Abstract
Based on the Arabidopsis model of production and transport of cuticular components in silico analysis of apple EST and genomic sequences identified candidate genes potentially involved in these processes. Expression profiling of the selected genes in apple leaves and fruit tissues at the stage of full tree ripeness showed them to be active in fruit skin, in some cases in a tissue-specific manner. Apart from sequence conservation, characteristic transcript profiles make these genes likely participants of fruit cuticle formation. Genes with putative functions in the fatty acid elongase complex, wax and cutin modifications, transport and a potential regulator were identified this way. Activity of some of the putative genes can be correlated with the known wax composition of the ‘Florina’ cultivar. Year-to-year and cultivar specific variations in expression of some of these genes indicate plasticity of lipid biosynthetic pathways in apple. Coordinated expression of several cuticle associated genes further supports their proposed role in cuticular lipid metabolism. The presented data suggest conservation of some key determinants of biosynthesis and transport of cuticular lipids between Arabidopsis epidermis and apple fruit skin.
Similar content being viewed by others
References
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
Albert Z, Deák C, Miskó A, Tóth M, Papp I (2011a) Development of cDNA normalization system and preliminary transcription analysis of KCS genes in apple tissues. Acta Univ Agric et Silvic Mendel Brun LIX 3:9–12
Albert Z, Ivanics B, Molnár A, Deák C, Miskó A, Tóth M, Papp I (2011b) Characterization of gene expression in apple, connected potentially to cuticular wax production. Acta Biol Szegediensis 55(1):59–61
Alkio M, Jonas U, Sprink T, van Nocker S, Knoche M (2012) Identification of putative candidate genes involved in cuticle formation in Prunus avium (sweet cherry) fruit. Ann Bot 110(1):101–112
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Asif M, Trivedi P, Solomos T, Tucker M (2006) Isolation of high-quality RNA from apple (Malus domestica) fruit. J Agric Food Chem 54:5227–5229
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(413):1049–1060
Belding RD, Blankenship SM, Young E, Leidy RB (1998) Composition and variability of epicuticular waxes in apple cultivars. J Am Soc Hortic Sci 123(3):348–356
Bernard A, Domergue F, Pascal S, Jetter R, Renne C, Faure JD, Haslam RP, Napier JA, Lessire R, Joubès J (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
Bourdenx B, Bernard A, Domergue F, Pascal S, Léger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubès J (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
Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101(13):4706–4711
Buschhaus C, Jetter R (2011) Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces? J Exp Bot 62(3):841–853
Costa F, Alba R, Schouten H, Soglio V, Gianfranceschi L, Serra S, Musacchi S, Sansavini S, Costa G, Fei Z, Giovannoni J (2010) Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol 10:229
Deák C, Jäger K, Fábián A, Papp I (2010) Low and high (pszi) ways from post-transcriptional RNA regulation to drought tolerance. Plant Signal Behav 5(12):1539–1542
DeBono A, Yeats TH, Rose JK, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21(4):1230–1238
Domínguez AE, López-Casado BG, Jesús Cuartero AC, Heredia A (2008) Development of fruit cuticle in cherry tomato (Solanum lycopersicum). Funct Plant Biol 35(5):403–411
Hu X, Zhang Z, Li W, Fu Z, Zhang S, Xu P (2009) cDNA cloning and expression analysis of a putative decarbonylase TaCer1 from wheat (Triticum aestivum L.). Acta Physiol Plant 31:1111–1118
Isaacson T, Kosma DK, Matas AJ, Buda GJ, He Y, Yu B, Pravitasari A, Batteas JD, Stark RE, Jenks MA, Rose JK (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(2):363–377
Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16
Jenks MA, Eigenbrode SD, Lemieux B (2002) Cuticular waxes of Arabidopsis. In: The Arabidopsis book. The American Society of Plant Biologists, vol 1, p e0016. doi:10.1199/tab.0016
Joubés J, Raffaele S, Bourdenx B, Garcia C, Laroche-Traineau J, Moreau P, Domergue F, Lessire R (2008) The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modeling and expression profiling. Plant Mol Biol 67:547–566
Ju Z, Bramlage WJ (2001) Developmental changes of cuticular constituents and their association with ethylene during fruit ripening in ‘Delicious’ apples. Postharvest Biol Technol 21(3):257–263
Jung S, Staton M, Lee T, Blenda A, Svancara R, Abbott A, Main D (2008) GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acids Res 36(Database issue):D1034–D1040
Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12:721–727
Lee Y-P, Yu G-H, Seo YS, Han SE, Choi Y-O, Kim D, Mok I-G, Kim WT, Sung S-K (2007) Microarray analysis of apple gene expression engaged in early fruit development. Plant Cell Rep 26:917–926
Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (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 59:553–564
Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, Ponnala L, Adato A, Aharoni A, Stark R, Fernie AR, Fei Z, Giovannoni JJ, Rose JK (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(11):3893–3910
Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A, Aharoni A (2008) Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol 147(2):823–851
Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9:281–287
Panikashvili D, Aharoni A (2008) ABC-type transporters and cuticle assembly. Linking function to polarity in epidermis cells. Plant Signal Behav 3(10):806–809
Park S, Sugimoto N, Larson MD, Beaudry R, van Nocker S (2006) Identification of genes with potential roles in apple fruit development and biochemistry through large-scale statistical analysis of expressed sequence tags. Plant Physiol 141(3):811–824
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13(5):236–246
Richardson A, Boscari A, Schreiber L, Kerstiens G, Jarvis M, Herzyk P, Fricke W (2007) Cloning and expression analysis of candidate genes involved in wax deposition along the growing barley (Hordeum vulgare) leaf. Planta 226(6):1459–1473
Rowland O, Zheng H, Hepworth SH, Lam P, Jetter R, Kunst L (2006) CER4 encodes an alcohol-forming fatty acyl-Coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142:866–877
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Ann Rev Plant Biol 59:683–707
Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629–642
Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15(10):546–553
Seo PJ, Park C-M (2011) Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signal Behav 6(7):1043–1045
Shockey JM, Martin S, Fulda MS, Browse JA (2002) Arabidopsis contains nine long-chain acyl-Coenzyme A synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol 129(4):1710–1722
Soglio V, Costa F, Molthoff JW, Weemen-Hendriks WMJ, Schouten HJ, Gianfranceschi L (2009) Transcription analysis of apple fruit development using cDNA microarrays. Tree Genet Genomes 5:685–698
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42(10):833–839
Verardo G, Pagani E, Geatti P, Martinuzzi P (2003) A thorough study of the surface wax of apple fruits. Anal Bioanal Chem 376:659–667
Veraverbeke EA, Lammertyn J, Saevels S, Nicolaï BM (2001a) Changes in chemical wax composition of three different apple (Malus domestica Borkh.) cultivars during storage. Postharvest Biol Technol 23:197–208
Veraverbeke EA, Van Bruaene N, Van Oostveldt P, Nicolaï BM (2001b) Non destructive analysis of the wax layer of apple (Malus domestica Borkh.) by means of confocal laser scanning microscopy. Planta 213(4):525–533
Veraverbeke EA, Verboven P, Van Oostveldt P, Nicolaï BM (2003) Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. mitis (Wallr.)) during storage: part 2. Model simulations and practical applications. Postharvest Biol Technol 30:89–97
Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Yephremov A (2001) Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid ϖ-hydroxylation in development. Proc Natl Acad Sci USA 98(17):9694–9699
Yephremov A, Schreiber L (2005) The dark side of the cell wall: molecular genetics of plant cuticle. Plant Biosyst 139(1):74–79
Acknowledgments
We would like to thank to Peter Symmons for critical reading of the manuscript and to Gábor Solymossy for his help in light microscopy. The work was funded by the TÁMOP-4.2.1/B-09/1/KMR-2010-0005 grant from the National Development Agency of Hungary, Zs.A. was supported by the Doctoral Council of Life Sciences of Corvinus University of Budapest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Albert, Z., Ivanics, B., Molnár, A. et al. Candidate genes of cuticle formation show characteristic expression in the fruit skin of apple. Plant Growth Regul 70, 71–78 (2013). https://doi.org/10.1007/s10725-012-9779-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-012-9779-y