A comparative transcriptomic approach to understanding the formation of cork

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

doi:10.1007/s11103-017-0682-9

Published: 15 November 2017

A comparative transcriptomic approach to understanding the formation of cork

Plant Molecular Biology volume 96, pages 103–118 (2018)Cite this article

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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.

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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).

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Affiliations

Laboratori del Suro, Faculty of Science, Biology Department, Universitat de Girona, C/ Maria Aurèlia Campmany 40, 17003, Girona, Spain
Pau Boher, Marçal Soler, Anna Sánchez, Olga Serra & Mercè Figueras
PF Bioinfo GenoToul, MIAT, Université de Toulouse, INRA, 24 Chemin de Borde Rouge, 31320, Auzeville-Tolosane, France
Claire Hoede & Céline Noirot
iBET, Instituto de Biologia Experimental e Tecnológica, Avenida da República, Estação Agronómica Nacional, 2780-157, Oeiras, Portugal
Jorge Almiro Pinto Paiva
Institute of Plant Genetics, Department of Integrative Plant Biology, Polish Academy of Sciences, ul. Strzeszyńska 34, 60-479, Poznan, Poland
Jorge Almiro Pinto Paiva

Authors

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

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Correspondence to Mercè Figueras.

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11103_2017_682_MOESM1_ESM.tif

Fig. S1. Workflow of sequencing, assembly, annotation and differential expression analyses (TIF 9517 KB)

11103_2017_682_MOESM2_ESM.xlsx

Table S1. Functional annotation of contigs and gene expression values in 454 libraries. (XLSX 2528 KB)

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Table S2. For each contig A) gene ontology terms and B) MapMan annotations are shown (XLSX 2943 KB)

Table S3. Sequences of the primers (PDF 231 KB)

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Table S4. Statistics of the 454 sequencing, transcriptome assembly and functional annotation of contigs (PDF 331 KB)

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Table S5. Gene ontology enrichment of the differentially regulated contigs (XLSX 389 KB)

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Table S6. Classification in accordance with Arabidopsis databases for carbohydrates and acyl-lipid metabolism (XLSX 54 KB)

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Boher, P., Soler, M., Sánchez, A. et al. A comparative transcriptomic approach to understanding the formation of cork. Plant Mol Biol 96, 103–118 (2018). https://doi.org/10.1007/s11103-017-0682-9

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Received: 24 August 2017
Accepted: 08 November 2017
Published: 15 November 2017
Issue Date: January 2018
DOI: https://doi.org/10.1007/s11103-017-0682-9

Keywords

Cork
Cork oak
Phellem
Rhytidome
Suberin
Wax

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Acknowledgements

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Contributions

Corresponding author

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Conflict of interest

Electronic supplementary material

11103_2017_682_MOESM1_ESM.tif

11103_2017_682_MOESM2_ESM.xlsx

11103_2017_682_MOESM3_ESM.xlsx

Table S3. Sequences of the primers (PDF 231 KB)

11103_2017_682_MOESM5_ESM.pdf

11103_2017_682_MOESM6_ESM.xlsx

11103_2017_682_MOESM7_ESM.xlsx

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