Periodic Reporting for period 2 - DOUBLE-TROUBLE (Replaying the ‘genome duplication’ tape of life: the importance of polyploidy for adaptation in a changing environment)
Período documentado: 2021-07-01 hasta 2022-12-31
Polyploidy, i.e. the possession of multiple sets of chromosomes as a consequence of whole-genome duplication (WGD), has been known for a long time, especially in plants. Although polyploidy is rarer in animals, there are also numerous cases of polyploid insects, fishes, amphibians, and reptiles. For a long time, ancient polyploidy, dating back millions of years, was much less well documented and it was not until the advent of genomics and whole genome sequencing that it became clear that the significance of polyploidy extends across all eukaryotes, and even prokaryotes, from ancient history to the recent past. Most, if not all, extant species (including our own) carry the signature of at least one ancient WGD. Because of their often-enhanced phenotypic appearance, polyploidy has also been a key force in the origin and success of most crops. Artificial polyploidization of crops can increase yield, consumer satisfaction, and specific nutrients, thereby improving food security, a critical goal given the Earth’s expanding population and limited arable land. In addition to occurring in whole organisms, programmed or unprogrammed events can increase the ploidy of specific somatic cells and cell lineages. In humans, for instance, polyploid cells keep the human heart beating, and are essential for repair of the most regenerative organ in the human body; the liver. Polyploid cells are important in the development of structures including trichomes, fruits, and root nodules. Acute, induced polyploidy in individual cells or tissues can also occur in response to tissue stress and in disease. Finally, unprogrammed ploidy increases are now known to be among the most common events in human tumor growth. In conclusion, polyploidy is a driving force in organismal and sub-organismal evolution and elucidating the consequences of WGD at multiple levels is key to understanding global patterns of biodiversity and ecology, as well as cellular fates, physiology, and metabolism. Although the implications of polyploidy range from cells to ecosystems and from agriculture to human health, polyploidy remains understudied in many contexts, and its roles and impact in biological processes and across phylogeny are unclear.
One recurring theme is the link between polyploidy and stress. It is known that stress can trigger polyploidy, but there are also strong indications that polyploidy confers a selective advantage under stressful conditions, such as during environmental turmoil. In this research project, we want to build on our current expertise in polyploidy and WGD by unraveling the mechanistic complexities underlying polyploidy under stressful conditions. To this end, we want to use a holistic interdisciplinary approach integrating genomics, experimental evolution, modeling, and Artificial Intelligence (AI).
One recurring theme is the link between polyploidy and stress. It is known that stress can trigger polyploidy, but there are also strong indications that polyploidy confers a selective advantage under stressful conditions, such as during environmental turmoil. In this research project, we want to build on our current expertise in polyploidy and WGD by unraveling the mechanistic complexities underlying polyploidy under stressful conditions. To this end, we want to use a holistic interdisciplinary approach integrating genomics, experimental evolution, modeling, and Artificial Intelligence (AI).
So far, we have created polyploid Chlamydomonas and Spirodela strains and have set up four long term evolutionary experiments including the longest mutation accumulation experiment in duckweeds and flowering plants ever. We have also provided the first evidence for Spirodela polyrhiza that the immediate effect of WGD can confer a fitness benefit under stressful conditions, but that this depends on the combination of the exact environment and the genotype of the species. We also developed a spatially explicit macro eco-evolutionary model of mixed-ploidy populations, which is neutral and simulates stable environments, and still shows possible polyploid establishment. Furthermore, this model explains why polyploids seem to experience higher extinction rates than diploids. In addition, the model considers expected metabolic and body size changes upon polyploidization and shows there is a clear range of parameters where polyploids are able to stably coexist with diploids and even can invade diploid populations, although polyploidy is expected to lower the metabolic efficiency.
Although challenging, we have now been able to successfully set up long-term evolution experiments with stable lines of haploid/diploid Chlamydomonas (a unicellular alga) and with stable lines of diploid/tetraploid Spirodela polyrhiza (greater duckweed, an angiosperm). In a next phase of the project, these will be used for 'replaying the (duplication) tape of life', at scales and under conditions that have not been possible before, except maybe in yeast (which are only very distantly related to plants and therefore knowledge gained is limited), which is quite unique. At the same time, we have developed our first beyond the state-of-the-art eco-evolutionary models for polyploid establishment, which are neutral and do not even need selection to explain when and how polyploid populations can survive and get established. We have also build our first models of duplicated gene regulatory networks and are currently running simulations to study how signals (e.g. cues from the environment) propagate over simple and duplicated networks, and how duplicated gene regulatory networks can possibly explain 'big' jumps in evolution.