The role of structural variation in adaptive radiation

Project Information

StrucRadiation

Grant agreement ID: 101066772

DOI

10.3030/101066772

Project closed

EC signature date 15 June 2022

Start date 15 August 2022

End date 14 August 2024

Funded under

• Marie Skłodowska-Curie Actions (MSCA)

Total cost

No data

EU contribution

€ 183 600,96

Coordinated by

UNIVERSITAT WIEN
Austria

Periodic Reporting for period 1 - StrucRadiation (The role of structural variation in adaptive radiation)

Reporting period: 2022-08-15 to 2024-08-14

Summary of the context and overall objectives of the project

Understanding how organisms adapt to changing environments is crucial for unravelling the mechanisms that drive biodiversity, a task that is becoming ever more pressing as species must respond to the challenges of a rapidly changing climate. An emerging factor in understanding adaptive evolution is the role of transposable elements (TEs) - selfish genetic elements which move and multiply throughout the host genome. While traditionally thought to be wholly harmful to the host, recent evidence from across the tree of life is beginning to suggest that TEs can represent an important driver of adaptive variation through their modification and modulation of host genetic pathways. However the stochastic and unpredictable nature of TEs proliferation makes it difficult to directly link their activity to adaptive traits.

To investigate the potential role of TEs in the emergence of adaptive traits, StrucRadiation focused on a New Caledonian clade of the persimmon genus Diospyros. Diospyros colonised New Caledonia, a remote Pacific archipelago, roughly ten million years ago, undergoing a rapid burst of speciation to form an adaptive radiation of 30 ecologically diverse species. These species now inhabit nearly all habitat types found in New Caledonia.

The unique geological history of New Caledonia has resulted in a variety of soil types, including fertile volcanic soil, calcium rich calcareous soil and nutritionally challenging serpentine and ultramafic soils. These soils, distributed in patches across the island, create a heterogeneous landscape of contrasting edaphic selection pressures. Serpentine and ultramafic soils, which are characterised by low nutrient availability, imbalanced mineral content and high concentrations of heavy metals, pose significant challenges for plant survival and growth. Interestingly, adaptation to these difficult soil types has evolved multiple times across the New Caledonian Diospyros adaptive radiation, with closely related species often exhibiting contrasting edaphic preferences.

Notably, species within this Diospyros New Caledonian radiation show a marked increase in TE proliferation compared to their closest relatives. The repeated adaptation in this clade of Diospyros to challenging and heterogeneously distributed ultramafic and serpentine soils on New Caledonia present an excellent opportunity to test the role of TEs in adaptive evolution. The aim of StrucRadiation is to investigate the potential association of TEs with ecologically relevant genes, focussing on genes related to adaptation to ultramafic and serpentine soils. By focusing on these soil-related adaptations, StrucRadiation aimed to shed light on how TEs may facilitate rapid evolution in response to environmental pressures, despite decreased starting levels of genetic variation.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

StrucRadiation aimed to leverage the repeated edaphic adaptations of New Caledonian Diospyros species to explore the relationship between transposable element (TE) dynamics and ecological adaptation in the face of new environmental opportunities.

Our first objective was to produce a comprehensive multi-trait dataset that integrates genomic, transcriptomic, physiological and environmental data for Diospyros species pairs with contrasting edaphic preferences across the New Caledonian adaptive radiation. Apart from gathering molecular data, we focused in particular on soil and leaf chemistry, together with quantifications of photosynthetic parameters. In collaboration with local plant nurseries in New Caledonia, we established a common garden experiment including selected ultramafic and volcanic species pairs. This common garden provided the material for transcriptomic analysis, and remains an easily accessible source of genetic material for Diospyros species in New Caledonia for ongoing studies of the system.

We assayed gene expression profiles of leaf and root tissue from Diospyros species adapted to ultramafic or serpentine and volcanic soils, grown in the common garden. Our goal was to identify fixed gene expression differences related to edaphic adaptation. Screening differentially expressed genes between edaphically contrasting species pairs using known serpentine and ultramafic adaptation genes from the literature, we found significant overlap only for the ultramafic-calcareous species pair. Interestingly, the known gene found to be differentially expressed in this species pair, a putative cyclin transmembrane metal transporter, is likely involved in metal ion homeostasis. However, no unique differentially expressed genes were identified in the serpentine-volcanic species pair, highlighting the polygenic nature of edaphic adaptation - a topic that is the subject of further investigation.

We assembled high-quality genomes for five selected species from the radiation plus an outgroup using long read PacBio data. The assemblies have been further characterised with structural and functional gene annotations, as well as repeat content analyses, focusing on TEs and tandem repeats. By comparing genome assemblies for species with contrasting edaphic adaptation (volcanic versus ultramafic), we identified patterns of gene-transposable element proximity, revealing highly lineage specific patterns of TE activity. Leveraging soil chemistry analysis performed on soil collected in New Caledonia, we discovered that TE insertions in Diospyros species growing in challenging ultramafic soil were associated with genes involved in DNA and RNA metabolism, providing a list of candidate genes for further investigation in Diospyros.

The results obtained over the course of StrucRadiation are currently being prepared for publication, with preprints to be shared on platforms such as bioRxiv prior to submission to open-access peer-reviewed journals. One publication dealing with the involvement of phenotypic plasticity in edaphic adaptation that used bioinformatic pipelines produced in StrucRadiation is available in bioRxiv and is currently undergoing peer-review in a journal. All associated data and metadata will be made publicly available via repositories such as the European Nucleotide Archive and FigShare. EU funding through StrucRadiation will continue to be acknowledged in all publications and dissemination activities.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Research into transposable elements (TEs) is a fast developing field, with much yet to be still uncovered regarding their role in host evolution. The recent advent of new technologies such as long-read sequencing has enabled ever greater insights into TE dynamics, offering a clearer understanding of how these genetic elements influence evolutionary processes. By combining a multi-omics strategy with detailed ecological metadata, StrucRadiation has significantly advanced our understanding of TE dynamics in the context of rapid host evolution. Our work has established a robust foundation for the continued study of TE proliferation and host adaptation in response to new ecological opportunities. The Diosypros system developed during StrucRadiation provides a valuable new model for studying these dynamics, offering insights that extend beyond those gained from more traditional model organisms. Our results contribute to a wider understanding of the balance between TE proliferation and host control, a topic of increasing relevance in evolutionary biology and beyond.
The findings of StrucRadiation are of great interest to the wider scientific community focused on TEs, genome evolution and adaptation. Ongoing preparations for publications, will complement further dissemination in international conferences and invited talks, where the results of StrucRadiation will be presented and discussed with the wider transposable element community. This dialogue will help refine the interpretation of our findings and contribute to shaping future research directions. Beyond the academic sphere, the outcomes of StrucRadiation hold great value through our collaborations with local plant nurseries in New Caledonia involved in conservation programmes. By sharing knowledge and resources with amateur botanists, non-profit conservation organisations and local communities, StrucRadiation is contributing to conservation efforts and fosters a deeper understanding of biodiversity and plant adaptation in the region.