Analysis of gene expression patterns in animals

During my PhD, my aim was to provide new tools to increase our capacity to analyse gene expression patterns, and to study on a large-scale basis the evolution of gene expression in animals. Gene expression patterns (when and where a gene is expressed) are a key feature in understanding gene function, notably in development. It appears clear now that the evolution of developmental processes and of phenotypes is shaped both by evolution at the coding sequence level, and at the gene expression level.Studying gene expression evolution in animals, with complex expression patterns over tissues and developmental time, is still challenging. No tools are available to routinely compare expression patterns between different species, with precision, and on a large-scale basis. Studies on gene expression evolution are therefore performed only on small genes datasets, or using imprecise descriptions of expression patterns.The aim of my PhD was thus to develop and use novel bioinformatics resources, to study the evolution of gene expression. To this end, I developed the database Bgee (Base for Gene Expression Evolution). The approach of Bgee is to transform heterogeneous expression data (ESTs, microarrays, and in-situ hybridizations) into present/absent calls, and to annotate them to standard representations of anatomy and development of different species (anatomical ontologies). An extensive mapping between anatomies of species is then developed based on hypothesis of homology. These precise annotations to anatomies, and this extensive mapping between species, are the major assets of Bgee, and have required the involvement of many co-workers over the years. My main personal contribution is the development and the management of both the Bgee database and the web-application.Bgee is now on its ninth release, and includes an important gene expression dataset for 5 species (human, mouse, drosophila, zebrafish, Xenopus), with the most data from mouse, human and zebrafish. Using these three species, I have conducted an analysis of gene expression evolution after duplication in vertebrates.Gene duplication is thought to be a major source of novelty in evolution, and to participate to speciation. It has been suggested that the evolution of gene expression patterns might participate in the retention of duplicate genes. I performed a large-scale comparison of expression patterns of hundreds of duplicated genes to their singleton ortholog in an outgroup, including both small and large-scale duplicates, in three vertebrate species (human, mouse and zebrafish), and using highly accurate descriptions of expression patterns. My results showed unexpectedly high rates of de novo acquisition of expression domains after duplication (neofunctionalization), at least as high or higher than rates of partitioning of expression domains (subfunctionalization). I found differences in the evolution of expression of small- and large-scale duplicates, with small-scale duplicates more prone to neofunctionalization. Duplicates with neofunctionalization seemed to evolve under more relaxed selective pressure on the coding sequence. Finally, even with abundant and precise expression data, the majority fate I recovered was neither neo- nor subfunctionalization of expression domains, suggesting a major role for other mechanisms in duplicate gene retention

BgeeDB, an R package for retrieval of curated expression datasets and for gene list expression localization enrichment tests.

BgeeDB is a collection of functions to import into R re-annotated, quality-controlled and re-processed expression data available in the Bgee database. This includes data from thousands of wild-type healthy samples of multiple animal species, generated with different gene expression technologies (RNA-seq, Affymetrix microarrays, expressed sequence tags, and in situ hybridizations). BgeeDB facilitates downstream analyses, such as gene expression analyses with other Bioconductor packages. Moreover, BgeeDB includes a new gene set enrichment test for preferred localization of expression of genes in anatomical structures ("TopAnat"). Along with the classical Gene Ontology enrichment test, this test provides a complementary way to interpret gene lists. Availability: https://www.bioconductor.org/packages/BgeeDB/

Unification of multi-species vertebrate anatomy ontologies for comparative biology in Uberon.

BACKGROUND: Elucidating disease and developmental dysfunction requires understanding variation in phenotype. Single-species model organism anatomy ontologies (ssAOs) have been established to represent this variation. Multi-species anatomy ontologies (msAOs; vertebrate skeletal, vertebrate homologous, teleost, amphibian AOs) have been developed to represent 'natural' phenotypic variation across species. Our aim has been to integrate ssAOs and msAOs for various purposes, including establishing links between phenotypic variation and candidate genes. RESULTS: Previously, msAOs contained a mixture of unique and overlapping content. This hampered integration and coordination due to the need to maintain cross-references or inter-ontology equivalence axioms to the ssAOs, or to perform large-scale obsolescence and modular import. Here we present the unification of anatomy ontologies into Uberon, a single ontology resource that enables interoperability among disparate data and research groups. As a consequence, independent development of TAO, VSAO, AAO, and vHOG has been discontinued. CONCLUSIONS: The newly broadened Uberon ontology is a unified cross-taxon resource for metazoans (animals) that has been substantially expanded to include a broad diversity of vertebrate anatomical structures, permitting reasoning across anatomical variation in extinct and extant taxa. Uberon is a core resource that supports single- and cross-species queries for candidate genes using annotations for phenotypes from the systematics, biodiversity, medical, and model organism communities, while also providing entities for logical definitions in the Cell and Gene Ontologies. THE ONTOLOGY RELEASE FILES ASSOCIATED WITH THE ONTOLOGY MERGE DESCRIBED IN THIS MANUSCRIPT ARE AVAILABLE AT: http://purl.obolibrary.org/obo/uberon/releases/2013-02-21/ CURRENT ONTOLOGY RELEASE FILES ARE AVAILABLE ALWAYS AVAILABLE AT: http://purl.obolibrary.org/obo/uberon/releases

TRY plant trait database – enhanced coverage and open access

Plant traits—the morphological, anatomical, physiological, biochemical and phenological characteristics of plants—determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait-based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits—almost complete coverage for ‘plant growth form’. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait–environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects. We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives.Rest of authors: Decky Junaedi, Robert R. Junker, Eric Justes, Richard Kabzems, Jeffrey Kane, Zdenek Kaplan, Teja Kattenborn, Lyudmila Kavelenova, Elizabeth Kearsley, Anne Kempel, Tanaka Kenzo, Andrew Kerkhoff, Mohammed I. Khalil, Nicole L. Kinlock, Wilm Daniel Kissling, Kaoru Kitajima, Thomas Kitzberger, Rasmus Kjøller, Tamir Klein, Michael Kleyer, Jitka Klimešová, Joice Klipel, Brian Kloeppel, Stefan Klotz, Johannes M. H. Knops, Takashi Kohyama, Fumito Koike, Johannes Kollmann, Benjamin Komac, Kimberly Komatsu, Christian König, Nathan J. B. Kraft, Koen Kramer, Holger Kreft, Ingolf Kühn, Dushan Kumarathunge, Jonas Kuppler, Hiroko Kurokawa, Yoko Kurosawa, Shem Kuyah, Jean-Paul Laclau, Benoit Lafleur, Erik Lallai, Eric Lamb, Andrea Lamprecht, Daniel J. Larkin, Daniel Laughlin, Yoann Le Bagousse-Pinguet, Guerric le Maire, Peter C. le Roux, Elizabeth le Roux, Tali Lee, Frederic Lens, Simon L. Lewis, Barbara Lhotsky, Yuanzhi Li, Xine Li, Jeremy W. Lichstein, Mario Liebergesell, Jun Ying Lim, Yan-Shih Lin, Juan Carlos Linares, Chunjiang Liu, Daijun Liu, Udayangani Liu, Stuart Livingstone, Joan Llusià, Madelon Lohbeck, Álvaro López-García, Gabriela Lopez-Gonzalez, Zdeňka Lososová, Frédérique Louault, Balázs A. Lukács, Petr Lukeš, Yunjian Luo, Michele Lussu, Siyan Ma, Camilla Maciel Rabelo Pereira, Michelle Mack, Vincent Maire, Annikki Mäkelä, Harri Mäkinen, Ana Claudia Mendes Malhado, Azim Mallik, Peter Manning, Stefano Manzoni, Zuleica Marchetti, Luca Marchino, Vinicius Marcilio-Silva, Eric Marcon, Michela Marignani, Lars Markesteijn, Adam Martin, Cristina Martínez-Garza, Jordi Martínez-Vilalta, Tereza Mašková, Kelly Mason, Norman Mason, Tara Joy Massad, Jacynthe Masse, Itay Mayrose, James McCarthy, M. Luke McCormack, Katherine McCulloh, Ian R. McFadden, Brian J. McGill, Mara Y. McPartland, Juliana S. Medeiros, Belinda Medlyn, Pierre Meerts, Zia Mehrabi, Patrick Meir, Felipe P. L. Melo, Maurizio Mencuccini, Céline Meredieu, Julie Messier, Ilona Mészáros, Juha Metsaranta, Sean T. Michaletz, Chrysanthi Michelaki, Svetlana Migalina, Ruben Milla, Jesse E. D. Miller, Vanessa Minden, Ray Ming, Karel Mokany, Angela T. Moles, Attila Molnár V, Jane Molofsky, Martin Molz, Rebecca A. Montgomery, Arnaud Monty, Lenka Moravcová, Alvaro Moreno-Martínez, Marco Moretti, Akira S. Mori, Shigeta Mori, Dave Morris, Jane Morrison, Ladislav Mucina, Sandra Mueller, Christopher D. Muir, Sandra Cristina Müller, François Munoz, Isla H. Myers-Smith, Randall W. Myster, Masahiro Nagano, Shawna Naidu, Ayyappan Narayanan, Balachandran Natesan, Luka Negoita, Andrew S. Nelson, Eike Lena Neuschulz, Jian Ni, Georg Niedrist, Jhon Nieto, Ülo Niinemets, Rachael Nolan, Henning Nottebrock, Yann Nouvellon, Alexander Novakovskiy, The Nutrient Network, Kristin Odden Nystuen, Anthony O'Grady, Kevin O'Hara, Andrew O'Reilly-Nugent, Simon Oakley, Walter Oberhuber, Toshiyuki Ohtsuka, Ricardo Oliveira, Kinga Öllerer, Mark E. Olson, Vladimir Onipchenko, Yusuke Onoda, Renske E. Onstein, Jenny C. Ordonez, Noriyuki Osada, Ivika Ostonen, Gianluigi Ottaviani, Sarah Otto, Gerhard E. Overbeck, Wim A. Ozinga, Anna T. Pahl, C. E. Timothy Paine, Robin J. Pakeman, Aristotelis C. Papageorgiou, Evgeniya Parfionova, Meelis Pärtel, Marco Patacca, Susana Paula, Juraj Paule, Harald Pauli, Juli G. Pausas, Begoña Peco, Josep Penuelas, Antonio Perea, Pablo Luis Peri, Ana Carolina Petisco-Souza, Alessandro Petraglia, Any Mary Petritan, Oliver L. Phillips, Simon Pierce, Valério D. Pillar, Jan Pisek, Alexandr Pomogaybin, Hendrik Poorter, Angelika Portsmuth, Peter Poschlod, Catherine Potvin, Devon Pounds, A. Shafer Powell, Sally A. Power, Andreas Prinzing, Giacomo Puglielli, Petr Pyšek, Valerie Raevel, Anja Rammig, Johannes Ransijn, Courtenay A. Ray, Peter B. Reich, Markus Reichstein, Douglas E. B. Reid, Maxime Réjou-Méchain, Victor Resco de Dios, Sabina Ribeiro, Sarah Richardson, Kersti Riibak, Matthias C. Rillig, Fiamma Riviera, Elisabeth M. R. Robert, Scott Roberts, Bjorn Robroek, Adam Roddy, Arthur Vinicius Rodrigues, Alistair Rogers, Emily Rollinson, Victor Rolo, Christine Römermann, Dina Ronzhina, Christiane Roscher, Julieta A. Rosell, Milena Fermina Rosenfield, Christian Rossi, David B. Roy, Samuel Royer-Tardif, Nadja Rüger, Ricardo Ruiz-Peinado, Sabine B. Rumpf, Graciela M. Rusch, Masahiro Ryo, Lawren Sack, Angela Saldaña, Beatriz Salgado-Negret, Roberto Salguero-Gomez, Ignacio Santa-Regina, Ana Carolina Santacruz-García, Joaquim Santos, Jordi Sardans, Brandon Schamp, Michael Scherer-Lorenzen, Matthias Schleuning, Bernhard Schmid, Marco Schmidt, Sylvain Schmitt, Julio V. Schneider, Simon D. Schowanek, Julian Schrader, Franziska Schrodt, Bernhard Schuldt, Frank Schurr, Galia Selaya Garvizu, Marina Semchenko, Colleen Seymour, Julia C. Sfair, Joanne M. Sharpe, Christine S. Sheppard, Serge Sheremetiev, Satomi Shiodera, Bill Shipley, Tanvir Ahmed Shovon, Alrun Siebenkäs, Carlos Sierra, Vasco Silva, Mateus Silva, Tommaso Sitzia, Henrik Sjöman, Martijn Slot, Nicholas G. Smith, Darwin Sodhi, Pamela Soltis, Douglas Soltis, Ben Somers, Grégory Sonnier, Mia Vedel Sørensen, Enio Egon Sosinski Jr, Nadejda A. Soudzilovskaia, Alexandre F. Souza, Marko Spasojevic, Marta Gaia Sperandii, Amanda B. Stan, James Stegen, Klaus Steinbauer, Jörg G. Stephan, Frank Sterck, Dejan B. Stojanovic, Tanya Strydom, Maria Laura Suarez, Jens-Christian Svenning, Ivana Svitková, Marek Svitok, Miroslav Svoboda, Emily Swaine, Nathan Swenson, Marcelo Tabarelli, Kentaro Takagi, Ulrike Tappeiner, Rubén Tarifa, Simon Tauugourdeau, Cagatay Tavsanoglu, Mariska te Beest, Leho Tedersoo, Nelson Thiffault, Dominik Thom, Evert Thomas, Ken Thompson, Peter E. Thornton, Wilfried Thuiller, Lubomír Tichý, David Tissue, Mark G. Tjoelker, David Yue Phin Tng, Joseph Tobias, Péter Török, Tonantzin Tarin, José M. Torres-Ruiz, Béla Tóthmérész, Martina Treurnicht, Valeria Trivellone, Franck Trolliet, Volodymyr Trotsiuk, James L. Tsakalos, Ioannis Tsiripidis, Niklas Tysklind, Toru Umehara, Vladimir Usoltsev, Matthew Vadeboncoeur, Jamil Vaezi, Fernando Valladares, Jana Vamosi, Peter M. van Bodegom, Michiel van Breugel, Elisa Van Cleemput, Martine van de Weg, Stephni van der Merwe, Fons van der Plas, Masha T. van der Sande, Mark van Kleunen, Koenraad Van Meerbeek, Mark Vanderwel, Kim André Vanselow, Angelica Vårhammar, Laura Varone, Maribel Yesenia Vasquez Valderrama, Kiril Vassilev, Mark Vellend, Erik J. Veneklaas, Hans Verbeeck, Kris Verheyen, Alexander Vibrans, Ima Vieira, Jaime Villacís, Cyrille Violle, Pandi Vivek, Katrin Wagner, Matthew Waldram, Anthony Waldron, Anthony P. Walker, Martyn Waller, Gabriel Walther, Han Wang, Feng Wang, Weiqi Wang, Harry Watkins, James Watkins, Ulrich Weber, James T. Weedon, Liping Wei, Patrick Weigelt, Evan Weiher, Aidan W. Wells, Camilla Wellstein, Elizabeth Wenk, Mark Westoby, Alana Westwood, Philip John White, Mark Whitten, Mathew Williams, Daniel E. Winkler, Klaus Winter, Chevonne Womack, Ian J. Wright, S. Joseph Wright, Justin Wright, Bruno X. Pinho, Fabiano Ximenes, Toshihiro Yamada, Keiko Yamaji, Ruth Yanai, Nikolay Yankov, Benjamin Yguel, Kátia Janaina Zanini, Amy E. Zanne, David Zelený, Yun-Peng Zhao, Jingming Zheng, Ji Zheng, Kasia Ziemińska, Chad R. Zirbel, Georg Zizka, Irié Casimir Zo-Bi, Gerhard Zotz, Christian Wirth.Max Planck Institute for Biogeochemistry; Max Planck Society; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig; International Programme of Biodiversity Science (DIVERSITAS); International Geosphere-Biosphere Programme (IGBP); Future Earth; French Foundation for Biodiversity Research (FRB); GIS ‘Climat, Environnement et Société'.http://wileyonlinelibrary.com/journal/gcbhj2021Plant Production and Soil Scienc