar
  57. Serra O, Soler M, Hohn C, Franke R, Schreiber L et al (2009) Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration. J Exp Bot 60(2):697–707.  https://doi.org/10.1093/jxb/ern314 CrossRefPubMedGoogle Scholar
  58. Smirnova A, Leide J, Riederer M (2013) Deficiency in a very-long-chain fatty acid beta-ketoacyl-coenzyme a synthase of tomato impairs microgametogenesis and causes floral organ fusion. Plant Physiol 161(1):196–209.  https://doi.org/10.1104/pp.112.206656 CrossRefPubMedGoogle Scholar
  59. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1(4):2019–2025.  https://doi.org/10.1038/nprot.2006.286 CrossRefPubMedGoogle Scholar
  60. Trenkamp S, Martin W, Tietjen K (2004) Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides. Proc Natl Acad Sci USA 101(32):11903–11908.  https://doi.org/10.1073/pnas.0404600101 CrossRefPubMedGoogle Scholar
  61. Tuominen LK, Johnson VE, Tsai CJ (2011) Differential phylogenetic expansions in BAHD acyltransferases across five angiosperm taxa and evidence of divergent expression among Populus paralogues. BMC Genomics 12:236.  https://doi.org/10.1186/1471-2164-12-236 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Velasco R, Korfhage C, Salamini A, Tacke E, Schmitz J et al (2002) Expression of the glossy2 gene of maize during plant development. Maydica 47(2):71–81Google Scholar
  63. Wang Y, Fan GY, Liu YM, Sun FM, Shi CC et al (2013) The sacred lotus genome provides insights into the evolution of flowering plants. Plant J 76(4):557–567.  https://doi.org/10.1111/tpj.12313 CrossRefPubMedGoogle Scholar
  64. Wang X, Guan Y, Zhang D, Dong X, Tian L et al (2017) A beta-ketoacyl-CoA synthase is involved in rice leaf cuticular wax synthesis and requires a CER2-LIKE protein as a cofactor. Plant Physiol 173(2):944–955.  https://doi.org/10.1104/pp.16.01527 CrossRefPubMedGoogle Scholar
  65. Wood AJ (2005) Eco-physiological adaptations to limited water environments. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress. Wiley-Blackwell, Oxford, pp 1–13Google Scholar
  66. Xia Y, Nikolau BJ, Schnable PS (1997) Developmental and hormonal regulation of the Arabidopsis CER2 gene that codes for a nuclear-localized protein required for the normal accumulation of cuticular waxes. Plant Physiol 115(3):925–937CrossRefGoogle Scholar
  67. Xu L, Zeisler V, Schreiber L, Gao J, Hu K et al (2017) Overexpression of the novel Arabidopsis gene At5g02890 alters inflorescence stem wax composition and affects phytohormone homeostasis. Front Plant Sci 8:68.  https://doi.org/10.3389/fpls.2017.00068 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Xue JH, Dong WP, Cheng T, Zhou SL (2012) Nelumbonaceae: systematic position and species diversification revealed by the complete chloroplast genome. J Syst Evol 50(6):477–487.  https://doi.org/10.1111/j.1759-6831.2012.00224.x CrossRefGoogle Scholar
  69. Yang XP, Zhao HY, Kosma DK, Tomasi P, Dyer JM et al (2017) The acyl desaturase CER17 is involved in producing wax unsaturated primary alcohols and cutin monomers. Plant Physiol 173(2):1109–1124.  https://doi.org/10.1104/pp.16.01956 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yeats TH, Rose JK (2013) The formation and function of plant cuticles. Plant Physiol 163(1):5–20.  https://doi.org/10.1104/pp.113.222737 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.Changchun Guoxin Modern Agricultural Science and Technology Development Co., Ltd.ChangchunChina
  3. 3.Applied Biotechnology CenterWuhan Institute of BioengineeringWuhanChina
  4. 4.Division of Plant and Soil SciencesWest Virginia UniversityMorgantownUSA
  5. 5.Sino-Africa Joint Research CenterChinese Academy of SciencesWuhanChina

Personalised recommendations