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Whole genome duplication – the gateway to adaptation?

Periodic Reporting for period 2 - DOUBLE ADAPT (Whole genome duplication – the gateway to adaptation?)

Periodo di rendicontazione: 2022-07-01 al 2023-12-31

Our research revolves around the intricate process of "whole genome duplication" in plants and its significance within the realm of evolutionary biology. Whole Genome Duplication (WGD), also known as polyploidy, is a fundamental genetic event that has played a significant role in the evolution of many organisms, particularly plants. It involves the duplication of an organism's entire set of chromosomes, resulting in multiple copies of the entire genome. This genetic phenomenon has profound implications for evolutionary biology, shaping the genetic diversity, adaptation, and speciation of species over geological timescales. However, we still know little about how WGD affects diversity of a genome, in particular selection and adaptation in natural populations of polyploid organisms. In our work, we've explored this phenomenon in depth by addressing the following principal aims (1) Does genome duplication promote accumulation of genetic variation? and (2) Is this variation used in adaptation?
In the first half of the project we proceeded in the following five major points
1) Investigating Novel Plant Systems: We focused on eight distinct plant species that vary in their ploidy levels. These species vary in their ploidy level and include close relatives of well-known plants like Arabidopsis, important crops like Medicago and Vaccinium, timber trees like Alnus, and some lesser-known wild species like Cardamine, Alyssum, Mimulus, and Saxifraga. Our research extends beyond merely documenting ploidy variations; it delves into understanding the ecological distributions, population dynamics, and phylogenetic relationships among cytotypes and populations within each species.
2) Unraveling the Genomic Consequences: Whole genome duplication has subtle but pervasive effects on genetic variation across entire genomes. This influence is observed in both single-nucleotide polymorphisms (SNPs) and structural variations in wild Arabidopsis species. We are extending this analysis to other species for which we have already collected genomic data to determine if these patterns hold true across the broad flowering plant diversity.
3) Adapting to Whole Genome Duplication: We have found that whole genome duplication can lead to the admixture of genes between different plant species, breaking down the barriers that typically keep them separate. This genetic exchange has played a crucial role in helping these plants adapt to the challenges posed by having extra copies of their genetic material, i.e. the WGD itself. This process of gene flow is a key driver of adaptation in our leading study species, Arabidopsis arenosa, and we are currently investigating the generality of the process in other plant species.
4) Adapting to Extreme Environments: We have conducted experiments on synthetic polyploid populations, when whole genome is experimentally doubled. These experiments have allowed us to explore how these plants evolve and adapt to extreme environments. Including both synthetic and closely related natural products of WGD (polyploids), we could separate the effect of genome duplication per se from later post-WGD evolution that happened in nature..
5) Theoretical Insights: We have developed theoretical models to understand how whole genome duplication influences the establishment and adaptive potential of plant populations. Interestingly, our findings challenge some of our initial expectations, revealing subtle effects of whole genome duplication on the evolutionary potential of plant populations.
Major Discovery: A notable breakthrough in our research has been the identification of widespread gene flow between cytotypes and even between different plant species facilitated by whole genome duplication. This genetic exchange serves as a critical source of variation, supporting the adaptation of polyploid lineages. This adaptation extends to the challenges posed by genome doubling itself and further environmental adaptations, such as those related to challenging soil conditions.
Unexpected Insights: Contrary to initial expectations, we have observed that whole genome duplication does not necessarily lead to a significant increase in adaptive variation across the entire genome. This is primarily due to the localized nature of adaptive introgression, where specific genetic variants are introduced into a population.
In summary, our research extends a comprehensive exploration into the impact of whole genome duplication on plant evolution. By delving into the intricacies of genomic dynamics and genetic exchange, we contribute to a deeper understanding of how plants adapt and thrive in response to these complex processes. Our work has broader implications for evolutionary biology and ecology, shedding light on the intricate mechanisms that drive genetic diversity and adaptation. By studying whole genome duplication across diverse plant systems, we gain insights into the general dynamics of genome evolution and how it influences the survival and adaptation of these plant populations in their natural environments.