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Final Report Summary - ORIGIN (The model plant system Trithuria (Hydatellaceae), a new window into the origin of flowering plants and gene function)

Flowering plants (angiosperms) are the dominant life form on land. They drive terrestrial ecosystems by using photosynthesis to produce most of our oxygen and complex nutrients. We depend on them, directly or indirectly, for almost all of our food, in addition to pharmaceuticals, textiles, timber and biofuel. A major difficulty in interpreting vast genomic data sets from single species is that plant genomes are known to be fluid over relatively short evolutionary time spans, due to substantial genomic turnover through gene duplication, diversification and extinction. Since all plant genes ultimately derive from duplication and subsequent diversification processes, understanding deep evolutionary history (phylogeny) is important for predicting the function of genes in multigene families (i. e., most genes). We now know that the two major flowering angiosperm groups (the monocots and eudicots) diverged from each other close to the origin of the flowering plants. As such, it would be invaluable to develop genomic tools for a model plant lineage that pre-dated this major evolutionary split. This would be broadly useful for plant biology research, as it would allow us to pinpoint which gene families predate vs. postdate the origin of most the world’s major crop plants and to reveal recent vs. ancient genes, permitting inference of gene orthologs, gene copies that are inherited in different plants through speciation events, vs. paralogs, gene copies derived from independently evolved genes or genome duplication events, which may often gain new functionality.

The main objective of ORIGIN is to unravel the evolutionary history of Trithuria by defining its species boundaries and by facilitating its use as an “early angiosperm” model plant to root studies of multigene family diversification and gene function. To reach this objective, three main goals have been defined.

Hydatellaceae: a new window into flowering plant origins. The genus Trithuria (family Hydatellaceae) is an excellent candidate plant to develop as a new model plant system for early angiosperms. This family originated very close to the origin of flowering-plant phylogeny. It is an attractive prospect for development as a new model-plant system because its stem lineage pre-dates the origin of monocots and eudicots, and the plants are small and easily cultivable while other early flowering plants are mostly long-lived trees. The new phylogenetic placement of Hydatellaceae near the origin of all flowering plants re-opens debates on early angiosperm evolution, including the origin of their basic reproductive biology and ecology. However, knowledge of species boundaries in Trithuria remains unexplored, therefore constraining its use as a new model plant and ultimately the development of genomic tools for detecting ortholog and paralog genes.

Goal 1: Define species boundaries and uncover phylogenetic relationships in Trithuria (Hydatellaceae).
Under this first goal, ORIGIN has addressed the taxonomic and genetic limits of species of Trithuria, helping to clarify the status of the current known species. In collaboration with the University of British Columbia (Canada), Kew Botanical Gardens (UK), University of Moscow (Russia), and University of Perth (Australia) several species new to science and to the public were found and described.

Goal 2: Resolve a key ambiguity in early plant evolution addressing where the root of flowering-plant phylogeny belong?
Pinpointing the root of angiosperm phylogeny is crucial for clarifying some of the remaining mysteries concerning flowering-plant origins. It is also critical for understanding the origin and subsequent radiation of gene families that arose close to the origin of flowering plants, and that have since then subsequently diversified spectacularly in major plant groups like the monocots and eudicots. These groups include almost of our major crop plants—e. g., rice, Oryza—and the model plant Brachypodium. As such, through this second defined goal, ORIGIN has published several articles clarifying the root of flowering-plant phylogeny with large-scale genomic evidence from the nuclear genome. ORIGIN has developed transcriptome data from Hydatellaceae and other early lineages of angiosperms that was complemented with data being produced in large-scale transcriptome data sets (such as the ‘1000 plant tanscriptome’ project) to (i) identify low or single-copy genes across these species for large-scale concatenated phylogenetic inference and (ii) use tree-reconciliation methods to infer early gene duplication events.

Goal 3: Determine the origin of ortholog and paralog genes on a large evolutionary scale
Having solved the genetic boundaries of the early-flowering plant Trithuria (Goal 1) and clarified the overall root of the angiosperm tree (Goal 2), ORIGIN used the developed genomic framework for the determination of orthologs vs. paralogs in other plant important groups, such as the monocot model plant Brachypodium (which is closely related to cereal crops). This goal, which was developed during the last year in the University of Zaragoza, aimed to identify the origin of gene families that control flowering in Brachypodium and trace back their evolutionary history relative to Trithuria and other angiosperms, identifying the origin of new gene functionality.

Originality and Innovative nature of the project, and relationship to the 'state of the art' of research in the field
The use of an early flowering-plant lineage facilitates our ability to distinguish which gene copies are orthologs versus paralogs in other plants by using tree reconciliation methods that consider (or co-predict) species phylogeny. Definition of species limits in Trithuria (Goal 1) will supply a key piece of information for the future development of this species as a model plant system. It will also have significance for developing future management strategies for conserving members of this family in the wild. Accurate rooting of flowering-plant phylogeny (Goal 2) will facilitate attempts to reconstruct early evolutionary transitions and the origin of new adaptations in plants. New inferences on the timing of the first splits in angiosperm evolution (Goals 1 and 2) are relevant to other phylogenetic and biogeographical plant studies like those using molecular dating methods. Contribution to the detection of which genes predate vs. postdate the origin of monocot and eudicot plants (Goal 3) is a crucial aspect for the European and global economy since these two groups include almost all of the crop plants that we rely on for our food and other natural resources. The international alliance created during ORIGIN has trained new students in this area of science, and will help to develop future coalitions of cooperation, ensuring an enabling environment for the study of early plant evolution in Europe.
The project website is available at https://isabelmarquesevolution.wordpress.com/. Updates on research are provided at https://isabelmarquesevolution.wordpress.com/origin-fp7/

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UNIVERSIDAD DE ZARAGOZA
Spain
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