Scratching the surface: Genetic regulation of cuticle assembly in fleshy fruit

Journal of Experimental Botany

Volumn 65, Issue 16, 2014, Pages 4653-4664

  Hen Avivi, Shelly ^a   Lashbrooke, Justin ^a,b,c   Costa, Fabrizio ^b   Aharoni, Asaph ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b RESEARCH AND INNOVATION CENTRE   (Italy)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Cuticle; cutin; epidermis; fruit; regulation; tomato; transcription factor; wax

Indexed keywords

TRANSCRIPTION FACTOR; WAX;

CYTOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT EPIDERMIS; ULTRASTRUCTURE;

FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; PLANT EPIDERMIS; TRANSCRIPTION FACTORS; WAXES;

EID: 84905472364     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru225     Document Type: Review

References (118)

1. Abe M, Katsumata H, Komeda Y, Takahashi T. 2003. Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130, 635-643.
2. Adato A, Mandel T, Mintz-Oron S et al. 2009. Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genetics 5, 823-851.
3. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A. 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, 2463-2480.
4. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF. 2000. MADS-box gene evolution beyond flowers: Expression in pollen, endosperm, guard cells, roots and trichomes. The Plant Journal 24, 457-466.
5. Ambawat S, Sharma P, Yadav NR, Yadav RC. 2013. MYB transcription factor genes as regulators for plant responses: An overview. Physiology and Molecular Biology of Plants 19, 307-321.
6. Ballester AR, Molthoff J, de Vos R et al. 2010. Biochemical and molecular analysis of pink tomatoes: Deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiology 152, 71-84.
7. Barandoozi F, Talaie A. 2009. The effect of gibberellins on russeting in golden delicious apples. Journal of Horticulture and Forestry 1, 61-64.
8. Bargel H, Koch K, Cerman Z, Neinhuis C. 2006. Structure-function relationships of the plant cuticle and cuticular waxes-a smart material? Functional Plant Biology 33, 893-910.
9. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134, 1691-1701.
10. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto PeB, Angenent GC, de Maagd RA. 2012. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24, 4437-4451.
11. Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, Petétot JM, Métraux JP, Nawrath C. 2007. A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO Journal 26, 2158-2168.
12. Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP. 2007. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiology 143, 1347-1361.
13. Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA. 2011. The Sol Genomics Network (solgenomics.net): Growing tomatoes using Perl. Nucleic Acids Research 39, D1149-1155.
14. Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL. 2004. WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proceedings of the National Academy of Science, USA 101, 4706-4711.
15. Buxdorf K, Rubinsky G, Barda O, Burdman S, Aharoni A, Levy M. 2014. The transcription factor SlSHINE3 modulates defense responses in tomato plants. Plant Molecular Biology 84, 37-47.
16. Chassot C, Nawrath C, Métraux JP. 2007. Cuticular defects lead to full immunity to a major plant pathogen. The Plant Journal 49, 972-980.
17. Cho S, Jang S, Chae S, Chung KM, Moon YH, An G, Jang SK. 1999. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Molecular Biology 40, 419-429.
18. Colombo M, Masiero S, Vanzulli S, Lardelli P, Kater MM, Colombo L. 2008. AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. The Plant Journal 54, 1037-1048.
19. Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C. 2008. Overexpression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. The Plant Journal 53, 53-64.
20. de Folter S, Angenent GC. 2006. trans meets cis in MADS science. Trends in Plant Science 11, 224-231.
21. Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Mérillon JM, Hamdi S. 2006. Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiology 140, 499-511.
22. Depège-Fargeix N, Javelle M, Chambrier P, Frangne N, Gerentes D, Perez P, Rogowsky PM, Vernoud V. 2011. Functional characterization of the HD-ZIP IV transcription factor OCL1 from maize. Journal of Experimental Botany 62, 293-305.
23. Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G. 1996. The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. The Plant Journal 10, 393-402.
24. Di Stilio VS, Martin C, Schulfer AF, Connelly CF. 2009. An ortholog of MIXTA-like2 controls epidermal cell shape in flowers of Thalictrum. New Phytologist 183, 718-728.
25. Domínguez E, Cuartero J, Heredia A. 2011. An overview on plant cuticle biomechanics. Plant Science 181, 77-84.
26. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science 15, 573-581.
27. Egea-Cortines M, Saedler H, Sommer H. 1999. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO Journal 18, 5370-5379.
28. Evans MM, Passas HJ, Poethig RS. 1994. Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120, 1971-1981.
29. Finkelstein RR, Rock CD. 2002. Abscisic acid biosynthesis and response. The Arabidopsis Book 1, e0058.
30. Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L. 2005. Apoplastic polyesters in Arabidopsis surface tissues-a typical suberin and a particular cutin. Phytochemistry 66, 2643-2658.
31. Giese BN. 1975. Effects of light and temperature on the composition of epicuticular wax of barley leaves. Phytochemistry 14, 921-929.
32. Gilding EK, Marks MD. 2010. Analysis of purified glabra3-shapeshifter trichomes reveals a role for NOECK in regulating early trichome morphogenic events. The Plant Journal 64, 304-317.
33. Giménez E, Pineda B, Capel J, Antón MT, Atarés A, Pérez-Martín F, García-Sogo B, Angosto T, Moreno V, Lozano R. 2010. Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS One 5, e14427.
34. Giovannoni JJ. 2004. Genetic regulation of fruit development and ripening. Plant Cell 16 Suppl, S170-180.
35. Go YS, Kim H, Kim HJ, Suh MC. 2014. Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. Plant Cell doi: 10.1105/tpc.114.123307.
36. Gális I, Simek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K. 2006. A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. The Plant Journal 46, 573-592.
37. Gutterson N, Reuber TL. 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology 7, 465-471.
38. Hooker TS, Lam P, Zheng H, Kunst L. 2007. A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19, 904-913.
39. Hülskamp M, Mis?a S, Jürgens G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76, 555-566.
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. The Plant Journal 60, 363-377.
41. Ishida T, Hattori S, Sano R et al. 2007. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19, 2531-2543.
42. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A. 2009. TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant Journal 60, 1081-1095.
43. Jäger K, Fábián A, Tompa G, Deák C, Höhn M, Olmedilla A, Barnabás B, Papp I. 2011. New phenotypes of the drought-tolerant cbp20 Arabidopsis thaliana mutant have changed epidermal morphology. Plant Biology (Stuttg) 13, 78-84.
44. Jaillon O, Aury JM, Noel B et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467.
45. Javelle M, Vernoud V, Depège-Fargeix N, Arnould C, Oursel D, Domergue F, Sarda X, Rogowsky PM. 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 Physiology 154, 273-286.
46. Javelle M, Vernoud V, Rogowsky PM, Ingram GC. 2011. Epidermis: The formation and functions of a fundamental plant tissue. New Phytologist 189, 17-39.
47. Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G, Höfte H, Pauly M, Riechmann JL, Broun P. 2007. The transcription factor WIN1/SHN1 regulates Cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19, 1278-1294.
48. Kimbara J, Yoshida M, Ito H et al. 2013. Inhibition of CUTIN DEFICIENT 2 causes defects in cuticle function and structure and metabolite changes in tomato fruit. Plant Cell Physiology 54, 1535-1548.
49. Knoche M, Peschel S. 2007. Gibberellins increase cuticle deposition in developing tomato fruit. Plant Growth Regulation 51, 1-10.
50. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA. 2009. The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiology 151, 1918-1929.
51. Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M. 1999. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11, 1217-1226.
52. Kunst L, Samuels AL. 2003. Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research 42, 51-80.
53. Kurdyukov S, Faust A, Nawrath C et al. 2006. The epidermisspecific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18, 321-339.
54. Lam P, Zhao L, McFarlane HE, Aiga M, Lam V, Hooker TS, Kunst L. 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 Physiology 159, 1385-1395.
55. 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 beta-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiology 144, 1667-1679.
56. Lippold F, Sanchez DH, Musialak M, Schlereth A, Scheible WR, Hincha DK, Udvardi MK. 2009. AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiology 149, 1761-1772.
57. Lisso J, Schröder F, Schippers JH, Müssig C. 2012. NFXL2 modifies cuticle properties in Arabidopsis. Plant Signaling and Behavior 7, 551-555.
58. Liu J, Xu B, Hu L, Li M, Su W, Wu J, Yang J, Jin Z. 2009. Involvement of a banana MADS-box transcription factor gene in ethylene-induced fruit ripening. Plant Cell Reports 28, 103-111.
59. López-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. Journal of Experimental Botany 58, 3875-3883.
60. Lu P, Porat R, Nadeau JA, O'Neill SD. 1996. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8, 2155-2168.
61. Lü S, Zhao H, Des Marais DL et al. 2012. Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiology 159, 930-944.
62. Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES. 2009. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant Journal 59, 52-62.
63. Mahjoub A, Hernould M, Joubès J, Decendit A, Mars M, Barrieu F, Hamdi S, Delrot S. 2009. Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism. Plant Physiology and Biochemistry 47, 551-561.
64. Martin C, Paz-Ares J. 1997. MYB transcription factors in plants. Trends in Genetics 13, 67-73.
65. Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW. 1996. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253-1260.
66. Matas AJ, Yeats TH, Buda GJ et al. 2011. Tissue-and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23, 3893-3910.
67. Matus JT, Loyola R, Vega A, Peña-Neira A, Bordeu E, Arce-Johnson P, Alcalde JA. 2009. Post-veraison sunlight exposure induces MYBmediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. Journal of Experimental Botany 60, 853-867.
68. McCourt RM, Delwiche CF, Karol KG. 2004. Charophyte algae and land plant origins. Trends in Ecology & Evolution 19, 661-666.
69. Mehrtens F, Kranz H, Bednarek P, Weisshaar B. 2005. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology 138, 1083-1096.
70. Mintz-Oron S, Mandel T, Rogachev I et al. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology 147, 823-851.
71. Moose SP, Sisco PH. 1994. Glossy15 controls the epidermal juvenile-toadult phase transition in maize. Plant Cell 6, 1343-1355.
72. Moose SP, Sisco PH. 1996. Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes & Development 10, 3018-3027.
73. Ménard R, Verdier G, Ors M, Erhardt M, Beisson F, Shen WH. 2014. Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant Cell Physiology 55, 455-466.
74. Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, Ric De Vos CH, van Tunen AJ, Verhoeyen ME. 2001. Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nature Biotechnology 19, 470-474.
75. 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 Physiology 159, 945-960.
76. Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T. 2006. Characterization of the class IV homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiology 141, 1363-1375.
77. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165-185.
78. Nawrath C. 2006. Unraveling the complex network of cuticular structure and function. Current Opinion in Plant Biology 9, 281-287.
79. Neinhuis C, Barthlott W. 1997. Characterization and distribution of waterrepellent, self-cleaning plant surfaces. Annals of Botany 79, 667-677.
80. Ng M, Yanofsky MF. 2001. Function and evolution of the plant MADSbox gene family. Nature Reviews Genetics 2, 186-195.
81. Noda K, Glover BJ, Linstead P, Martin C. 1994. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369, 661-664.
82. 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, 1609-1624.
83. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. 2005. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132, 359-370.
84. Plett JM, Wilkins O, Campbell MM, Ralph SG, Regan S. 2010. Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth. The Plant Journal 64, 419-432.
85. Pollard M, Beisson F, Li Y, Ohlrogge JB. 2008. Building lipid barriers: Biosynthesis of cutin and suberin. Trends in Plant Science 13, 236-246.
86. Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, Huard C, Blée E, Mongrand S, Domergue F, Roby D. 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, 752-767.
87. Reina-Pinto JJ, Yephremov A. 2009. Surface lipids and plant defenses. Plant Physiology and Biochemistry 47, 540-549.
88. Rerie WG, Feldmann KA, Marks MD. 1994. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes & Development 8, 1388-1399.
89. Riederer M, Muller C. 2006. Biology of the Plant Cuticle. Blackwell.
90. Saladié M, Matas AJ, Isaacson T et al. 2007. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiology 144, 1012-1028.
91. Samuels L, Kunst L, Jetter R. 2008. Sealing plant surfaces: Cuticular wax formation by epidermal cells. Annual Review of Plant Biology 59, 683-707.
92. San-Bento R, Farcot E, Galletti R, Creff A, Ingram G. 2013. Epidermal identity is maintained by cell-cell communication via a universally active feedback loop in Arabidopsis thaliana. The Plant Journal 77, 46-58.
93. Schrick K, Nguyen D, Karlowski WM, Mayer KF. 2004. START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biology 5, R41.
94. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR. 1997. Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872-1874.
95. 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, 1138-1152.
96. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM. 2009. The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiology 151, 275-289.
97. Sessions A, Weigel D, Yanofsky MF. 1999. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. The Plant Journal 20, 259-263.
98. Shepherd T, Robertson GW, Griffiths DW, Birch ANE, Duncan G. 1995. Effects of environment on the composition of epicuticular wax from kale and swede. Phytochemistry 40, 407-417.
99. Shepherd T, Wynne Griffiths D. 2006. The effects of stress on plant cuticular waxes. New Phytologist 171, 469-499.
100. Shi JX, Adato A, Alkan N et al. 2013. The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytologist 197, 468-480.
101. Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, Schreiber L, Aharoni A. 2011. SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genetics 7, e1001388.
102. Shima Y, Kitagawa M, Fujisawa M, Nakano T, Kato H, Kimbara J, Kasumi T, Ito Y. 2013. Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN. Plant Molecular Biology 82, 427-438.
103. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. ThePlant Journal 50, 660-677.
104. Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology 4, 447-456.
105. Tominaga-Wada R, Iwata M, Sugiyama J, Kotake T, Ishida T, Yokoyama R, Nishitani K, Okada K, Wada T. 2009. The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. The Plant Journal 60, 564-574.
106. Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M. 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 beta-ketoacyl-CoA synthase. Journal of Experimental Botany 55, 1401-1410.
107. Vrebalov J, Pan IL, Arroyo AJ et al. 2009. Fleshy fruit expansion and ripening are regulated by the Tomato SHATTERPROOF gene TAGL1. Plant Cell 21, 3041-3062.
108. Walford SA, Wu Y, Llewellyn DJ, Dennis ES. 2011. GhMYB25-like: A key factor in early cotton fibre development. The Plant Journal 65, 785-797.
109. Walford SA, Wu Y, Llewellyn DJ, Dennis ES. 2012. Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. The Plant Journal 71, 464-478.
110. Wang ZY, Xiong L, Li W, Zhu JK, Zhu J. 2011. The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23, 1971-1984.
111. Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ. 2004. Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131, 6083-6091.
112. Xia Y, Yu K, Navarre D, Seebold K, Kachroo A, Kachroo P. 2010. The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiology 154, 833-846.
113. Xu ZS, Chen M, Li LC, Ma YZ. 2011. Functions and application of the AP2/ERF transcription factor family in crop improvement. Journal of Integrative Plant Biology 53, 570-585.
114. Yeats TH, Rose JK. 2013. The formation and function of plant cuticles. Plant Physiol 163, 5-20.
115. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY. 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). The Plant Journal 42, 689-707.
116. Zhang JY, Broeckling CD, Sumner LW, Wang ZY. 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 Molecular Biology 64, 265-278.
117. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409.
118. Zhu JK. 2002. Salt and drought stress signal transduction in plants. Annu Review of Plant Biology 53, 247-273.