The Plant Polyester Cutin: Biosynthesis, Structure, and Biological Roles

Annual Review of Plant Biology

Volumn 67, Issue , 2016, Pages 207-233

  Fich, Eric A ^a   Segerson, Nicholas A ^a   Rose, Jocelyn K C ^a  

^a Cornell University ^*  (United States)

Author keywords

Acyltransferase; Cuticle; Cutin synthase; Monoacylglycerol; Organogenesis; Polyester

Indexed keywords

CUTIN; FATTY ACID; LIPID; MEMBRANE LIPID; POLYESTER; SUBERIN;

BIOSYNTHESIS; CELL WALL; METABOLISM; PLANT; PLANT EPIDERMIS; PLANT LEAF; POLYMERIZATION;

CELL WALL; FATTY ACIDS; LIPIDS; MEMBRANE LIPIDS; PLANT EPIDERMIS; PLANT LEAVES; PLANTS; POLYESTERS; POLYMERIZATION;

EID: 84968817479     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043015-111929     Document Type: Review

References (144)

1. Agull óC,Collar C, Seoane E. 1984. Free and bound hydroxyl and carboxyl groups in the cutin of Quercus suber leaves. Phytochemistry 23:2059-60
2. Badenes SM, Lemos F, Cabral JMS. 2011. Performance of a cutinase membrane reactor for the production of biodiesel in organic media. Biotechnol. Bioeng. 108:1279-89
3. Bargel H, Neinhuis C. 2005. Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. J. Exp. Bot. 56:1049-60
4. Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, et al. 1998. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu. Rev. Ecol. Syst. 29:263-92
5. BCC Research. 2014. Global markets for enzymes in industrial applications. Rep. BIO030H, BCC Res., Wellesley, MA. http://www.bccresearch.com/market-research/biotechnology/enzymesindustrial-applications-bio030h.html
6. Beisson F, Li-Beisson Y, PollardM. 2012. Solving the puzzles of cutin and suberin polymer biosynthesis. Curr. Opin. Plant Biol. 15:329-37
7. Benavente J, Ramos-Barrado J, Heredia A. 1998. A study of the electrical behaviour of isolated tomato cuticular membranes and cutin by impedance spectroscopy measurements. Colloid Surf. A 140:333-38
8. Bessire M, Borel S, Fabre G, Carraca L, Efremova N, et al. 2011. A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23:1958-70
9. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, et al. 2007. A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 26:2158-68
10. Bird D, Beisson F, Brigham A, Shin J, Greer S, et al. 2007. Characterization of Arabidopsis ABCG11/ WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J. 52:485-98
11. Bolger A, Scossa F, Bolger ME, Lanz C,Maumus F, et al. 2014. The genome of the highly stress tolerant wild tomato species Solanum pennellii. Nat. Genet. 46:1034-38
12. Brissos V, Eggert T, Cabral JMS, Jaeger KE. 2008. Improving activity and stability of cutinase towards the anionic detergent AOT by complete saturation mutagenesis. Protein Eng. Des. Sel. 21:387-93
13. 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 25:4000-13
14. Buda GJ, Isaacson T, Matas AJ, Paolillo DJ, Rose JKC. 2009. Three-dimensional imaging of plant cuticle architecture using confocal scanning laser microscopy. Plant J. 60:378-85
15. Caldicott AB, Eglinton G. 1976. Cutin acids from bryophytes: an -l hydroxy alkanoic acid in two liverwort species. Phytochemistry 15:1139-43
16. Caldicott AB, Simoneit BRT, EglintonG. 1975. Alkanetriols in Psilophyte cutins. Phytochemistry 14:2223-28
17. Chamel A, Pineri M, EscoubesM. 1991. Quantitative determination of water sorption by plant cuticles. Plant Cell Environ. 14:87-95
18. Chassot C, Nawrath C, Metraux JP. 2007. Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 49:972-80
19. Chen S, Su L, Chen J, Wu J. 2013. Cutinase: characteristics, preparation, and application. Biotechnol. Adv. 31:1754-67
20. Chen S, Tong X, Woodard RW, Du G, Wu J, Chen J. 2008. Identification and characterization of bacterial cutinase. J. Biol. Chem. 283:25854-62
21. Cock ME, Graham LE. 1998. Structural similarities between surface layers of selected charophycean algae and bryophytes and the cuticles of vascular plants. Int. J. Plant Sci. 159:780-87
22. Deas AHB, Holloway PJ. 1977. The intermolecular structure of some plant cutins. In Lipids and Lipid Polymers in Higher Plants, ed. M Tevini, HK Lichtenthaler, pp. 293-99. Berlin: Springer
23. DeBono A, Yeats TH, Rose JKC, Bird D, Jetter R, et al. 2009. Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21:1230-38
24. Deshmukh AP, Simpson AJ, Hadad CM, Hatcher PG. 2005. Insights into the structure of cutin and cutan from Agave americana leaf cuticle using HRMAS NMR spectroscopy. Org. Geochem. 36:1072-85
25. Deshmukh AP, Simpson AJ, Hatcher PG. 2003. Evidence for crosslinking in tomato cutin using HRMAS NMR spectroscopy. Phytochemistry 64:1163-70
26. Dickman MB, Patil SS, Kolattukudy PE. 1982. Purification, characterization and role in infection of an extracellular cutinolytic enzyme from Colletotrichum gloeosporioides Penz. on Carica papaya L. Physiol. Plant Pathol. 20:333-47
27. Domínguez E, Cuartero J, Heredia A. 2011. An overview on plant cuticle biomechanics. Plant Sci. 181:77-84
28. Domínguez E, Heredia-Guerrero JA, Benátez JJ, Heredia A. 2010. Self-assembly of supramolecular lipid nanoparticles in the formation of plant biopolyester cutin. Mol. Biosyst. 6:948-50
29. Duan H, SchulerMA. 2005. Differential expression and evolution of the Arabidopsis CYP86A subfamily. Plant Physiol. 137:1067-81
30. Edwards D, Abbott GD, Raven JA. 1996. Cuticles of early land plants: a palaeoecophysiological evaluation. In Plant Cuticles: An Integrated Functional Approach, ed. G Kerstiens, pp. 1-32. Oxford, UK: BIOS
31. Fang X, Qiu F, Yan B, Wang H, Mort AJ, Stark RE. 2001. NMR studies of molecular structure in fruit cuticle polyesters. Phytochemistry 57:1035-42
32. Flipsen JAC, Appel ACM, van derHijdenHTWM, Verrips CT. 1998. Mechanism of removal of immobilized triacylglycerol by lipolytic enzymes in a sequential laundry wash process. Enzyme Microb. Technol. 23:274-80
33. Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, et al. 2005. Apoplastic polyesters in Arabidopsis surface tissues-a typical suberin and a particular cutin. Phytochemistry 66:2643-58
34. Garbow JR, Stark RE. 1990. Nuclear magnetic relaxation studies of plant polyester dynamics. 1. Cutin from limes. Macromolecules 23:2814-19
35. Giménez E, Dominguez E, Pineda B, Heredia A, Moreno V, et al. 2015. Transcriptional activity of the MADS box ARLEQUIN/ TOMATO AGAMOUS-LIKE1 gene is required for cuticle development of tomato fruit. Plant Physiol. 168:1036-48
36. Girard A-L, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, et al. 2012. Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3119-34
37. Goñi MA, Hedges JI. 1990. Potential applications of cutin-derived CuO reaction products for discriminating vascular plant sources in natural environments. Geochim. Cosmochim. Acta 54:3073-81
38. Graça J, Lamosa P. 2010. Linear and branched poly(-hydroxyacid) esters in plant cutins. J. Agric. Food Chem. 58:9666-74
39. Graça J, Schreiber L, Rodrigues J, Pereira H. 2002. Glycerol and glyceryl esters of -hydroxyacids in cutins. Phytochemistry 61:205-15
40. Grochulski P, Li Y, Schrag JD, Bouthillier F, Smith P, et al. 1993. Insights into interfacial activation from an open structure of Candida rugosa lipase. J. Biol. Chem. 268:12843-47
41. GuptaNS. 2014. Molecular decay of plant biopolymers. In Biopolymers: AMolecular Paleontology Approach, ed. N Landman, PJ Harries, pp. 1-16. Top. Geobiol. Vol. 38. Dordrecht, Neth.: Springer
42. Guzmán P, Fernández V, Garcá ML, Khayet M, Fernández A, Gil L. 2014. Localization of polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzyme-gold labelling. Plant Physiol. Biochem. 76:1-6
43. Guzmán P, Fernández V, Graça J, Cabral V, Kayali N, et al. 2014. Chemical and structural analysis of Eucalyptus globulus and E. camaldulensis leaf cuticles: a lipidized cell wall region. Front. Plant Sci. 5:481
44. Han JX, Clement JM, Li J, King A,Ng S, Jaworski JG. 2010. The cytochrome P450 CYP86A22 is a fatty acyl-CoA -hydroxylase essential for estolide synthesis in the stigma of Petunia hybrida. J. Biol. Chem. 285:3986-96
45. Hen-Avivi S, Lashbrooke J, Costa F, Aharoni A. 2014. Scratching the surface: genetic regulation of cuticle assembly in fleshy fruit. J. Exp. Bot. 65:4653-64
46. Holloway PJ. 1973. Cutins of Malus pumila fruits and leaves. Phytochemistry 12:2913-20
47. Holloway PJ. 1982. The chemical constitution of plant cutins. In The Plant Cuticle, ed. DF Cutler, KL Alvin, CE Price, pp. 45-85. London: Academic
48. HunnemanDH, EglintonG. 1972. The constituent acids of gymnosperm cutins. Phytochemistry 11:1989-2001
49. HwangBY. 2012. Directed evolution of cutinase using in vitro compartmentalization. Biotechnol. Bioprocess Eng. 17:500-505
50. Isaacson T, Kosma DK,Matas AJ, Buda GJ, He Y, et al. 2009. Cutin deficiency in the tomato fruit cuticle consistently affects resistance tomicrobial infection and biomechanical properties, but not transpirational water loss. Plant J. 60:363-77
51. Javelle M, Vernoud V, Depège-Fargeix N, Arnould C, Oursel D, 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. 154:273-86
52. Jeffree CE. 2006. The fine structure of the plant cuticle. In Biology of the Plant Cuticle, ed.MRiederer, C Müller, pp. 11-125. Annu. Plant Rev. Vol. 23. Oxford, UK: Blackwell
53. Jelsch C, Longhi S, Cambillau C. 1998. Packing forces in nine crystal forms of cutinase. Proteins 31:320-33
54. Kannangara R, BraniganC, Liu Y, Penfield T, Rao V, et al. 2007. The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19:1278-94
55. Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389:33-39
56. Kim H, Lee SB, Kim HJ, Min MK, Hwang I, Suh MC. 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. 53:1391-403
57. Kissinger M, Tuvia-Alkalai S, Shalom Y, Fallik E, Elkind Y, et al. 2005. Characterization of physiological and biochemical factors associated with postharvest water loss in ripe pepper fruit during storage. J. Am. Soc. Hortic. Sci. 130:735-41
58. Kolattukudy PE. 1977. Lipid polymers and associated phenols, their chemistry, biosynthesis, and role in pathogenesis. Recent Adv. Phytochem. 77:185-246
59. Kolattukudy PE. 1980. Biopolyester membranes of plants: cutin and suberin. Science 208:990-1000
60. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lu S, et al. 2009. The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol. 151:1918-29
61. Kosma DK,Murmu J, Razeq FM, Santos P, Bourgault R, et al. 2014. AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J. 80:216-29
62. Krolikowski KA, Victor JL, Wagler TN, Lolle SJ, Pruitt RE. 2003. Isolation and characterization of the Arabidopsis organ fusion gene HOTHEAD. Plant J. 35:501-11
63. Kurdyukov S, Faust A, Nawrath C, Bar S, Voisin D, et al. 2006. The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18:321-39
64. Kurdyukov S, Faust A, Trenkamp S, Bar S, Franke R, et al. 2006. Genetic and biochemical evidence for involvement of HOTHEAD in the synthesis of long-chain -,-dicarboxylic acids in the formation of extracellular matrix. Planta 224:315-29
65. KutscheraU,BergfeldR, Schopfer P. 1987. Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170:168-80
66. Kutschera U, Niklas KJ. 2007. The epidermal-growth-control theory of stem elongation: an old and new perspective. J. Plant Physiol. 164:1395-409
67. Lee SB, Go YS, Bae HJ, Park JH, Cho SH, et al. 2009. Disruption of glycosylphosphatidylinositolanchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol. 150:42-54
68. Leide J, Hildebrandt U, Reussing K, Riederer M, Vogg G. 2007. The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a -ketoacyl-coenzyme A synthase (LeCER6). Plant Physiol. 144:1667-79
69. Lendzian KJ, Nakajima A, Ziegler H. 1986. Isolation of cuticular membranes from various conifer needles. Trees 1:47-53
70. Li Y, Beisson F,Koo AJ, Molina I, PollardM,Ohlrogge J. 2007. Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. PNAS 104:18339-44
71. Li Y, Beisson F, Ohlrogge J, Pollard M. 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. 144:1267-77
72. Li-Beisson Y, Pollard M, Sauveplane V, Pinot F, Ohlrogge J, Beisson F. 2009. Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. PNAS 106:22008-13
73. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, et al. 2013. Acyl-lipid metabolism. Arabidopsis Book 8:e0133
74. Lisso J, Schr öder F, Schippers JHM,Müssig C. 2012. NFXL2modifies cuticle properties in Arabidopsis. Plant Signal. Behav. 7:551-55
75. Longhi S, CzjzekM, Lamzin V, Nicolas A, Cambillau C. 1997. Atomic resolution (1.0A ) crystal structure of Fusarium solani cutinase: stereochemical analysis. J. Mol. Biol. 268:779-99
76. Longhi S, Mannesse M, VerheijHM, De Haas GH, Egmond M, et al. 1997. Crystal structure of cutinase covalently inhibited by a triglyceride analogue. Protein Sci. 6:275-86
77. L? opez-Casado G, Matas AJ, Domínguez E, Cuartero J, Heredia A. 2007. Biomechanics of isolated tomato (Solanum lycopersicum L.) fruit cuticles: The role of the cutin matrix and polysaccharides. J. Exp. Bot. 58:3875-83
78. Lu S, Song T, Kosma DK, Parsons EP,RowlandO, Jenks MA. 2009. Arabidopsis CER8 encodesLONGCHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J. 59:553-64
79. Luque P, Bruque S, Heredia A. 1995. Water permeability of isolated cuticular membranes-a structural analysis. Arch. Biochem. Biophys. 317:417-22
80. Martin LBB, Rose JKC. 2014. There's more than one way to skin a fruit: formation and functions of fruit cuticles. J. Exp. Bot. 65:4639-51
81. Martinez C, Nicolas A, van TilbeurghH, EgloffMP, Cudrey C, et al. 1994. Cutinase, a lipolytic enzyme with a preformed oxyanion hole. Biochemistry 33:83-89
82. Matas AJ, Cobb ED, Bartsch JA, Paolillo DJ, Niklas KJ. 2004. Biomechanics and anatomy of Lycopersicon esculentum fruit peels and enzyme-treated samples. Am. J. Bot. 91:352-60
83. Matas AJ, Heredia A. 1999. Molecular dynamics modellization and simulation of water diffusion through plant cutin. Z. Naturforsch. 54:896-902
84. McCoy M. 2001. Novozymes emerges. Chem. Eng. News 79:23-25
85. Molina I, Ohlrogge JB, Pollard M. 2008. Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. Plant J. 53:437-49
86. Müller K, Levesque-Tremblay G, Fernandes A, Wormit A, Bartels S, et al. 2013. Overexpression of a pectin methylesterase inhibitor in Arabidopsis thaliana leads to altered growth morphology of the stem and defective organ separation. Plant Signal. Behav. 8:e26464
87. Murphy CA, Cameron JA, Huang SJ, Vinopal RT. 1996. Fusarium polycaprolactone depolymerase is cutinase. Appl. Environ. Microbiol. 62:456-60
88. Nadakuduti SS, Pollard M, Kosma DK, Allen C, Ohlrogge JB, Barry CS. 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. 159:945-60
89. Niklas KJ. 1976. Chemical examinations of some non-vascular paleozoic plants. Brittonia 28:113-37
90. Nip M, Tegelaar EW, de Leeuw JW, Schenck PA, Holloway PJ. 1986. A new non-saponifiable highly aliphatic and resistant biopolymer in plant cuticles. Naturwissenschaften 73:579-85
91. Norris RF, Bukovac MJ. 1968. Structure of the pear leaf cuticle with special reference to cuticular penetration. Am. J. Bot. 55:975-83
92. Orgell WH. 1955. The isolation of plant cuticle with pectic enzymes. Plant Physiol. 30:78-80
93. Oshima Y, Shikata M, Koyama T, Ohtsubo N, Mitsuda N, Ohme-Takagi M. 2013. MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25:1609-24
94. Panikashvili D, Shi JX, Schreiber L, Aharoni A. 2009. The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol. 151:1773-89
95. Panikashvili D, Shi JX, Schreiber L, Aharoni A. 2011. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 190:113-24
96. PollardM, Beisson F, Li Y,Ohlrogge JB. 2008. Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13:236-46
97. Pulsifer IP, Kluge S, RowlandO. 2012. Arabidopsis long-chain acyl-CoA synthetase 1 (LACS1), LACS2, and LACS3 facilitate fatty acid uptake in yeast. Plant Physiol. Biochem. 51:31-39
98. Rani SH, Krishna THA, Saha S, Negi AS, Rajasekharan R. 2010. Defective in cuticular ridges (DCR) of Arabidopsis thaliana, a gene associated with surface cutin formation, encodes a soluble diacylglycerol acyltransferase. J. Biol. Chem. 285:38337-47
99. Rautengarten C, Ebert B, Ouellet M, Nafisi M, Baidoo EEK, et al. 2012. Arabidopsis Deficient in Cutin Ferulate encodes a transferase required for feruloylation of-hydroxy fatty acids in cutin polyester. Plant Physiol. 158:654-65
100. Roussel A, Amara S, Nyyss öla A, Mateos-Diaz E, Blangy S, et al. 2014. A cutinase from Trichoderma reesei with a lid-covered active site and kinetic properties of true lipases. J. Mol. Biol. 22:3757-72
101. Rupasinghe SG, Duan H, Schuler MA. 2007. Molecular definitions of fatty acid hydroxylases in Arabidopsis thaliana. Proteins 68:279-93
102. Saladíe M, Matas AJ, Isaacson T, Jenks MA, Goodwin M, et al. 2007. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol. 144:1012-28
103. Samuels L, Kunst L, Jetter R. 2008. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu. Rev. Plant Biol. 59:683-707
104. Samuels L, McFarlane HE. 2012. Plant cell wall secretion and lipid traffic at membrane contact sites of the cell cortex. Protoplasma 249(Suppl. 1):S19-23
105. Sarrouh B, Santos TM, Miyoshi A, Dias R, Azevedo V. 2012. Up-to-date insight on industrial enzymes applications and global market. J. Bioprocess. Biotech. S4:002
106. SauveplaneV, Kandel S, Kastner PE, Ehlting J, CompagnonV, et al. 2009. Arabidopsis thaliana CYP77A4 is the first cytochrome P450 able to catalyze the epoxidation of free fatty acids in plants. FEBS J. 276:719-35
107. Savaldi-Goldstein S, Peto C, Chory J. 2007. The epidermis both drives and restricts plant shoot growth. Nature 446:199-202
108. Schnurr J, Shockey J, Browse J. 2004. The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629-42
109. Schönherr J, Bukovac MJ. 1973. Ion exchange properties of isolated tomato fruit cuticular membranes: exchange capacity, nature of fixed charges and cation selectivity. Planta 109:73-93
110. Schreiber L. 2010. Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci. 15:546-53
111. Schweizer P, Jeanguénat A, Métraux JP, Mösinger E. 1994. Plant protection by free cutin monomers in two cereal pathosystems. In Advances in Molecular Genetics of Plant-Microbe Interactions, ed. MJ Daniels, JA Downie, AE Osbourn, pp. 371-74. Curr. Plant Sci. Biotechnol. Agric. Vol. 21. Dordrecht, Neth.: Springer
112. Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM. 2011. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138-52
113. Serra O, Chatterjee S, Huang W, Stark RE. 2012. Mini-review: what nuclear magnetic resonance can tell us about protective tissues. Plant Sci. 195:120-24
114. Shi JX, Adato A, Alkan N, He Y, Lashbrooke J, et al. 2013. The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytol. 197:468-80
115. Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, et al. 2011. SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLOS Genet. 7:e1001388
116. Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, et al. 2000. Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12:721-38
117. Skamnioti P,Gurr SJ. 2007. Magnaporthe grisea cutinase2mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19:2674-89
118. Suh MC, Samuels AL, Jetter R, Kunst L, Pollard M, et al. 2005. Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol. 139:1649-65
119. Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, et al. 2010. Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. Plant Cell Physiol. 51:123-31
120. Takahashi Y, Tsubaki S, Sakamoto M, Watanabe S, Azuma J. 2012. Growth-dependent chemical and mechanical properties of cuticular membranes from leaves of Sonneratia alba. Plant Cell Environ. 35:1201-10
121. Tanaka T, Tanaka H, Machida C,WatanabeM,Machida Y. 2004. A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J. 37:139-46
122. Tang DZ, Simonich MT, Innes RW. 2007. Mutations in LACS2, a long-chain acyl-coenzyme A synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiol. 144:1093-103
123. Taylor TN, Taylor EL, Krings M. 2009. Paleobotany: The Biology and Evolution of Fossil Plants.New York: Elsevier. 2nd ed.
124. Tegelaar EW, de Leeuw JW, Largeau C, Derenne S, Schulten H-R, et al. 1989. Scope and limitation of several pyrolysis methods in the structural elucidation of a macromolecular plant constituent in the leaf cuticle of Agave americana L. J. Anal. Appl. Pyrol. 15:29-54
125. Tian S, Fang X, Wang W, Yu B, Cheng X, et al. 2008. Isolation and identification of oligomers from partial degradation of lime fruit cutin. J. Agric. Food Chem. 56:10318-25
126. Tsubaki S, Ozaki Y, Yonemori K, Azuma J. 2012. Mechanical properties of fruit-cuticular membranes isolated from 27 cultivars of Diospyros kaki Thunb. Food Chem. 132:2135-39
127. Van Kan JAL, van't Klooster JW, Wagemakers CAM, Dees DCT, van der Vlugt-Bergmans CJB. 1997. Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol. Plant-Microbe Interact. 10:30-38
128. Villena JF, Domínguez E, Heredia A. 2000. Monitoring biopolymers present in plant cuticles by FT-IR spectroscopy. J. Plant Physiol. 156:419-22
129. Villena JF, Domínguez E, Stewart D, Heredia A. 1999. Characterization and biosynthesis of nondegradable polymers in plant cuticles. Planta 208:181-87
130. Vishwanath SJ, Delude C, Domergue F, Rowland O. 2015. Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep. 34:573-86
131. Voisin D, Nawrath C, Kurdyukov S, Franke RB, Reina-Pinto JJ, et al. 2009. Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLOS Genet. 5:e1000703
132. Wang Y, Wan L, Zhang L, Zhang Z, Zhang H, 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. 78:275-88
133. Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, et al. 2001. Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid -hydroxylation in development. PNAS 98:9694-99
134. Weng H, Molina I, Shockey J, Browse J. 2010. Organ fusion and defective cuticle function in a lacs1 lacs2 double mutant of Arabidopsis. Planta 231:1089-100
135. Wu R, Li S, He S, Wassmann F, Yu C, et al. 2011. CFL1, a WW domain protein, regulates cuticle development bymodulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell 23:3392-411
136. Xiao FM, Goodwin SM, Xiao YM, Sun ZY, Baker D, et al. 2004. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 23:2903-13
137. Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, Ohlrogge J. 2010. A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. PNAS 107:12040-45
138. Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB. 2012. A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol. 160:638-652
139. Yeats TH, Huang W, Chatterjee S, Viart HMF, Clausen MH, et al. 2014. Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J. 77:667-75
140. Yeats TH, Martin LBB, Viart HMF, Isaacson T, He Y, et al. 2012. The identification of cutin synthase: formation of the plant polyester cutin. Nat. Chem. Biol. 8:609-11
141. Yeats TH, Rose JKC. 2013. The formation and function of plant cuticles. Plant Physiol. 163:5-20
142. Zhang Y, Chen S, He M, Wu J, Chen J, Wang Q. 2011. Effects of Thermobifida fusca cutinasecarbohydrate-binding module fusion proteins on cotton bioscouring. Biotechnol. Bioprocess Eng. 16:645-53
143. Zhou X, JenksMA, Liu J,Liu A, ZhangX. 2014. Overexpression of transcription factorOsWR2regulates wax and cutin biosynthesis in rice and enhances its tolerance to water deficit. PlantMol. Biol. Rep. 32:719-31
144. Zlotnik-Mazori T, Stark RE. 1988. Nuclear magnetic-resonance studies of cutin, an insoluble plant polyester. Macromolecules 21:2412-17