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Mechanisms of symbiotic incompatibility in the arbuscular mycorrhizal association

Periodic Reporting for period 1 - SYMBIO-INC (Mechanisms of symbiotic incompatibility in the arbuscular mycorrhizal association)

Reporting period: 2020-09-01 to 2022-08-31

This project addressed poorly understood mechanisms underlying the differences between mycorrhizal and non-mycorrhizal plants. Mycorrhizal symbiosis is an important factor mediating plant growth and tolerance to stress, and plays therefore a crucial role in plant production systems. Understanding these mechanisms is central to improving mycorrhizal symbioses for practical applications. Although initial aims were focused at molecular mechanisms, due to COVID-19-related restrictions, the project re-directed focus towards ecological and evolutionary mechanisms, and adopted a data mining strategy combined with modeling to unravel ecological and evolutionary differences between mycorrhizal and non-mycorrhizal plants.
First, natural variation of the non-mycorrhizal plant Arabidopsis thaliana in its ability to associated with arbuscular mycorrhizal (AM) fungi was tested. This involved pre-growth of mycorrhizal networks to boost AM association with roots of 80 A. thaliana accessions varying in adaptive ecological strategies. The outcome was unfortunately inconclusive leading to aim revision.
Second, data was assembled using multiple published datasets with information on different symbiotic types (including non-mycorrhizal), adaptive ecological strategies, and phylogeny of plants, resulting in three new datasets: (D1) 1,638 plant species assigned with time-calibrated phylogeny, different mycorrhizal strategies, and drought adaptation; (D2) 3,014 plant species assigned to different symbiotic types and a continuous CSR strategy variable; and (D3) 2,795 plant species assigned with time-calibrated phylogeny, different symbiotic types, and generalist or specialist adaptive strategy.
Third, I have reconstructed the co-evolution of plant mycorrhizal strategy and drought adaptation, by inputting D1 into phylogenetic comparative models of increasing complexity allowing for heterogeneity in evolution and for unobserved factors to influence the observed trait evolution. Detected correlated evolution unveiled gains and losses of drought tolerance occurring at faster rates in lineages with ecto- or ericoid mycorrhizal strategy, compared with that of the AM or naked root. This study unveiled also that AM plants sensitive to drought are more likely to lose their mycorrhizal symbiosis. These results, which help to shape our fundamental understanding of the underlying mechanisms governing plants adaption to drought, were published as a preprint and are currently in peer-review.
Fourth, a global characterization of ecological links among plant symbiotic types and adaptive ecological strategies was performed, using D2 combined with Dirichlet regression. This characterization contributes to improve our understanding of how different symbiotic types inter-links with CSR strategies. In particular, it revealed that non-mycorrhizal plants have the global highest ruderal strategy of all symbiotic types tested. These results will be combined with those of D3 (described below) into one manuscript under preparation.
Fifth, in collaboration with Dr. Boyko, we have reconstructed the co-evolution of plant symbiotic types and adaptive ecological strategies at the global scale, using D3. To this end, we developed customized phylogenetic comparative models allowing for character-state dependent evolution heterogeneity. We identified, from 256 possible transitions, that 49 have likely occurred in 325My-history of land plants. Depending on symbiotic association, transitions could range from nearly instantaneous to rarely occurring. The ericoid mycorrhizal, non-mycorrhizal, AM, and facultatively AM type associated with the fastest changes in adaptive strategies. Among conclusions, the study suggests that similar patterns can be observed between non-mycorrhizal and mycorrhizal plants when looking at broad-ranging ecological parameters. A manuscript on this is currently under preparation.
No website has been developed for the project.
The project helps to improve our understanding of how mycorrhizal and non-mycorrhizal states help to shape the evolution of plants on Earth, unraveling mechanisms underlying differences between these groups. The project compiled large and diverse datasets of plant species to model the evolution of drought adaptation and ecological adaptive strategies over the past 325My, while assessing the role of different symbiotic types in these important processes. This will help to narrow down uncertainties in the prediction of temporal dynamics of vegetation ecosystems particularly important under the context of Climate Change. The project offers therefore a contribution to answer pressing questions and contributes to the broader fundamental knowledge on host-microbe associations by quantitatively demonstrating different long-term evolutionary advantages of plant-microbe symbioses. Such advantages have been often appreciated qualitatively for a myriad of organisms, but are only seldomly quantitatively evaluated. The results are thus of interest to a broad audience of scientists as well as to policy makers, advancing our capacity towards the prediction and management of plant and soil communities essential to achieve the European policy objectives on Sustainable Development. Two manuscripts are planned for open access publication, one published as preprint currently under revision in the Nature portfolio journal Communications Biology (open access), and another under preparation to be submitted to an open access high-impact journal.
The project also served as a basis to develop and implement teaching content for university students, inspiring scientific aspirations and disseminating scientific values. This teaching content received the Sustainability Certificate by HU-Berlin due to its relevance in Education for Sustainable Development.
Evolution model of drought adaptation and mycorrhizal strategy in land plants