Oak genome reveals facets of long lifespan

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes1 but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times2. With 450 species spread throughout Asia, Europe and America3, oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical4 and modelling5 approaches have shown that intra-organismal genetic heterogeneity can be selected for6 and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes7. However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.Oaks can live hundreds of years. Comparative genomics using a high-quality genome sequence provides new insights that may explain tree longevity. Samples from branches and corresponding acorns also help quantify heritable somatic mutations.

Olivier Panaud | Hadi Quesneville | Franck Salin | Mohammed-Amin Madoui | Karine Labadie | Patrick Wincker | Jean-Marc Aury | Christophe Klopp | Francis Martin | Sébastien Faye | Célia Michotey | Arnaud Lemainque | Florian Maumus | Sébastien Duplessis | François Ehrenmann | Corinne Da Silva | Jonathan Mercier | Isabelle Luyten | Jérôme Salse | Florent Murat | Nathalie Chantret | Martin Lascoux | David Cohen | Jean-Charles Leplé | Jun Chen | Emilie Chancerel | Erwan Guichoux | Carole Dossat | Mika Tarkka | Grégoire Le Provost | Christophe Plomion | Jacqueline Grima-Pettenati | Christine Gaspin | Thibault Leroy | Caroline Belser | Céline Lalanne | Hélène Bergès | Antoine Kremer | Jérôme Bartholomé | Valérie Barbe | P. Wincker | A. Zanne | A. Couloux | V. Barbe | H. Quesneville | A. Lemainque | J. Aury | S. Mangenot | M. Lascoux | Florent Murat | Marçal Soler | J. Grima-Pettenati | J. Salse | C. Dossat | K. Labadie | Florian Maumus | S. Duplessis | A. Kohler | J. Leplé | P. Hugueney | C. Gaspin | N. Rouhier | F. Martin | M. Desprez-Loustau | O. Panaud | C. Plomion | M. Bogeat-Triboulot | A. Diévart | I. Luyten | Caroline Belser | Jonathan Mercier | J. Amselem | Mohammed-Amin Madoui | C. da Silva | D. Cohen | S. Herrmann | M. Tarkka | C. Klopp | H. Bergès | F. Salin | E. Lasserre | B. Brachi | E. Chancerel | O. Rué | I. Lesur | I. Hummel | G. Le Provost | N. Chantret | S. Faye | A. Kremer | Thibault Leroy | J. Bartholomé | C. Lalanne | P. Faivre-Rampant | Camille Rustenholz | Amy E Zanne | Arnaud Hecker | F. Ehrenmann | N. Picault | Nathalie Picault | Marçal Soler | C. Bodénès | Arnaud Couloux | E. Guichoux | Marie-Lara Bouffaud | Nicolas Francillonne | Jun Chen | Tina Alaeitabar | Clémence Marchal | C. Michotey | C. Rustenholz | Amandine Velt | Annegret Kohler | Benjamin Brachi | Arnaud Hecker | Sophie Mangenot | Nicolas Rouhier | Clémence Marchal | Marie-Laure Desprez-Loustau | Philippe Hugueney | Irène Hummel | Catherine Bodénès | Anne Diévart | Joëlle Amselem | Tina Alaeitabar | Nicolas Francillonne | Isabelle Lesur | Patricia Faivre-Rampant | Sylvie Herrmann | Marie-Béatrice Bogeat-Triboulot | Marie-Lara Bouffaud | Eric Lasserre | Olivier Rué | Amandine Velt | C. Bodénès | N. Francillonne | É. Chancerel | F. Martin | Isabelle Luyten | Célia Michotey | Iréne Hummel | Marie-Béatrice Bogeat-Triboulot | Marie‐Lara Bouffaud | M. Bouffaud

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