Drivers and dynamics of diversity in plant genomes


Plant Genome Dynamics Meeting, Banyuls-sur-Mer, France, September 2013

A meeting of c. 40 leading plant genome and evolutionary biologists from Europe, North and South America was held 12–13 September 2013, in Banyuls-sur-Mer, France. The meeting, entitled Plant Genome Dynamics, was organized by Olivier Panaud (University of Perpignan, France), Scott Jackson (University of Georgia, USA), and Jonathan Wendel (Iowa State University, USA). The principle goals were to share recent insights in plant evolutionary genomics, and by doing so attempt to identify larger, unanswered questions and promising directions for future research in this field. In addition to scientific presentations, roundtable discussions were built into the agenda. This structure and size of the meeting were designed to stimulate discussion and synthesis. The scientific organization was built around what arguably are the two most important realizations about plant genome evolution that have emerged from the genomics era, that is, that all plants have evolutionary histories that include multiple rounds of whole genome doubling; and that the major contributor to plant genome dynamics and differentiation has been the differential and lineage-specific proliferation (and subsequent deletional processes) of various classes of transposable elements (TEs) (Kellogg & Bennetzen, 2004). Accordingly, the two days of talks and discussions were divided into three primary topic areas: (1) polyploidy; (2) TEs and genome evolution; and (3) genome evolution – from populations to species. Here we summarize key points from the meeting as well as ‘Grand challenges’ for the broader plant community to help direct future research and funding.

‘This search for ‘evolutionary significance’ was, in fact, a recurring theme during the conference.’

Summary of Workshop presentations


The first of the three sessions focused on whole genome duplication, or polyploidy. Six speakers addressed topics ranging from the immediate, or long-term, consequences of polyploidy with respect to genome organization and evolution, to the relevance of the phenomenon to plant diversification. Eric Schranz (Wageningen University, the Netherlands) demonstrated how phylogenetically informed comparative genomics offers insights into genome structure and fractionation following polyploidy in the Brassicales (Cheng et al., 2013). He also reviewed evidence for a pattern of persistent time lag between polyploidy events and bursts of speciation in the angiosperms (Schranz et al., 2012). Pam Soltis (University of Florida, USA) focused on the immediate consequences of polyploidy in the well-known model system Tragopogon, in which three allopolyploid species have repeatedly formed from three introduced diploids in western North America in the last 100 yr. She highlighted the immediate and rapid chromosomal evolution and high frequency of gene loss that occurred in different populations of these allopolyploids (Buggs et al., 2012; Chester et al., 2012, 2013; Lipman et al., 2013). The immediate genomic effects of allopolyploidy were also highlighted by the next speaker, Karine Alix (AgroParisTech/UMR de génétique végétale du Moulon, France), who presented new information on rapid small RNA response and TE amplification in synthetic allopolyploid Brassica napus (Sarilar et al., 2013). Doug Soltis (University of Florida, USA) shifted gears and looked at polyploidy on the grand scale, focusing on the phylogenetic distribution of genome doubling events and their effects on plant diversification. Like a number of other speakers in the conference, he pointed out the benefits that will derive from broader sampling of diverse plant groups, emphasizing that this will be essential to infer general principles that govern the evolution and evolutionary significance of plant polyploids. Malika Ainouche and Armel Salmon (Université de Rennes, France) presented a tag-team demonstration of the complexity of working with a neo-allododecaploid, Spartina anglica, an ecologically important tidal grass derived from recent hybridization (followed by doubling) of the introduced S. alterniflora with the native European S. maritima (Ainouche et al., 2012; Ferreira de Carvalho et al., 2013). Their presentation on Spartina, supplemented by a briefer exposition on Lupinus, underscored the importance of ecological context for evolution in polyploids. The complexity of studying plants that have higher ploidy levels was similarly noted by Angélique D'Hont (CIRAD, Montpellier, France), who, in addition to reviewing features of the newly sequenced banana genome, presented detailed BAC sequence analyses for homoeologous segments in the decaploid sugarcane; one remarkable result, particularly in light of the rapid evolution observed in Tragopogon (as discussed by Pam Soltis), is the general stasis observed in terms of homoeolog structure and gene retention, apparently across all genomic copies.

Transposable elements (TEs) and genome evolution

The session dedicated to the evolutionary impact of transposable elements gathered seven speakers: Josep Casacuberta (CRAG Barcelona, Spain), Marie Mirouze (IRD, France), Esther van der Knaap (Ohio state University, USA), Marie-Angèle Grandbastien (INRA Versailles, France), Thomas Wicker (University of Zürich, Switzerland), Natasha-Marie Glover (INRA Clermont Ferrand, France) and Clémentine Vitte (CNRS/UMR de génétique végétale du Moulon, Gif-sur-Yvette/Yvette, France). Thomas Wicker presented the discovery of new types of TEs, based on the analysis of the genome sequences of species that belong to under-studied taxonomic groups, thus showing that the overall diversity of TEs in eukaryotes is far from being fully documented (T. Wicker, unpublished data). Natasha-Marie Glover presented the analysis of the TE repertoire of the wheat genome. This very large plant genome is one of the most challenging models for genome sequencing in crops. She showed that TEs form the vast majority of this genome, highlighting that, for example, 88% of chromosome 3B is composed of TEs (Choulet et al., 2010). Clémentine Vitte presented genome-wide analyses of structural variations in maize. Comparative study of the genome sequence of two maize inbred lines showed that 16 Mbp of sequence is cultivar-specific, thereby demonstrating both TE- and non TE-mediated genome differentiation at the intra-specific level (C. Vitte, unpublished data). Three presentations concerned the functional impact of TEs on plant genomes. First, Esther van der Knaap, showed the impact of Rider, a recently amplified long terminal repeat (LTR) retrotransposon, on fruit shape in tomato (Xiao et al., 2008), while Josep Casacuberta showed how MITE families recently amplified a transcription factor (E2F) binding site in the Brassica genome through transposition. He showed the putative impact of this TE family upon insertion in the vicinity of genes (J. Casacuberta, unpublished data). Marie-Angèle Grandbastien described work on the overall impact of the Tnt1 LTR retrotransposon on stress responses in tobacco. Tnt1 harbors variable regulatory sequences in its LTRs, and several subfamilies exhibit different transcriptional activation patterns, with differential responses to microbial factors in different materials (leaves or cell cultures) (M-A. Grandbastien, unpublished data). Finally, Marie Mirouze presented her work on the epigenetic control of transposition in Arabidopsis thaliana (Bucher et al., 2012) for which several pathways have been well described in this model species. She showed how the impediment of one or several of these pathways could lead to the activation of transposition. She also presented some recent findings on the characterization of extrachromosomal forms of TEs (the mobilome; M. Mirouze, unpublished data).

Genome evolution – from populations to species

The final session included seven presentations, from Michael Purugganan (New York University, USA), Jerome Salse (INRA, France), Ana Caicedo (University of Massachussetts, USA), Andrew Leitch (Queen Mary University, UK), Antonio Costa de Oliveira (Federal University of Pelotas, Brazil), Jim Leebens-Mack (University of Georgia, USA) and John Burke (University of Georgia, USA). Michael Purugganan highlighted the effect of genome architecture on distribution of genetic variation within species and populations and presented the question of how to go from a ‘collection of single-nucleotide polymorphisms (SNPs) and structural variation among genomes or within species’ to identification of ‘those that have functional or evolutionary significance’(Flowers et al., 2012).

This search for ‘evolutionary significance’ was, in fact, a recurring theme during the conference. Jerome Salse presented comparative analyses of plant genomes and reconstruction of ancestral genomes and genes, noting how genes have functionally evolved and the utility of comparative/evolutionary genomics for understanding the basis of agricultural traits, for example nitrogen use in cereals (Quraishi et al., 2011a,b). Ana Caicedo presented an example of de-domestication of crops to weeds using weedy rice as an example, illustrating both multiple origins of weedy phenotypes and the lack of convergence at the genomic level for this apparent phenotypic convergence (Reagon et al., 2010; Thurber et al., 2013). Andrew Leitch reviewed data on the remarkable variation in plant genome sizes and presented a thought provoking analysis of ecological factors constraining genome size. The work of Antonio Costa de Oliveira on iron-related genes and the role of gene duplication in rice was a good example of the impact of evolutionary processes on important agricultural traits (Victoria et al., 2012). Jim Leebens-Mack echoed the earlier talks by Doug Soltis and others, in emphasizing the importance of sampling broadly across the plant kingdom to understand gene and gene family evolution and how such sampling is yielding more precise estimates of the timing of events such as polyploidy (Soltis et al., 2009; Jiao et al., 2011, 2012; McKain et al., 2012). He also questioned whether the processes that may spur diversification immediately following polyploidy are the same as those that sustain diversification over the long run. John Burke presented an update on sunflower genomics, here specifically addressing the impact of chromosome rearrangements on interspecific gene flow within rearranged regions and near breakpoints, and hence their potential role in speciation (J. Burke, unpublished data). He also highlighted the challenge of distinguishing the ecological or evolutionary effects of rearrangements themselves from those due to genes contained therein.

Synthesis and perspectives

Although the presentations in the three formal sessions and the numerous discussions over the two days covered an extraordinary diversity of topics and model systems, it became apparent by the end that several key perspectives were recurrent, and that these are at least loosely interwoven. One of these concerns the overriding goal of many in our field, namely, to describe and understand the sheer diversity of plant genomes, which are extraordinarily variable in so many aspects of their genomes, including size, resident populations of TEs and their histories, other repetitive elements, footprints of past whole genome doubling events, and the full spectrum of RNA encoding elements. While some speakers offered long-term perspectives on various aspects of this diversity, involving the full sweep of angiosperm history and beyond, others concentrated on genome evolution and diversification at the population and species level. This ‘genome centered’ perspective was balanced by a more ‘organismal’ perspective, where the goal is to understand the effects of genomic processes such as polyploidy or TE proliferation on speciation and cladogenesis, or the relationships between genomic variants of various kinds and phenotypes, or fitness. An additional recurring idea was the challenge to reconcile the here and now of genome evolution within and among populations with the enormous range of genome variation that is extant among modern plant lineages. Finally, we were reminded, in a number of talks, that all evolution takes place in an ecological context, and that understanding the interplay of extrinsic, population-level and ecological forces may be essential to understanding the genesis of intrinsic, genomic structures.


The meeting involved the following participants: Karine Alix (AgroParisTech/UMR de génétique végétale du Moulon, France); Kader Ainouche (Université de Rennes, France); Malika Ainouche (Université de Rennes, France); John Burke (University of Georgia, USA): Ana Caicedo (University of Massachussets, USA); Marie-christine Carpentier (University of Perpignan, France); Josep Casacuberta (CRAG Barcelona, Spain); Richard Cooke (University of Perpignan, France); Antonio Costa de Oliveira (Federal University of Pelotas, Brazil); Emilie Debladis (IRD, Montpellier, France); Michel Delseny (University of Perpignan, France); Angélique D'Hont (CIRAD Montpellier, France); Natasha-Marie Glover (INRA, Clermont Ferrrand, France); Marie-Angèle Grandbastien (INRA Versailles, France); Elisabeth Henaff (CRAG, Barcelona, Spain); Eric Lasserre (University of Perpignan, France); Andrew Leitch (Queen Mary University, UK); Jim Leebens-Mack (University of Georgia, USA); Christel Llauro (Université de Perpignan, France); Marie Mirouze (IRD Montpellier, France); Nathalie Picault (University of Perpignan, France); Michael Purugganan (New York University, USA); Mathieu Rousseau (Université de Rennes, France); Armel Salmon (Université de Rennes, France); Jérôme Salse (INRA Clermont-Ferrand, France); Eric Schranz (Wageningen University, The Netherlands); Doug Soltis (University of Florida, USA); Pam Soltis (University of Florida, USA); Esther van der Knaap (Ohio State University, USA); Clémentine Vitte (CNRS/UMR de génétique végétale du Moulon, France); and Thomas Wicker (University of Zürich, Switzerland).