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Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall

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Legay, Sylvain Guerriero, Gea Deleruelle, Amélie [UCL] Lateur, Marc Evers, Danièle Hausman, Jean-Francois

Russeting, a commercially important defect in the exocarp of apple (Malus × domestica), is mainly characterized by the accumulation of suberin on the inner part of the cell wall of the outer epidermal cell layers. However, knowledge on the underlying genetic components triggering this trait remains sketchy. Bulk transcriptomic profiling was performed on the exocarps of three russeted and three waxy apple varieties. This experimental design was chosen to lower the impact of genotype on the obtained results. Validation by qPCR was carried out on representative genes and additional varieties. Gene ontology enrichment revealed a repression of lignin and cuticle biosynthesis genes in russeted exocarps, concomitantly with an enhanced expression of suberin deposition, stress responsive, primary sensing, NAC and MYB-family transcription factors, and specific triterpene biosynthetic genes. Notably, a strong correlation (R2 = 0.976) between the expression of a MYB93-like transcription factor and key suberin biosynthetic genes was found. Our results suggest that russeting is induced by a decreased expression of cuticle biosynthetic genes, leading to a stress response which not only affects suberin deposition, but also the entire structure of the cell wall. The large number of candidate genes identified in this study provides a solid foundation for further functional studies.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2015
Language Anglais
Journal information "Plant Molecular Biology" - Vol. 88, p. 21-40 (2015)
Peer reviewed yes
Publisher Springer Nature
issn 0167-4412
e-issn 1573-5028
Publication status Publié
Affiliations UCL - SST/ISV - Institut des sciences de la vie
UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
Keywords Agronomy and Crop Science ; Plant Science ; Genetics ; General Medicine
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  1. Andre Christelle M., Greenwood Jeffrey M., Walker Edward G., Rassam Maysoon, Sullivan Michael, Evers Danièle, Perry Nigel B., Laing William A., Anti-Inflammatory Procyanidins and Triterpenes in 109 Apple Varieties, 10.1021/jf302809k
  2. Andre Christelle M., Larsen Lesley, Burgess Elaine J., Jensen Dwayne J., Cooney Janine M., Evers Danièle, Zhang Jingli, Perry Nigel B., Laing William A., Unusual Immuno-Modulatory Triterpene-Caffeates in the Skins of Russeted Varieties of Apples and Pears, 10.1021/jf305190e
  3. Baggerly K. A., Deng L., Morris J. S., Aldaz C. M., Differential expression in SAGE: accounting for normal between-library variation, 10.1093/bioinformatics/btg173
  4. Balbontin C, Ayala H, Rubilar J, Cote J, Figueroa CR (2014) Transcriptional analysis of cell wall and cuticle related genes during fruit development of two sweet cherry cultivars with contrasting levels of cracking tolerance. Chilean, J Agric Res 74
  5. Barabdoozi FN, Talaie A (2009) The effect of gibberellins on russeting in Golden Delicious apples. J Hortic Sci For 1:061–064
  6. Baxter Ivan, Hosmani Prashant S., Rus Ana, Lahner Brett, Borevitz Justin O., Muthukumar Balasubramaniam, Mickelbart Michael V., Schreiber Lukas, Franke Rochus B., Salt David E., Root Suberin Forms an Extracellular Barrier That Affects Water Relations and Mineral Nutrition in Arabidopsis, 10.1371/journal.pgen.1000492
  7. Beisson F., Li Y., Bonaventure G., Pollard M., Ohlrogge J. B., The Acyltransferase GPAT5 Is Required for the Synthesis of Suberin in Seed Coat and Root of Arabidopsis, 10.1105/tpc.106.048033
  8. Beisson Fred, Li-Beisson Yonghua, Pollard Mike, Solving the puzzles of cutin and suberin polymer biosynthesis, 10.1016/j.pbi.2012.03.003
  9. Belkhadir Youssef, Subramaniam Rajagopal, Dangl Jeffery L, Plant disease resistance protein signaling: NBS–LRR proteins and their partners, 10.1016/j.pbi.2004.05.009
  10. Benveniste Irène, Tijet Nathalie, Adas Fadi, Philipps Gabriel, Salaün Jean-Pierre, Durst Francis, CYP86A1 fromArabidopsis thalianaEncodes a Cytochrome P450-Dependent Fatty Acid Omega-Hydroxylase, 10.1006/bbrc.1998.8156
  11. Bernards Mark A, Demystifying suberin, 10.1139/b02-017
  12. Bernards Mark A., Razem Fawzi A., The poly(phenolic) domain of potato suberin: a non-lignin cell wall bio-polymer, 10.1016/s0031-9422(01)00046-2
  13. Bernards Mark A., Lopez Marta L., Zajicek Jaroslav, Lewis Norman G., Hydroxycinnamic Acid-derived Polymers Constitute the Polyaromatic Domain of Suberin, 10.1074/jbc.270.13.7382
  14. Bernards Mark A., Susag Lyndia M., Bedgar Diana L., Anterola Aldwin M., Lewis Norman G., Induced phenylpropanoid metabolism during suberization and lignification: a comparative analysis, 10.1016/s0176-1617(00)80002-4
  15. Bindea Gabriela, Mlecnik Bernhard, Hackl Hubert, Charoentong Pornpimol, Tosolini Marie, Kirilovsky Amos, Fridman Wolf-Herman, Pagès Franck, Trajanoski Zlatko, Galon Jérôme, ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks, 10.1093/bioinformatics/btp101
  16. Bindea Gabriela, Galon Jérôme, Mlecnik Bernhard, CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data, 10.1093/bioinformatics/btt019
  17. Boher Pau, Serra Olga, Soler Marçal, Molinas Marisa, Figueras Mercè, The potato suberin feruloyl transferase FHT which accumulates in the phellogen is induced by wounding and regulated by abscisic and salicylic acids, 10.1093/jxb/ert163
  18. Bonaventure G., Disruption of the FATB Gene in Arabidopsis Demonstrates an Essential Role of Saturated Fatty Acids in Plant Growth, 10.1105/tpc.008946
  19. Bourquin V., Xyloglucan Endotransglycosylases Have a Function during the Formation of Secondary Cell Walls of Vascular Tissues, 10.1105/tpc.007773
  20. Brendolise Cyril, Yauk Yar-Khing, Eberhard Ellen D., Wang Mindy, Chagne David, Andre Christelle, Greenwood David R., Beuning Lesley L., An unusual plant triterpene synthase with predominant α-amyrin-producing activity identified by characterizing oxidosqualene cyclases from Malus × domestica : Oxidosqualene cyclases from apple, 10.1111/j.1742-4658.2011.08175.x
  21. Bustin S. A., Benes V., Garson J. A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M. W., Shipley G. L., Vandesompele J., Wittwer C. T., The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments, 10.1373/clinchem.2008.112797
  22. Cassan-Wang Hua, Goué Nadia, Saidi Mohammed N., Legay Sylvain, Sivadon Pierre, Goffner Deborah, Grima-Pettenati Jacqueline, Identification of novel transcription factors regulating secondary cell wall formation in Arabidopsis, 10.3389/fpls.2013.00189
  23. Compagnon V., Diehl P., Benveniste I., Meyer D., Schaller H., Schreiber L., Franke R., Pinot F., CYP86B1 Is Required for Very Long Chain  -Hydroxyacid and  , -Dicarboxylic Acid Synthesis in Root and Seed Suberin Polyester, 10.1104/pp.109.141408
  24. Cosgrove Daniel J., Growth of the plant cell wall, 10.1038/nrm1746
  25. Curry EA (2009) Growth-induced microcracking and repair mechanisms of fruit cuticles. Proceedings of the SEM annual conference
  26. De Vos Martin, Denekamp Marten, Dicke Marcel, Vuylsteke Marnik, Van Loon LC, Smeekens Sjef CM, Pieterse Corne, TheArabidopsis thalianaTranscription Factor AtMYB102 Functions in Defense Against The Insect HerbivorePieris rapae, 10.4161/psb.1.6.3512
  27. Devoghalaere Fanny, Doucen Thomas, Guitton Baptiste, Keeling Jeannette, Payne Wendy, Ling Toby, Ross John, Hallett Ian, Gunaseelan Kularajathevan, Dayatilake GA, Diak Robert, Breen Ken C, Tustin D Stuart, Costes Evelyne, Chagné David, Schaffer Robert, David Karine, A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control, 10.1186/1471-2229-12-7
  28. Faust M, Shear C (1972) Russeting of apples, an interpretative review. HortScience 7:233–235
  29. Fornalé Silvia, Sonbol Fathi-Mohamed, Maes Tamara, Capellades Montserrat, Puigdomènech Pere, Rigau Joan, Caparrós-Ruiz David, Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors, 10.1007/s11103-006-9058-2
  30. Franke Rochus, Schreiber Lukas, Suberin — a biopolyester forming apoplastic plant interfaces, 10.1016/j.pbi.2007.04.004
  31. Franke Rochus, Briesen Isabel, Wojciechowski Tobias, Faust Andrea, Yephremov Alexander, Nawrath Christiane, Schreiber Lukas, Apoplastic polyesters in Arabidopsis surface tissues – A typical suberin and a particular cutin, 10.1016/j.phytochem.2005.09.027
  32. Fukushima Ery O., Seki Hikaru, Ohyama Kiyoshi, Ono Eiichiro, Umemoto Naoyuki, Mizutani Masaharu, Saito Kazuki, Muranaka Toshiya, CYP716A Subfamily Members are Multifunctional Oxidases in Triterpenoid Biosynthesis, 10.1093/pcp/pcr146
  33. Gasic Ksenija, Hernandez Alvaro, Korban Schuyler S., RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction, 10.1007/bf02772687
  34. Gildemacher Peter, Heijne Bart, Silvestri Massimiliano, Houbraken Jos, Hoekstra Ellen, Theelen Bart, Boekhout Teun, Interactions between yeasts, fungicides and apple fruit russeting, 10.1111/j.1567-1364.2006.00109.x
  35. Gou J.-Y., Yu X.-H., Liu C.-J., A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis, 10.1073/pnas.0905555106
  36. Gra�a Jos�, Pereira Helena, Methanolysis of bark suberins: analysis of glycerol and acid monomers, 10.1002/(sici)1099-1565(200001/02)11:1<45::aid-pca481>3.0.co;2-8
  37. Graça José, Pereira Helena, Suberin Structure in Potato Periderm:  Glycerol, Long-Chain Monomers, and Glyceryl and Feruloyl Dimers, 10.1021/jf0006123
  38. Graça José, Santos Sara, Suberin: A Biopolyester of Plants' Skin, 10.1002/mabi.200600218
  39. Hellemans Jan, Mortier Geert, De Paepe Anne, Speleman Frank, Vandesompele Jo, 10.1186/gb-2007-8-2-r19
  40. Höfer Rene, Briesen Isabel, Beck Martina, Pinot Franck, Schreiber Lukas, Franke Rochus, The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis, 10.1093/jxb/ern101
  41. Hussey Steven G, Mizrachi Eshchar, Spokevicius Antanas V, Bossinger Gerd, Berger Dave K, Myburg Alexander A, SND2, a NAC transcription factor gene, regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus, 10.1186/1471-2229-11-173
  42. Jung Yu-Jin, Lee Myung-Chul, Kang Kwon-Kyoo, A transcription factor "OsNAC075" is essential for salt resistance in rice (Oryza sativa L.), 10.5010/jpb.2011.38.1.094
  43. Khanal B. P., Grimm E., Knoche M., Russeting in apple and pear: a plastic periderm replaces a stiff cuticle, 10.1093/aobpla/pls048
  44. Kosma Dylan K., Murmu Jhadeswar, Razeq Fakhria M., Santos Patricia, Bourgault Richard, Molina Isabel, Rowland Owen, AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types, 10.1111/tpj.12624
  45. Kurdyukov Sergey, Faust Andrea, Trenkamp Sandra, Bär Sascha, Franke Rochus, Efremova Nadia, Tietjen Klaus, Schreiber Lukas, Saedler Heinz, Yephremov Alexander, Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain α-,ω-dicarboxylic fatty acids and formation of extracellular matrix, 10.1007/s00425-005-0215-7
  46. Lewis D. R., Ramirez M. V., Miller N. D., Vallabhaneni P., Ray W. K., Helm R. F., Winkel B. S. J., Muday G. K., Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks, 10.1104/pp.111.172502
  47. Li Yonghua, Beisson Fred, The biosynthesis of cutin and suberin as an alternative source of enzymes for the production of bio-based chemicals and materials, 10.1016/j.biochi.2009.03.016
  48. Li Y., Beisson F., Koo A. J. K., Molina I., Pollard M., Ohlrogge J., Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers, 10.1073/pnas.0706984104
  49. Li F., Wu X., Lam P., Bird D., Zheng H., Samuels L., Jetter R., Kunst L., Identification of the Wax Ester Synthase/Acyl-Coenzyme A:Diacylglycerol Acyltransferase WSD1 Required for Stem Wax Ester Biosynthesis in Arabidopsis, 10.1104/pp.108.123471
  50. Liang Mingxiang, Davis Elizabeth, Gardner Dale, Cai Xiaoning, Wu Yajun, Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis, 10.1007/s00425-006-0300-6
  51. Li-Beisson Y., Pollard M., Sauveplane V., Pinot F., Ohlrogge J., Beisson F., Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester, 10.1073/pnas.0909090106
  52. Liepman Aaron H., Wightman Raymond, Geshi Naomi, Turner Simon R., Scheller Henrik Vibe, Arabidopsis - a powerful model system for plant cell wall research, 10.1111/j.1365-313x.2010.04161.x
  53. Lulai E.C, Corsini D.L, Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosumL.) wound-healing, 10.1006/pmpp.1998.0179
  54. Lulai Edward C., Suttle Jeffrey C., The involvement of ethylene in wound-induced suberization of potato tuber (Solanum tuberosum L.): a critical assessment, 10.1016/j.postharvbio.2004.05.012
  55. MacMillan Colleen P., Mansfield Shawn D., Stachurski Zbigniew H., Evans Rob, Southerton Simon G., Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus : FLAs specialized for stem biomechanics and cell walls, 10.1111/j.1365-313x.2010.04181.x
  56. Mahapatro Anil, Kumar Ajay, Gross Richard A., Mild, Solvent-Free ω-Hydroxy Acid Polycondensations Catalyzed byCandidaantarcticaLipase B, 10.1021/bm0342382
  57. McFarlane Heather E., Shin John J.H., Bird David A., Samuels A. Lacey, ArabidopsisABCG Transporters, Which Are Required for Export of Diverse Cuticular Lipids, Dimerize in Different Combinations, 10.1105/tpc.110.077974
  58. Moire Laurence, Schmutz Alain, Buchala Antony, Yan Bin, Stark Ruth E., Ryser Ulrich, Glycerol Is a Suberin Monomer. New Experimental Evidence for an Old Hypothesis, 10.1104/pp.119.3.1137
  59. Molhoj M., The Biosynthesis of D-Galacturonate in Plants. Functional Cloning and Characterization of a Membrane-Anchored UDP-D-Glucuronate 4-Epimerase from Arabidopsis, 10.1104/pp.104.043745
  60. Molina I., Li-Beisson Y., Beisson F., Ohlrogge J. B., Pollard M., Identification of an Arabidopsis Feruloyl-Coenzyme A Transferase Required for Suberin Synthesis, 10.1104/pp.109.144907
  61. Mortazavi Ali, Williams Brian A, McCue Kenneth, Schaeffer Lorian, Wold Barbara, Mapping and quantifying mammalian transcriptomes by RNA-Seq, 10.1038/nmeth.1226
  62. Moura Jullyana Cristina Magalhães Silva, Bonine Cesar Augusto Valencise, de Oliveira Fernandes Viana Juliana, Dornelas Marcelo Carnier, Mazzafera Paulo, Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants, 10.1111/j.1744-7909.2010.00892.x
  63. Müller Kerstin, Levesque-Tremblay Gabriel, Fernandes Anwesha, Wormit Alexandra, Bartels Sebastian, Usadel Bjoern, Kermode Allison, Overexpression of a pectin methylesterase inhibitor inArabidopsis thalianaleads to altered growth morphology of the stem and defective organ separation, 10.4161/psb.26464
  64. Olsson Ann, Lindström Mikael, Iversen Tommy, Lipase-Catalyzed Synthesis of an Epoxy-Functionalized Polyester from the Suberin Monomercis-9,10-Epoxy-18-hydroxyoctadecanoic Acid, 10.1021/bm060965w
  65. Panikashvili David, Shi Jian Xin, Bocobza Samuel, Franke Rochus Benni, Schreiber Lukas, Aharoni Asaph, The Arabidopsis DSO/ABCG11 Transporter Affects Cutin Metabolism in Reproductive Organs and Suberin in Roots, 10.1093/mp/ssp103
  66. PASSARDI F, PENEL C, DUNAND C, Performing the paradoxical: how plant peroxidases modify the cell wall, 10.1016/j.tplants.2004.09.002
  67. PELLOUX J, RUSTERUCCI C, MELLEROWICZ E, New insights into pectin methylesterase structure and function, 10.1016/j.tplants.2007.04.001
  68. Pinot Franck, Beisson Fred, Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles : Cytochrome P450 metabolizing fatty acids in plants, 10.1111/j.1742-4658.2010.07948.x
  69. Pollard Mike, Beisson Fred, Li Yonghua, Ohlrogge John B., Building lipid barriers: biosynthesis of cutin and suberin, 10.1016/j.tplants.2008.03.003
  70. Quiroga Mónica, Guerrero Consuelo, Botella Miguel A., Barceló Araceli, Amaya Iraida, Medina Marı́a I., Alonso Francisco J., de Forchetti Silvia Milrad, Tigier Horacio, Valpuesta Victoriano, A Tomato Peroxidase Involved in the Synthesis of Lignin and Suberin, 10.1104/pp.122.4.1119
  71. Ranathunge Kosala, Schreiber Lukas, Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin, 10.1093/jxb/erq389
  72. Ranathunge Kosala, Schreiber Lukas, Franke Rochus, Suberin research in the genomics era—New interest for an old polymer, 10.1016/j.plantsci.2010.11.003
  73. Roudier F., COBRA, an Arabidopsis Extracellular Glycosyl-Phosphatidyl Inositol-Anchored Protein, Specifically Controls Highly Anisotropic Expansion through Its Involvement in Cellulose Microfibril Orientation, 10.1105/tpc.105.031732
  74. Sampedro Javier, Cosgrove Daniel J, 10.1186/gb-2005-6-12-242
  75. Serra Olga, Soler Marçal, Hohn Carolin, Franke Rochus, Schreiber Lukas, Prat Salomé, Molinas Marisa, Figueras Mercè, Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration, 10.1093/jxb/ern314
  76. Serra O., Soler M., Hohn C., Sauveplane V., Pinot F., Franke R., Schreiber L., Prat S., Molinas M., Figueras M., CYP86A33-Targeted Gene Silencing in Potato Tuber Alters Suberin Composition, Distorts Suberin Lamellae, and Impairs the Periderm's Water Barrier Function, 10.1104/pp.108.127183
  77. Serra Olga, Hohn Carolin, Franke Rochus, Prat Salomé, Molinas Marisa, Figueras Mercè, A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm : FHT function in potato periderm, 10.1111/j.1365-313x.2010.04144.x
  78. Skene D.S., The Development of Russet, Rough Russet and Cracks on the Fruit of the Apple Cox’s Orange Pippin During the Course of the Season, 10.1080/00221589.1982.11515037
  79. Soler M., Serra O., Molinas M., Huguet G., Fluch S., Figueras M., A Genomic Approach to Suberin Biosynthesis and Cork Differentiation, 10.1104/pp.106.094227
  80. Sousa Andreia F., Silvestre Armando J. D., Gandini Alessandro, Neto Carlos Pascoal, Synthesis of aliphatic suberin-like polyesters by ecofriendly catalytic systems, 10.1177/0954008311431114
  81. Suh M. C., Cuticular Lipid Composition, Surface Structure, and Gene Expression in Arabidopsis Stem Epidermis, 10.1104/pp.105.070805
  82. Thimm Oliver, Bläsing Oliver, Gibon Yves, Nagel Axel, Meyer Svenja, Krüger Peter, Selbig Joachim, Müller Lukas A., Rhee Seung Y., Stitt Mark, mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes, 10.1111/j.1365-313x.2004.02016.x
  83. Tor M., Lotze M. T., Holton N., Receptor-mediated signalling in plants: molecular patterns and programmes, 10.1093/jxb/erp233
  84. Vandesompele Jo, De Preter Katleen, Pattyn Filip, Poppe Bruce, Van Roy Nadine, De Paepe Anne, Speleman Frank, 10.1186/gb-2002-3-7-research0034
  85. Velasco Riccardo, Zharkikh Andrey, Affourtit Jason, Dhingra Amit, Cestaro Alessandro, Kalyanaraman Ananth, Fontana Paolo, Bhatnagar Satish K, Troggio Michela, Pruss Dmitry, Salvi Silvio, Pindo Massimo, Baldi Paolo, Castelletti Sara, Cavaiuolo Marina, Coppola Giuseppina, Costa Fabrizio, Cova Valentina, Dal Ri Antonio, Goremykin Vadim, Komjanc Matteo, Longhi Sara, Magnago Pierluigi, Malacarne Giulia, Malnoy Mickael, Micheletti Diego, Moretto Marco, Perazzolli Michele, Si-Ammour Azeddine, Vezzulli Silvia, Zini Elena, Eldredge Glenn, Fitzgerald Lisa M, Gutin Natalia, Lanchbury Jerry, Macalma Teresita, Mitchell Jeff T, Reid Julia, Wardell Bryan, Kodira Chinnappa, Chen Zhoutao, Desany Brian, Niazi Faheem, Palmer Melinda, Koepke Tyson, Jiwan Derick, Schaeffer Scott, Krishnan Vandhana, Wu Changjun, Chu Vu T, King Stephen T, Vick Jessica, Tao Quanzhou, Mraz Amy, Stormo Aimee, Stormo Keith, Bogden Robert, Ederle Davide, Stella Alessandra, Vecchietti Alberto, Kater Martin M, Masiero Simona, Lasserre Pauline, Lespinasse Yves, Allan Andrew C, Bus Vincent, Chagné David, Crowhurst Ross N, Gleave Andrew P, Lavezzo Enrico, Fawcett Jeffrey A, Proost Sebastian, Rouzé Pierre, Sterck Lieven, Toppo Stefano, Lazzari Barbara, Hellens Roger P, Durel Charles-Eric, Gutin Alexander, Bumgarner Roger E, Gardiner Susan E, Skolnick Mark, Egholm Michael, Van de Peer Yves, Salamini Francesco, Viola Roberto, The genome of the domesticated apple (Malus × domestica Borkh.), 10.1038/ng.654
  86. Walter TE (1967) Russeting and cracking in apples, a review of world literature. Annu Rep East Malling Res Stn 1966:83–95
  87. Wang Yue-zhi, Dai Mei-song, Zhang Shu-jun, Shi Ze-bin, Exploring Candidate Genes for Pericarp Russet Pigmentation of Sand Pear (Pyrus pyrifolia) via RNA-Seq Data in Two Genotypes Contrasting for Pericarp Color, 10.1371/journal.pone.0083675
  88. Wang Yue-zhi, Zhang Shujun, Dai Mei-song, Shi Ze-bin, Pigmentation in sand pear (Pyrus pyrifolia) fruit: biochemical characterization, gene discovery and expression analysis with exocarp pigmentation mutant, 10.1007/s11103-014-0173-1
  89. Watanabe S (1969) Historical studies on the cause of apple russeting. Bull Yamagata Univ 5:205–267
  90. Zhong R., Lee C., Zhou J., McCarthy R. L., Ye Z.-H., A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis, 10.1105/tpc.108.061325
  91. Zimmermann Hilde Monika, Hartmann Klaus, Schreiber Lukas, Steudle Ernst, Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.), 10.1007/pl00008138
Bibliographic reference Legay, Sylvain ; Guerriero, Gea ; Deleruelle, Amélie ; Lateur, Marc ; Evers, Danièle ; et. al. Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall. In: Plant Molecular Biology, Vol. 88, p. 21-40 (2015)
Permanent URL http://hdl.handle.net/2078.1/187865