The oak gene expression atlas: insights into Fagaceae genome evolution and the discovery of genes regulated during bud dormancy release

AIT Austrian Institute of Technology GmbH, Konrad-Lorenz Str Lesur et al. - The oak gene expression atlas: insights into Fagaceae genome evolution and the discovery of genes regulated during bud dormancy release Open Access The oak gene expression atlas: insights into Fagaceae genome evolution and the discovery of genes regulated during bud dormancy release Isabelle Lesur1,2, Grgoire Le Provost1,5, Pascal Bento3, Corinne Da Silva3, Jean-Charles Lepl6, Florent Murat7, Saneyoshi Ueno4, Jerme Bartholom1,8, Cline Lalanne1,5, Franois Ehrenmann1,5, Cline Noirot9, Christian Burban1,5, Valrie Lger1,5, Joelle Amselem10, Caroline Belser3, Hadi Quesneville10, Michael Stierschneider11, Silvia Fluch11, Lasse Feldhahn12, Mika Tarkka12,13, Sylvie Herrmann13,14, Franois Buscot12,13, Christophe Klopp9, Antoine Kremer1,5, Jrme Salse7, Jean-Marc Aury3 and Christophe Plomion1,5* Background: Many northern-hemisphere forests are dominated by oaks. These species extend over diverse environmental conditions and are thus interesting models for studies of plant adaptation and speciation. The genomic toolbox is an important asset for exploring the functional variation associated with natural selection. Results: The assembly of previously available and newly developed long and short sequence reads for two sympatric oak species, Quercus robur and Quercus petraea, generated a comprehensive catalog of transcripts for oak. The functional annotation of 91 k contigs demonstrated the presence of a large proportion of plant genes in this unigene set. Comparisons with SwissProt accessions and five plant gene models revealed orthologous relationships, making it possible to decipher the evolution of the oak genome. In particular, it was possible to align 9.5 thousand oak coding sequences with the equivalent sequences on peach chromosomes. Finally, RNA-seq data shed new light on the gene networks underlying vegetative bud dormancy release, a key stage in development allowing plants to adapt their phenology to the environment. Conclusion: In addition to providing a vast array of expressed genes, this study generated essential information about oak genome evolution and the regulation of genes associated with vegetative bud phenology, an important adaptive traits in trees. This resource contributes to the annotation of the oak genome sequence and will provide support for forward genetics approaches aiming to link genotypes with adaptive phenotypes. Background Many northern-hemisphere forests are dominated by evergreen and deciduous oaks (Quercus spp.). The genus Quercus consists of about 400 species extending over a wide range of environmental conditions, from temperate to subtropical regions. Some sympatric species (such as Q. robur, Q. petraea, Q. pyrenaica, Q. faginea, and Q. pubescens in Europe) occupy different ecological niches [1] and are therefore interesting models for studies of * Correspondence: 1INRA, UMR1202, BIOGECO, F-33610, Cestas, France 5University Bordeaux, BIOGECO, UMR1202, F-33170, Talence, France Full list of author information is available at the end of the article plant adaptation [2] and ecological speciation [3]. An important question in biological science concerns the response of these long-lived organisms to rapid environmental change, their ability to evolve and the mechanisms involved. The genes and associated structural and expressional variants required for adaptation must be identified if we are to address these questions. To this end, a number of genomic tools and resources have been developed for oaks (reviewed in [4]), including two bacterial artificial chromosome (BAC) libraries [5], a large number of SSRs [6] that have been used to generate linkage maps [7] and expressed sequence tags (ESTs), mostly obtained by Sanger and Roche 454 sequencing [8,9]. Researchers can 2015 Lesur et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. now use these tools to address concerns about the adaptability of forest trees at the genomic level. However, studies aiming to address this objective have been hampered by a lack of genomic resources. Ultra-deep sequencing methods, in particular, could help to expand the oak transcript catalog for studies of the genomic mechanisms underlying plastic responses and evolutionary adaptation to environmental change. RNA-seq is a method of choice for quantifying gene expression [10,11], and for identifying genes preferentially expressed at specific developmental stages [11] or in specific physiological conditions [12]. RNA-seq can be used to infer gene regulatory networks on the basis of enrichment analysis for pathways and gene ontology groups [13], using established knowledge from model organisms [14], or with dedicated statistical approaches [15] for the de novo identification of sets of co-expressed genes. In this study, RNAseq was used to identify genes regulated during bud dormancy release, an important phase of vegetative bud phenology, known to be strongly affected by temperature and photoperiod and therefore, likely to be greatly disturbed by the unprecedented warming associated with climate change [16]. Low temperatures are essential to overcome endo-dormancy (chilling requirement), but high temperatures are also required for bud break (heat requirement). The effect of climate change, with milder autumns and warmer winters, on the timing of bud flush and the impact of exposure to late spring frost are key questions in forestry requiring a detailed understanding of the physiological and molecular mechanisms (and their genetic variability) involved in dormancy release. We addressed these questions, by studying the dynamics of gene expression over this critical period, focusing on two successive phases of bud dormancy release: i) ecodormancy, a dormancy state prevailing in late winter and spring imposed by environmental conditions unfavorable for growth (i.e. heat requirement not fulfilled), and ii) swelling bud, which occurs in spring, just before bud burst, when the heat requirement for bud break is almost satisfied. Once established, transcriptome analysis can also be used in a comparative framework, to reveal some of the evolutionary features of a genome, through the inference of whole-genome duplication and speciation events, for example [17,18]. It has been proposed that modern eudicots have derived from a founder ancestral genome structured in 21 protochromosomes followed by series of whole genome duplications (WGD) or polyploidizations and ancestral chromosome fusions and fissions [19]. Polyploidi (...truncated)