Characterization of the cork formation and production transcriptome in Quercus cerris × suber hybrids

Meireles, Brígida; Usié, Ana; Barbosa, Pedro; Fortes, Ana Margarida; Folgado, André; Chaves, Inês; Carrasquinho, Isabel; Costa, Rita Lourenço; Gonçalves, Sónia; Teixeira, Rita Teresa; Ramos, António Marcos; Nóbrega, Filomena

doi:10.1007/s12298-018-0526-3

Research Article
Published: 11 April 2018

Characterization of the cork formation and production transcriptome in Quercus cerris × suber hybrids

Brígida Meireles¹^na1,
Ana Usié^1,2^na1,
Pedro Barbosa¹,
Ana Margarida Fortes³,
André Folgado¹,
Inês Chaves¹,
Isabel Carrasquinho⁴,
Rita Lourenço Costa^4,5,
Sónia Gonçalves¹^nAff7,
Rita Teresa Teixeira⁶,
António Marcos Ramos ORCID: orcid.org/0000-0003-3450-0970^1,2 &
Filomena Nóbrega⁴

Physiology and Molecular Biology of Plants volume 24, pages 535–549 (2018)Cite this article

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Abstract

Cork oak is the main cork-producing species worldwide, and plays a significant economic, ecological and social role in the Mediterranean countries, in particular in Portugal and Spain. The ability to produce cork is limited to a few species, hence it must involve specific regulation mechanisms that are unique to these species. However, to date, these mechanisms remain largely understudied, especially with approaches involving the use of high-throughput sequencing technology. In this study, the transcriptome of cork-producing and non-cork-producing Quercus cerris × suber hybrids was analyzed in order to elucidate the differences between the two groups of trees displaying contrasting phenotypes for cork production. The results revealed the presence of a significant number of genes exclusively associated with cork production, in the trees that developed cork. Moreover, several gene ontology subcategories, such as cell wall biogenesis, lipid metabolic processes, metal ion binding and apoplast/cell wall, were only detected in the trees with cork production. These results indicate the existence, at the transcriptome level, of mechanisms that seem to be unique and necessary for cork production, which is an advancement in our knowledge regarding the genetic regulation behind cork formation and production.

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References

Alcázar R, Marco F, Cuevas JC et al (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3
Article PubMed CAS Google Scholar
Baxter HL, Stewart CN (2013) Effects of altered lignin biosynthesis on phenylpropanoid metabolism and plant stress. Biofuels 4:635–650. https://doi.org/10.4155/bfs.13.56
Article CAS Google Scholar
Bugalho MN, Caldeira MC, Pereira JS et al (2011) Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services. Front Ecol Environ 9:278–286. https://doi.org/10.1890/100084
Article Google Scholar
Caritat A, Gutiérrez E, Molinas M (2000) Influence of weather on cork-ring width. Tree Physiol 20:893–900
Article PubMed CAS Google Scholar
Chevreux B, Pfisterer T, Drescher B et al (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14:1147–1159
Article PubMed PubMed Central CAS Google Scholar
Coberly LC, Rausher MD (2003) Analysis of a chalcone synthase mutant in Ipomoea purpurea reveals a novel function for flavonoids: amelioration of heat stress. Mol Ecol 12:1113–1124
Article PubMed CAS Google Scholar
Correia B, Valledor L, Meijón M et al (2013) Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures ? PLoS ONE 8:e53543. https://doi.org/10.1371/journal.pone.0053543
Article PubMed PubMed Central CAS Google Scholar
Correia B, Rodriguez JL, Valledor L et al (2014) Analysis of the expression of putative heat-stress related genes in relation to thermotolerance of cork oak. J Plant Physiol 171:399–406. https://doi.org/10.1016/j.jplph.2013.12.004
Article PubMed CAS Google Scholar
Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412. https://doi.org/10.1007/s11101-011-9211-7
Article PubMed PubMed Central CAS Google Scholar
Denness L, McKenna JF, Segonzac C et al (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–1374. https://doi.org/10.1104/pp.111.175737
Article PubMed PubMed Central CAS Google Scholar
Ebadzad G, Cravador A (2014) Quantitative RT-PCR analysis of differentially expressed genes in Quercus suber in response to Phytophthora cinnamomi infection. SpringerPlus 3:613
Article PubMed PubMed Central CAS Google Scholar
Ghouil H, Montpied P, Epron D et al (2003) Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings. Tree Physiol 23:1031–1040
Article PubMed CAS Google Scholar
Gollop R, Farhi S, Perl A (2001) Regulation of the leucoanthocyanidin dioxygenase gene expression in Vitis vinifera. Plant Sci 161:579–588
Article CAS Google Scholar
Graça J (2015) Suberin: the biopolyester at the frontier of plants. Front Chem. https://doi.org/10.3389/fchem.2015.00062
PubMed PubMed Central Article Google Scholar
Graça J, Pereira H (2004) The periderm development in Quercus suber. IAWA J 25:325–335. https://doi.org/10.1163/22941932-90000369
Article Google Scholar
Graça J, Santos S (2007) Suberin: a biopolyester of plants’ skin. Macromol Biosci 7:128–135. https://doi.org/10.1002/mabi.200600218
Article PubMed CAS Google Scholar
Grand C (1984) Ferulic acid 5-hydroxylase: a new cytochrome P-450-dependent enzyme from higher plant microsomes involved in lignin synthesis. FEBS Lett 169:7–11
Article CAS Google Scholar
Haas BJ, Papanicolaou A, Yassour M et al (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. https://doi.org/10.1038/nprot.2013.084
Article PubMed CAS Google Scholar
Hu Z-L, Bao J, Reecy JM (2008) CateGOrizer: a web-based program to batch analyze gene on-tology classification categories. Online J Bioinform 9:108–112
Google Scholar
Huang B, Xu C (2008) Identification and characterization of proteins associated with plant tolerance to heat stress. J Integr Plant Biol 50:1230–1237. https://doi.org/10.1111/j.1744-7909.2008.00735.x
Article PubMed CAS Google Scholar
Jones P, Binns D, Chang H-Y et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031
Article PubMed PubMed Central CAS Google Scholar
Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242. https://doi.org/10.1016/j.tplants.2005.03.002
Article PubMed CAS Google Scholar
Kolattukudy PE (1981) Structure, biosynthesis, and biodegradation of cutin and suberin. Annu Rev Plant Physiol 32:539–567. https://doi.org/10.1146/annurev.pp.32.060181.002543
Article CAS Google Scholar
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Article PubMed PubMed Central CAS Google Scholar
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Article PubMed PubMed Central CAS Google Scholar
Lourenço A, Rencoret J, Chemetova C et al (2016) Lignin composition and structure differs between xylem, phloem and phellem in Quercus suber L. Front Plant Sci 10:10. https://doi.org/10.3389/fpls.2016.01612
Article Google Scholar
Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 21:3448–3449. https://doi.org/10.1093/bioinformatics/bti551
Article PubMed CAS Google Scholar
Marques AV, Pereira H (2013) Lignin monomeric composition of corks from the barks of Betula pendula, Quercus suber and Quercus cerris determined by Py–GC–MS/FID. J Anal Appl Pyrolysis 100:88–94. https://doi.org/10.1016/j.jaap.2012.12.001
Article CAS Google Scholar
Marum L, Miguel A, Ricardo CP, Miguel C (2012) Reference gene selection for quantitative real-time PCR normalization in Quercus suber. PLoS ONE 7:e35113. https://doi.org/10.1371/journal.pone.0035113
Article PubMed PubMed Central CAS Google Scholar
McKenna A, Hanna M, Banks E et al (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303. https://doi.org/10.1101/gr.107524.110
Article PubMed PubMed Central CAS Google Scholar
Merico D, Isserlin R, Stueker O et al (2010) Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS ONE 5:e13984. https://doi.org/10.1371/journal.pone.0013984
Article PubMed PubMed Central CAS Google Scholar
Miguel A, de Vega-Bartol J, Marum L et al (2015) Characterization of the cork oak transcriptome dynamics during acorn development. BMC Plant Biol. https://doi.org/10.1186/s12870-015-0534-1
PubMed PubMed Central Article Google Scholar
Mizrachi E, Mansfield SD, Myburg AA (2012) Cellulose factories: advancing bioenergy production from forest trees. New Phytol 194:54–62. https://doi.org/10.1111/j.1469-8137.2011.03971.x
Article PubMed CAS Google Scholar
Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194. https://doi.org/10.1093/pcp/pcu204
Article PubMed CAS Google Scholar
Pereira H (1988) Chemical composition and variability of cork from Quercus suber. Wood Sci Technol 22:211–218
Article CAS Google Scholar
Pereira H (2007) Cork: biology, production and uses, 1st edn. Elsevier, London
Google Scholar
Pereira-Leal JB, Abreu IA, Alabaça CS et al (2014) A comprehensive assessment of the transcriptome of cork oak (Quercus suber) through EST sequencing. BMC Genom 15:371
Article CAS Google Scholar
Pfaffl M (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
Article PubMed PubMed Central CAS Google Scholar
Pla M, Huguet G, Verdaguer D et al (1998) Stress proteins co-expressed in suberized and lignified cells and in apical meristems. Plant Sci 139:49–57
Article CAS Google Scholar
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
Article PubMed CAS Google Scholar
Rahantamalala A, Rech P, Martinez Y et al (2010) Research article coordinated transcriptional regulation of two key genes in the lignin branch pathway-CAD and CCR-is mediated through MYB-binding sites. BMC Plant Biol 10(1):130
Article PubMed PubMed Central CAS Google Scholar
Ranathunge K, Schreiber L, Franke R (2011) Suberin research in the genomics era—new interest for an old polymer. Plant Sci 180:399–413. https://doi.org/10.1016/j.plantsci.2010.11.003
Article PubMed CAS Google Scholar
Ravanel S, Block MA, Rippert P et al (2004) Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J Biol Chem 279:22548–22557. https://doi.org/10.1074/jbc.M313250200
Article PubMed CAS Google Scholar
Reid KE, Olsson N, Schlosser J et al (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27
Article PubMed PubMed Central CAS Google Scholar
Ricardo CPP, Martins I, Francisco R 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
Article PubMed CAS Google Scholar
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Article PubMed CAS PubMed Central Google Scholar
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Article PubMed PubMed Central CAS Google Scholar
Serra O, Soler M, Hohn C et al (2009) CYP86A33-targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm’s water barrier function. Plant Physiol 149:1050–1060. https://doi.org/10.1104/pp.108.127183
Article PubMed PubMed Central CAS Google Scholar
Serra O, Figueras M, Franke R et al (2010) Unraveling ferulate role in suberin and periderm biology by reverse genetics. Plant Signal Behav 5:953–958
Article PubMed PubMed Central Google Scholar
Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Article PubMed PubMed Central CAS Google Scholar
Silva SP, Sabino MA, Fernandes EM et al (2005) Cork: properties, capabilities and applications. Int Mater Rev 50:256. https://doi.org/10.1179/174328005X41168
Article CAS Google Scholar
Soler M, Serra O, Molinas M et al (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431. https://doi.org/10.1104/pp.106.094227
Article PubMed PubMed Central CAS Google Scholar
Srivastava AC, Dasgupta K, Ajieren E et al (2009) Arabidopsis plants harbouring a mutation in AtSUC2, encoding the predominant sucrose/proton symporter necessary for efficient phloem transport, are able to complete their life cycle and produce viable seed. Ann Bot 104:1121–1128. https://doi.org/10.1093/aob/mcp215
Article PubMed PubMed Central CAS Google Scholar
Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–8
Article PubMed PubMed Central CAS Google Scholar
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
Article PubMed CAS Google Scholar
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35(suppl_2):W71–W74
Article PubMed PubMed Central Google Scholar
Verdaguer R, Soler M, Serra O et al (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
Article PubMed PubMed Central CAS Google Scholar
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
Article PubMed CAS Google Scholar
Wang H, Ng TB (2002) Isolation of an antifungal thaumatin-like protein from kiwi fruits. Phytochemistry 61:1–6
Article PubMed CAS Google Scholar
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252. https://doi.org/10.1016/j.tplants.2004.03.006
Article PubMed CAS Google Scholar
Zhu YY, Machleder EM, Chenchik A et al (2001) Reverse transcriptase template switching: a SMART™ approach for full-length cDNA library construction. Biotechniques 30:892–897
PubMed CAS Article Google Scholar
Zhulidov PA, Bogdanova EA, Shcheglov AS et al (2005) A method for the preparation of normalized cDNA libraries enriched with full-length sequences. Russ J Bioorganic Chem 31:170–177
Article CAS Google Scholar

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Acknowledgements

This study was funded by Fundação para a Ciência e a Tecnologia (FCT) projects Cork Oak EST Consortium SOBREIRO/0017/2009 and UID/AGR/00115/2013. Financial support for AMR, AU and PB was provided by Investigador FCT project IF/00574/2012/CP1209/CT0001: “Genetic characterization of national animal and plant resources using next-generation sequencing”. Financial support for AMF was provided by projects PEst-OE/BIA/UI4046/2011 and FCT Investigator IF/00169/2015.

Author contribution

This study was conceived by IC, RC, AMF, RT, SG and FN (coordinator). Collection and identification of field material was performed by IC, RC and FN. Sample preparation and nucleic acid isolation were performed by RC and FN. qPCR validations were executed by AF and SG. Bioinformatics data analyses were conducted by BM, AU, PB, IC and AMR. Biological interpretation of the results was conducted by BM, AU, AMR, AMF, IC and FN. The manuscript was written by BM, AU, FN and AMR. All authors read and approved the final manuscript.

Data availability

Sequence reads were deposited in the NCBI Sequence Read Archive (SRA) under the accession numbers ERX143070 and ERX143071, for the normalized libraries, and SRX2677031 and SRX2677030, for the non-normalized libraries.

Author information

Sónia Gonçalves
Present address: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB101SA, UK
Brígida Meireles and Ana Usié have contributed equally to this work.

Affiliations

Centro de Biotecnologia Agrícola e Agro-Alimentar do Alentejo (CEBAL), Instituto Politécnico de Beja (IPBeja), Beja, Portugal
Brígida Meireles, Ana Usié, Pedro Barbosa, André Folgado, Inês Chaves, Sónia Gonçalves & António Marcos Ramos
Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM), Universidade de Évora, Évora, Portugal
Ana Usié & António Marcos Ramos
Faculdade de Ciências de Lisboa, Biosystems and Integrative Sciences Institute (BIOISI), Universidade de Lisboa, Lisbon, Portugal
Ana Margarida Fortes
Instituto Nacional de Investigação Agrária e Veterinária, I.P, Quinta do Marquês, 2780-159, Oeiras, Portugal
Isabel Carrasquinho, Rita Lourenço Costa & Filomena Nóbrega
Centro de estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017, Lisbon, Portugal
Rita Lourenço Costa
Instituto Superior de Agronomia da Universidade de Lisboa (ISA), Tapada da Ajuda, 1349-017, Lisbon, Portugal
Rita Teresa Teixeira

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Brígida Meireles
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Ana Usié
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Pedro Barbosa
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Ana Margarida Fortes
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André Folgado
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Inês Chaves
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Isabel Carrasquinho
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Rita Lourenço Costa
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Sónia Gonçalves
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Rita Teresa Teixeira
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António Marcos Ramos
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Filomena Nóbrega
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Correspondence to António Marcos Ramos.

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Meireles, B., Usié, A., Barbosa, P. et al. Characterization of the cork formation and production transcriptome in Quercus cerris × suber hybrids. Physiol Mol Biol Plants 24, 535–549 (2018). https://doi.org/10.1007/s12298-018-0526-3

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Received: 30 November 2017
Revised: 13 March 2018
Accepted: 20 March 2018
Published: 11 April 2018
Issue Date: July 2018
DOI: https://doi.org/10.1007/s12298-018-0526-3

Keywords

Cork oak
Transcriptome
Cork production
Hybrids