Periodic Reporting for period 4 - EVO-MEIO (Adaptive evolution of meiosis in response to genome and habitat change)
Periodo di rendicontazione: 2020-09-01 al 2021-03-31
Genome duplication yields polyploid organisms, which have been important in evolution and agriculture. The doubling of the chromosome complement, and associated increases in cell size have a dramatic impact on the organism. Some of these can be beneficial, and indeed have been capitalized on both in agriculture and natural evolution, where polyploidy can provide new phenotypes, larger fruits, and broad stress resilience. Yet newly formed polyploids face substantial challenges, particularly to fertility, making it mysterious how they survive, and limiting the otherwise great potential of polyploidy in crop improvement. A major challenge to polyploids arises from chromosome mis-segregation in meiosis. This is because polyploids have double the number of homologous chromosome copies, and the meiotic system that evolved to segregate pairs of chromosomes in diploids is ill-equipped to deal with more. What the problem actually is, and how evolution can solve it, were the big mysteries we set out to explore in this project. We used the natural autopolyploid Arabidopsis arenosa and its close diploid relatives to explore what the problem actually is with chromosome segregation after genome duplication, and to understand how the evolved autotetraploid solved this issue. This involved novel immunocytological approaches and analyses, as well as complementary genetic and biochemical approaches. Building on previous work showing that a set of meiosis genes were under selection in autotetraploid A. arenosa, we set out to: (1) Couple genetics and immunocytology to test whether and how derived alleles of meiosis genes that we previously found as targets of selection in the polyploid lineage confer tetraploid meiotic stability, (2) ask whether meiotic genes are co-evolving as a polygenic target of selection, and (3) study the evolutionary dynamics of meiosis genes and assess whether the derived alleles arose from standing variation already present in diploids. We conclude from this action that meiosis in autopolyploid A. arenosa improved via the evolution of stronger crossover interference, that modified alleles of structural meiotic proteins contribute to this, and that most of the alleles under selection in tetraploids arose from novel mutations rather than standing variation already found in diploids. We also show that the autotetraploid adaptation pre-adapts meiosis to additional rounds of duplication. Our results provide novel insights to how fertility is regained after whole genome duplication, which in turn provided fundamental insights into key meiotic processes such as crossover interference, while also paving the way to widening the promise of polyploidy as a crop improvement tool.
During the five years of this project, we conducted a number of experiments that gave us novel insights into the evolution of polyploid meiosis, and helped establish Arabidopsis arenosa as an informative and useful model system for research in the immediate consequences of genome duplication, as well as the evolutionary response to these challenges. Moreover, this project opened important new research avenues in the biology of polyploids.
The main achievements of the project in its 60 months are:
1) One of the most important sets of experiments we performed was to establish in detail what specifically goes awry in neo-tetraploid meiosis immediately after genome duplication. Though there have been many cytological studies reported previously, it was not clear what the cause really was in any particular case. We used novel super-resolution microscopy and immunocytology, coupled with new kinds of analyses to unravel what exactly is the problem for neo-polyploids. We show that through evolving novel features to a process called crossover interference, which patterns crossovers in diploids, established polyploids can stabilize chromosome interactions and bias them towards interacting as pairs as they do in diploids, without affecting pairing preferences. Importantly, we show that this solution is effective also at higher ploidy. This work is important for helping contextualize the functional effects of genes we are studying. A manuscript describing this work is currently in minor revision for Current Biology, and should be published later in 2021 (Morgan, White et al., 2021).
2) Another important study showed that derived alleles of two meiotic proteins with evidence of selection in the tetraploid lineage do have important roles in stabilizing tetraploid meiosis (Morgan et al 2020, PNAS).
3) We also generated additional understanding of the population genetics of A. arenosa (Monnahan et al. 2019, Nature Ecology and Evolution), as well as a genetic map for Arabidopsis arenosa which will be published this year (2021).
4) Studying the evolutionary dynamics of the meiosis genes in A. arenosa we found that tetraploid derived alleles were largely selected from either de novo alleles or standing variants no longer present in diploids; some genes show evidence of having co-evolved (Bohutinska et al. 2021, Molecular Biology and Evolution).
5) A collaborative side project on crossover interference led to new insights and a new model for how this important process works (Morgan et al., 2021, Nature Communications).
6) We are currently generating protein biochemical data to test the idea that the derived alleles of meiotic proteins differ functionally from diploid alleles, and to understand how. This work is in progress and will result in one or two additional publications in 2022.
7) The main project generated, through a chance discovery, additional work on the plasticity of meiotic recombination to temperature and its effects on tetraploids (Lloyd et al 2018, Genetics; Weitz et al., 2021, Molecular Ecology).
8) The results from the project have triggered additional thinking and ideas for follow-up work. Some of these ideas were presented in related reviews (Bomblies, 2020, Proc Royal Soc B; Henderson and Bomblies 2021, Annu Rev Genet; Morgan et al 2017, Proc Royal Soc B).
The main project goals were achieved, with only minor deviations from the original proposal as results warranted.
The main achievements of the project in its 60 months are:
1) One of the most important sets of experiments we performed was to establish in detail what specifically goes awry in neo-tetraploid meiosis immediately after genome duplication. Though there have been many cytological studies reported previously, it was not clear what the cause really was in any particular case. We used novel super-resolution microscopy and immunocytology, coupled with new kinds of analyses to unravel what exactly is the problem for neo-polyploids. We show that through evolving novel features to a process called crossover interference, which patterns crossovers in diploids, established polyploids can stabilize chromosome interactions and bias them towards interacting as pairs as they do in diploids, without affecting pairing preferences. Importantly, we show that this solution is effective also at higher ploidy. This work is important for helping contextualize the functional effects of genes we are studying. A manuscript describing this work is currently in minor revision for Current Biology, and should be published later in 2021 (Morgan, White et al., 2021).
2) Another important study showed that derived alleles of two meiotic proteins with evidence of selection in the tetraploid lineage do have important roles in stabilizing tetraploid meiosis (Morgan et al 2020, PNAS).
3) We also generated additional understanding of the population genetics of A. arenosa (Monnahan et al. 2019, Nature Ecology and Evolution), as well as a genetic map for Arabidopsis arenosa which will be published this year (2021).
4) Studying the evolutionary dynamics of the meiosis genes in A. arenosa we found that tetraploid derived alleles were largely selected from either de novo alleles or standing variants no longer present in diploids; some genes show evidence of having co-evolved (Bohutinska et al. 2021, Molecular Biology and Evolution).
5) A collaborative side project on crossover interference led to new insights and a new model for how this important process works (Morgan et al., 2021, Nature Communications).
6) We are currently generating protein biochemical data to test the idea that the derived alleles of meiotic proteins differ functionally from diploid alleles, and to understand how. This work is in progress and will result in one or two additional publications in 2022.
7) The main project generated, through a chance discovery, additional work on the plasticity of meiotic recombination to temperature and its effects on tetraploids (Lloyd et al 2018, Genetics; Weitz et al., 2021, Molecular Ecology).
8) The results from the project have triggered additional thinking and ideas for follow-up work. Some of these ideas were presented in related reviews (Bomblies, 2020, Proc Royal Soc B; Henderson and Bomblies 2021, Annu Rev Genet; Morgan et al 2017, Proc Royal Soc B).
The main project goals were achieved, with only minor deviations from the original proposal as results warranted.
The action went beyond the state of the art in understanding of autopolyploid meiosis. We substantially extended our understanding of what the challenge to meiotic chromosome segregation upon genome doubling actually is, and how the evolved autotetraploid A. arenosa solves this problem phenomenologically. We extended this work to show that several genes under selection in the tetraploid lineage contribute to autopolyploid stability – the first time this was done for an autopolyploid. We show that the evolution of stronger crossover interference is a key factor, and an offshoot of this work led to a new model for how this important but mysterious process might work mechanistically. We have also found in side-projects that meiotic recombination in A. arenosa is sensitive to temperature and that this has particularly important implications for meiotic stability of tetraploids. This project has provided novel insights into tetraploid meiosis that aid in fundamental understanding of meiosis, as well potentially helping pave ways to facilitate the use of genome duplication as the promising crop improvement tool that it is (because of its ability to non-transgenically confer multi-stress resilience).