A comparative transcriptomic approach to understanding the formation of cork

  • Pau Boher
  • Marçal Soler
  • Anna Sánchez
  • Claire Hoede
  • Céline Noirot
  • Jorge Almiro Pinto Paiva
  • Olga Serra
  • Mercè Figueras
Article

Abstract

Key message

The transcriptome comparison of two oak species reveals possible candidates accounting for the exceptionally thick and pure cork oak phellem, such as those involved in secondary metabolism and phellogen activity.

Abstract

Cork oak, Quercus suber, differs from other Mediterranean oaks such as holm oak (Quercus ilex) by the thickness and organization of the external bark. While holm oak outer bark contains sequential periderms interspersed with dead secondary phloem (rhytidome), the cork oak outer bark only contains thick layers of phellem (cork rings) that accumulate until reaching a thickness that allows industrial uses. Here we compare the cork oak outer bark transcriptome with that of holm oak. Both transcriptomes present similitudes in their complexity, but whereas cork oak external bark is enriched with upregulated genes related to suberin, which is the main polymer responsible for the protective function of periderm, the upregulated categories of holm oak are enriched in abiotic stress and chromatin assembly. Concomitantly with the upregulation of suberin-related genes, there is also induction of regulatory and meristematic genes, whose predicted activities agree with the increased number of phellem layers found in the cork oak sample. Further transcript profiling among different cork oak tissues and conditions suggests that cork and wood share many regulatory mechanisms, probably reflecting similar ontogeny. Moreover, the analysis of transcripts accumulation during the cork growth season showed that most regulatory genes are upregulated early in the season when the cork cambium becomes active. Altogether our work provides the first transcriptome comparison between cork oak and holm oak outer bark, which unveils new regulatory candidate genes of phellem development.

Keywords

Cork Cork oak Phellem Rhytidome Suberin Wax 

Notes

Acknowledgements

We would like to thank Professor M. Molinas (Departament de Biologia, UdG, Girona) for her useful advice and feedback during the analysis of the results and the drafting of the manuscript. The authors are grateful to Dr. R. Verdaguer, S. Fernández, S. Gómez and N. Salvatella for their help in cork harvesting. We thank Professor C. Pla (Departament de Biologia, UdG, Girona) for kindly lending the Thermocycler and Mr J. Blavia and Ms C. Carulla (Serveis Tècnics de Recerca, Universitat de Girona, Spain) for their highly skilled work with SEM. This work was supported by the Ministerio de Innovación y Ciencia [AGL2009-13745, FPI grant to P.B.], the Ministerio de Economía y Competitividad and FEDER funding [AGL2012-36725; AGL2015-67495-C2-1-R]. J.A.P.P. acknowledges the European Union’s Seventh Framework Programme for research, technological development and demonstration (EU FP7 Agreement No. 621321) and the Polish financial sources for education (2015–2019) allocated to Project No (W26/7.PR/2015).

Author contributions

PB, OS, JP and MF designed the experiment; PB extracted the RNA and purified the mRNA; PB, CH and CN performed bioinformatics; PB and AS performed qPCR; all authors analyzed and discussed the data. PB, MS, OS and MF wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2017_682_MOESM1_ESM.tif (9.3 mb)
Fig. S1. Workflow of sequencing, assembly, annotation and differential expression analyses (TIF 9517 KB)
11103_2017_682_MOESM2_ESM.xlsx (2.5 mb)
Table S1. Functional annotation of contigs and gene expression values in 454 libraries. (XLSX 2528 KB)
11103_2017_682_MOESM3_ESM.xlsx (2.9 mb)
Table S2. For each contig A) gene ontology terms and B) MapMan annotations are shown (XLSX 2943 KB)
11103_2017_682_MOESM4_ESM.pdf (231 kb)
Table S3. Sequences of the primers (PDF 231 KB)
11103_2017_682_MOESM5_ESM.pdf (331 kb)
Table S4. Statistics of the 454 sequencing, transcriptome assembly and functional annotation of contigs (PDF 331 KB)
11103_2017_682_MOESM6_ESM.xlsx (390 kb)
Table S5. Gene ontology enrichment of the differentially regulated contigs (XLSX 389 KB)
11103_2017_682_MOESM7_ESM.xlsx (55 kb)
Table S6. Classification in accordance with Arabidopsis databases for carbohydrates and acyl-lipid metabolism (XLSX 54 KB)

References

  1. Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM et al (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165. https://doi.org/10.1111/j.1365-313X.2005.02584.x CrossRefPubMedGoogle Scholar
  2. Andre C, Froehlich JE, Moll MR, Benning C (2007) A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell 19:2006–2022CrossRefPubMedPubMedCentralGoogle Scholar
  3. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639. https://doi.org/10.1038/nrg3291 CrossRefPubMedGoogle Scholar
  4. Azeez A, Miskolczi P, Tylewicz S, Bhalerao RP (2014) A tree ortholog of APETALA1 mediates photoperiodic control of seasonal growth. Curr Biol 24:717–724. https://doi.org/10.1016/j.cub.2014.02.037 CrossRefPubMedGoogle Scholar
  5. Barel G, Ginzberg I (2008) Potato skin proteome is enriched with plant defence components. J Exp Bot 59:3347–3357. https://doi.org/10.1093/jxb/ern184 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baud S, Wuillème S, Dubreucq B, De Almeida A, Vuagnat C, Lepiniec L et al (2007) Function of plastidial pyruvate kinases in seeds of Arabidopsis thaliana. Plant J 52:405–419. https://doi.org/10.1111/j.1365-313X.2007.03232.x CrossRefPubMedGoogle Scholar
  7. Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19:351–368. https://doi.org/10.1105/tpc.106.048033 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300. https://doi.org/10.2307/2346101 Google Scholar
  9. Bernal AJ, Yoo C-M, Mutwil M, Jensen JK, Hou G, Blaukopf C, Sørensen I, Blancaflor EB, Scheller HV, Willats WG (2008) Functional analysis of the cellulose synthase-like genes CSLD1, CSLD2, and CSLD4 in tip-growing Arabidopsis cells. Plant Physiol 148:1238–1253. https://doi.org/10.1104/pp.108.121939 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bernards MA (2002) Demystifying suberin. Can J Bot 80:227–240. https://doi.org/10.1139/B02-017 CrossRefGoogle Scholar
  11. Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB et al (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci USA 108:12527–12532. https://doi.org/10.1073/pnas.1106502108 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng JC et al (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351. https://doi.org/10.1242/dev.01403 CrossRefPubMedGoogle Scholar
  13. Caritat A, Gutierrez E, Molinas M (2000) Influence of weather on cork-ring width. Tree Physiol 20:893–900. https://doi.org/10.1093/treephys/20.13.893 CrossRefPubMedGoogle Scholar
  14. Castola V, Marongiu B, Bighelli A, Floris C, Laï A, Casanova J (2005) Extractives of cork (Quercus suber L.): chemical composition of dichloromethane and supercritical CO2 extracts. Ind Crops Prod 21:65–69. https://doi.org/10.1016/j.indcrop.2003.12.007 CrossRefGoogle Scholar
  15. Cavallini E, Matus JT, Finezzo L, Zenoni S, Loyola R, Guzzo F et al (2015) The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol 167:1448–1470. https://doi.org/10.1104/pp.114.256172 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T et al (1999) The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119:897–907. https://doi.org/10.1104/pp.119.3.897 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L et al (2009) CYP86B1 is required for very long chain omega-hydroxyacid and alpha, omega-dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiol 150:1831–1843. https://doi.org/10.1104/pp.109.141408 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Crevillén P, Yang H, Cui X, Greeff C, Trick M, Qiu Q et al (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515:587–590. https://doi.org/10.1038/nature13722 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Enjuto M, Balcells L, Campos N, Caelles C, Arró M, Boronat A (1994) Arabidopsis thaliana contains two differentially expressed 3-hydroxy-3-methylglutaryl-CoA reductase genes, which encode microsomal forms of the enzyme. Proc Natl Acad Sci USA 91:927–931. https://doi.org/10.1073/pnas.91.3.927 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Evert RF, Eichhorn SE (2006). Periderm. In Wiley-Blackwell (ed) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley, New YorkCrossRefGoogle Scholar
  21. Fahn A (1967) Plant anatomy. Pergamon Press, OxfordGoogle Scholar
  22. Fukuda H (1997) Tracheary element differentiation. Plant Cell 9:1147–1156. https://doi.org/10.1105/tpc.9.7.1147 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gil L (2014) Cork: a strategic material. Front Chem 2:1–2. https://doi.org/10.3389/fchem.2014.00016 CrossRefGoogle Scholar
  24. Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J et al (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3119–3134. https://doi.org/10.1105/tpc.112.101055 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435. https://doi.org/10.1093/nar/gkn176 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gou JY, Yu XH, Liu CJ (2009) A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc Natl Acad Sci USA 106:18855–18860. doi:https://doi.org/10.1073/pnas.0905555106\r0905555106 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gou M, Hou G, Yang H, Zhang X, Cai Y, Kai G, Liu CJ (2017) The MYB107 transcription factor positively regulates suberin biosynthesis. Plant Physiol 173(2):1045–1058. https://doi.org/10.1104/pp.16.01614 CrossRefPubMedGoogle Scholar
  28. Graça J (2015) Suberin the biopolyester at the frontier of plants. Front Chem. https://doi.org/10.3389/fchem.2015.00062 PubMedPubMedCentralGoogle Scholar
  29. Graça J, Santos S (2007) Suberin: a biopolyester of plants’ skin. Macromol Biosci 7:128–135. https://doi.org/10.1002/mabi.200600218 CrossRefPubMedGoogle Scholar
  30. Gray-Mitsumune M, Mellerowicz EJ, Abe H, Schrader J, Winzéll A, Sterky F, Blomqvist K, McQueen-Mason S, Teeri TT, Sundberg B (2004) Expansins abundant in secondary xylem belong to subgroup A of the alpha-expansin gene family. Plant Physiol 135:1552–1564. https://doi.org/10.1104/pp.104.039321 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Groover AT, Mansfield SD, DiFazio SP, Dupper G, Fontana JR, Millar R et al (2006) The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61:917–932. https://doi.org/10.1007/s11103-006-0059-y CrossRefPubMedGoogle Scholar
  32. Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629. https://doi.org/10.1105/tpc.110.076083 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, Franke R (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid -hydroxylase involved in suberin monomer biosynthesis. J Exp Bot 59:2347–2360. https://doi.org/10.1093/jxb/ern101 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Holloway PJ (1983) Some variations in the composition of suberin from the cork layers of higher plants. Phytochemistry 22:495–502. https://doi.org/10.1016/0031-9422(83)83033-7 CrossRefGoogle Scholar
  35. Howard ET (1977) Bark structure of southern upland oaks. Wood Fiber 9:172–183Google Scholar
  36. Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2:741–753. https://doi.org/10.1105/tpc.2.8.741 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ji J, Shimizu R, Sinha N, Scanlon MJ (2010) Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signal Behav 5:916–920. https://doi.org/10.1104/pp.109.149641 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J et al (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161. https://doi.org/10.1093/emboj/19.22.6150 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M et al (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390. https://doi.org/10.1105/tpc.113.118364 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Klahre U, Noguchi T, Fujioka S, Takatsuto S, Yokota T, Nomura T et al (1998) The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10:1677–1690. https://doi.org/10.1105/tpc.10.10.1677 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I et al (2014) AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. The Plant J 80:216–229. https://doi.org/10.1111/tpj.12624 CrossRefPubMedGoogle Scholar
  42. Lashbrooke J, Cohen H, Levy-Samocha D, Tzfadia O, Panizel I, Zeisler V et al (2016) MYB107 and MYB9 homologs regulate suberin deposition in angiosperms. Plant Cell 28:2097–2116. https://doi.org/10.1105/tpc.16.00490 CrossRefPubMedCentralGoogle Scholar
  43. Legay S, Sivadon P, Blervacq AS, Pavy N, Baghdady A, Tremblay L et al (2010) EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188:774–786. https://doi.org/10.1111/j.1469-8137.2010.03432.x CrossRefPubMedGoogle Scholar
  44. Legay S, Guerriero G, Deleruelle A, Lateur M, Evers D, André CM, Hausman J-F (2015) Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall. Plant Mol Biol 88:21–40. https://doi.org/10.1007/s11103-015-0303-4 CrossRefPubMedGoogle Scholar
  45. Legay S, Guerriero G, André C, Guignard C, Cocco E, Charton S et al (2016) MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. New Phytol 212:977–991. https://doi.org/10.1111/nph.14170 CrossRefPubMedGoogle Scholar
  46. Lendzian KJ (2006) Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. J Exp Bot 57:2535–2546. https://doi.org/10.1093/jxb/erl014 CrossRefPubMedGoogle Scholar
  47. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. https://doi.org/10.1093/bioinformatics/btl158 CrossRefPubMedGoogle Scholar
  49. Li Y, Beisson F, Koo AJK, Molina I, Pollard M, Ohlrogge JB (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104:18339–18344. https://doi.org/10.1073/pnas.0706984104 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD et al (2013) Acyl-lipid metabolism. Arab B 11:e0161. https://doi.org/10.1199/tab.0161 CrossRefGoogle Scholar
  51. Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 9:387–402. https://doi.org/10.1146/annurev.genom.9.081307.164359 CrossRefPubMedGoogle Scholar
  52. McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578. https://doi.org/10.1073/pnas.91.14.6574 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Miguel A, Milhinhos A, Novák O, Jones B, Miguel CM (2015) The SHORT-ROOT-like gene PtSHR2B is involved in Populus phellogen activity. J Exp Bot 67:1545–1555. https://doi.org/10.1093/jxb/erv547 CrossRefPubMedGoogle Scholar
  54. Molina I, Kosma D (2015) Role of HXXXD-motif/BAHD acyltransferases in the biosynthesis of extracellular lipids. Plant Cell Rep 34:587–601. https://doi.org/10.1007/s00299-014-1721-5 CrossRefPubMedGoogle Scholar
  55. Molina I, Li-Beisson Y, Beisson F, Ohlrogge JB, Pollard M (2009) Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiol 151:1317–1328. https://doi.org/10.1104/pp.109.144907\rpp.109.144907 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nagata N, Asami T, Yoshida S (2001) Brassinazole, an inhibitor of brassinosteroid biosynthesis, inhibits development of secondary xylem in cress plants (Lepidium sativum). Plant Cell Physiol 42:1006–1011. https://doi.org/10.1093/pcp/pce122 CrossRefPubMedGoogle Scholar
  57. Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E, Perrot-Rechenmann C et al (2008) Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20:843–855. https://doi.org/10.1105/tpc.107.055798 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pereira-Leal JB, Abreu IA, Alabaça CS, Almeida MH, Almeida P, Almeida T et al (2014) A comprehensive assessment of the transcriptome of cork oak (Quercus suber) through EST sequencing. BMC Genom 15:371. https://doi.org/10.1186/1471-2164-15-371 CrossRefGoogle Scholar
  59. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246. https://doi.org/10.1016/j.tplants.2008.03.003 CrossRefPubMedGoogle Scholar
  61. Porto DD, Bruneau M, Perini P, Anzanello R, Renou JP, dos Santos HP et al (2015) Transcription profiling of the chilling requirement for bud break in apples: a putative role for FLC-like genes. J Exp Bot 66:2659–2672. https://doi.org/10.1093/jxb/erv061 CrossRefPubMedGoogle Scholar
  62. Rains MK, Gardiyehewa de Silva ND, Molina I (2017) Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol 1:1–22. https://doi.org/10.1093/treephys/tpx060 Google Scholar
  63. Reinbothe C, Springer A, Samol I, Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 276:4666–4681. https://doi.org/10.1111/j.1742-4658.2009.07193.x CrossRefPubMedGoogle Scholar
  64. Ricardo CPP, Martins I, Francisco R, Sergeant K, Pinheiro C, Campos A et al (2011) Proteins associated with cork formation in Quercus suber L. stem tissues. J Proteomics 74:1266–1278. https://doi.org/10.1016/j.jprot.2011.02.003 CrossRefPubMedGoogle Scholar
  65. Schreiber L, Franke R, Hartmann K (2005) Wax and suberin development of native and wound periderm of potato (Solanum tuberosum L.) and its relation to peridermal transpiration. Planta 220:520–530. https://doi.org/10.1007/s00425-004-1364-9 CrossRefPubMedGoogle Scholar
  66. Serra O, Soler M, Hohn C, Franke R, Schreiber L, Prat S 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 60:697–707. https://doi.org/10.1093/jxb/ern314 CrossRefPubMedGoogle Scholar
  67. Serra O, Hohn C, Franke R, Prat S, Molinas M, Figueras M (2010) A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm. Plant J 62:277–290. https://doi.org/10.1111/j.1365-313X.2010.04144.x CrossRefPubMedGoogle Scholar
  68. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758. https://doi.org/10.1073/pnas.97.7.3753 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shindo C, Lister C, Crevillen P, Nordborg M, Dean C (2006) Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev 20:3079–3083. https://doi.org/10.1101/gad.405306 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sibout R, Plantegenet S, Hardtke CS (2008) Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr Biol 18:458–463. https://doi.org/10.1016/j.cub.2008.02.070 CrossRefPubMedGoogle Scholar
  71. Silva SP, Sabino MA, Fernandes EM, Correlo VM, Boesel LF, Reis RL (2005) Cork: properties, capabilities and applications. Int Mater Rev 50:345–365. https://doi.org/10.1179/174328005X41168 CrossRefGoogle Scholar
  72. Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431. https://doi.org/10.1104/pp.106.094227 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Soler M, Serra O, Molinas M, García-Berthou E, Caritat A, Figueras M (2008) Seasonal variation in transcript abundance in cork tissue analyzed by real time RT-PCR. Tree Physiol 28:743–751. https://doi.org/10.1093/treephys/28.5.743 CrossRefPubMedGoogle Scholar
  74. Soler M, Serra O, Fluch S, Molinas M, Figueras M (2011) A potato skin SSH library yields new candidate genes for suberin biosynthesis and periderm formation. Planta 233:933–945. https://doi.org/10.1007/s00425-011-1350-y CrossRefPubMedGoogle Scholar
  75. Soler M, Plasencia A, Larbat R, Pouzet C, Jauneau A, Rivas S et al (2017) The Eucalyptus linker histone variant EgH1.3 cooperates with the transcription factor EgMYB1 to control lignin biosynthesis during wood formation. New Phytol 213:287–299. https://doi.org/10.1111/nph.14129 CrossRefPubMedGoogle Scholar
  76. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–3259. https://doi.org/10.1105/tpc.111.087874 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Teixeira RT, Fortes AM, Pinheiro C, Pereira H (2014) Comparison of good- and bad-quality cork: application of high-throughput sequencing of phellogenic tissue. J Exp Bot 65:4887–4905. https://doi.org/10.1093/jxb/eru252 CrossRefPubMedGoogle Scholar
  78. Teixeira RT, Fortes AM, Bai H, Pinheiro C, Pereira H (2017) Transcriptional profiling of cork oak phellogenic cells isolated by laser microdissection. Planta. https://doi.org/10.1007/s00425-017-2786-5 PubMedGoogle Scholar
  79. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P et al (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x CrossRefPubMedGoogle Scholar
  80. Troncoso-Ponce MA, Kilaru A, Cao X, Durrett TP, Fan J, Jensen JK, Thrower NA, Pauly M, Wilkerson C, Ohlrogge JB (2011) Comparative deep transcriptional profiling of four developing oilseeds. Plant J 68:1014–1027. https://doi.org/10.1111/j.1365-313X.2011.04751.x CrossRefPubMedPubMedCentralGoogle Scholar
  81. Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–585. https://doi.org/10.1104/PP.115.2.577 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Verdaguer R, Soler M, Serra O, Garrote A, Fernández S, Company-Arumí D, Anticó E, Molinas M, Figueras M (2016) Silencing of the potato StNAC103 gene enhances the accumulation of suberin polyester and associated wax in tuber skin. J Exp Bot 67:5415–5427. https://doi.org/10.1093/jxb/erw305 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Vishwanath SJ, Delude C, Domergue F, Rowland O (2015) Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep 34:573–586. https://doi.org/10.1007/s00299-014-1727-z CrossRefPubMedGoogle Scholar
  84. Waisel Y (1995) Developmental and functional aspects of the periderm. In: Iqbal M (ed) The cambial derivatives. Gebruder Borntraeger, Stuttgart, pp 293–315Google Scholar
  85. Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586. https://doi.org/10.1104/pp.126.2.575 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Wang L, Feng Z, Wang X, Wang X, Zhang X (2009) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138. https://doi.org/10.1093/bioinformatics/btp612 CrossRefPubMedGoogle Scholar
  87. Wang Z, Gerstein M, Snyder M (2010) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. https://doi.org/10.1038/nrg2484 CrossRefGoogle Scholar
  88. Wang YZ, Zhang S, Dai MS, Shi ZB (2014) Pigmentation in sand pear (Pyrus pyrifolia) fruit: biochemical characterization, gene discovery and expression analysis with exocarp pigmentation mutant. Plant Mol Biol 85:123 –134. https://doi.org/10.1007/s11103-014-0173-1 CrossRefPubMedGoogle Scholar
  89. Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894. https://doi.org/10.1111/j.1365-313X.2006.02654.x CrossRefPubMedGoogle Scholar
  90. Wei Z, Qu Z, Zhang L, Zhao S, Bi Z, Ji X et al (2015) Overexpression of poplar xylem sucrose synthase in tobacco leads to a thickened cell wall and increased height. PLoS ONE 10:1–20. https://doi.org/10.1371/journal.pone.0120669 Google Scholar
  91. Zhong R, Ye ZH (2001) Alteration of auxin polar transport in the Arabidopsisifl1 mutants. Plant Physiol 126:549–563. https://doi.org/10.1104/pp.126.2.549 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Laboratori del Suro, Faculty of Science, Biology DepartmentUniversitat de GironaGironaSpain
  2. 2.PF Bioinfo GenoToul, MIAT, Université de Toulouse, INRAAuzeville-TolosaneFrance
  3. 3.iBET, Instituto de Biologia Experimental e Tecnológica, Avenida da RepúblicaOeirasPortugal
  4. 4.Institute of Plant Genetics, Department of Integrative Plant BiologyPolish Academy of SciencesPoznanPoland

Personalised recommendations