Periodic Reporting for period 1 - TEEPI (How Transposable Elements drive the Emergence of Phenotypic Innovations)
Reporting period: 2021-05-01 to 2023-04-30
How the evolution of genomes leads to the current diversity of life remains a central question in Biology. Some of the most puzzling genomic innovations are triggered by transposons. Transposons are mobile genetic elements (DNA sequences) that can jump within a genome. They are characterized by DNA motif repeats at both ends of their sequence (interspersed repeats) and were considered for long only as parasitic DNA elements or ‘junk’ DNA. However, recent evidence have demonstrated their role in adaptive evolution through several mechanisms. Nevertheless, most of transposons have no or a negative impact on host organisms and are therefore counter-acted by several host pathways, such as DNA methylation and PIWI-interacting RNAs (piRNAs). piRNAs are small RNAs that bind to transposons and are part of a protein complex which cut down transposons, disabling their ability to jump within genomes and producing more piRNAs (feedback loop). The recent advances in technologies, both sequencing techniques (long-read sequencing) and computational resources (Machine Learning / Artificial Intelligence), allow now to precisely categorize transposons. TEEPI is set to take advantage of those new technologies to understand the role of transposons in the emergence of phenotypic innovations. TEEPI is also set to understand the evolutionary dynamics of transposons with host defense mechanisms and its impact on the emergence of novel and complex phenotypes. To that end, both transposons and piRNAs are studied simultaneously to precisely understand their interactions.
In order to unravel the role of transposons, along with their evolutionary dynamics with host piRNAs, in the emergence of novel phenotypes, TEEPI focus on the evolution of the insect order Blattodea, which encompasses cockroaches and termites. Those insects were chosen as model system, since they have repeatedly evolved complex phenotypes, such as eusociality in termites (a Major Evolutionary Transition and the highest level of sociality) and wood feeding. Furthermore, only few blattodean species have been sequenced so far (3 cockroach and 6 termite species) and demonstrates that a large part of their genome is made up of transposons. This enhances the potential of TEEPI to bring groundbreaking results and to rely mostly on genomes obtained with long-read sequencing technology, hence allowing a precise categorization of transposons and piRNAs. In addition, several cockroach and termite species are common pests and responsible for billion of euros of damages to human societies, which warrant the need of a better characterization of their resilience and biology at the molecular level to efficiently manage them without hindering other valuable insect species. More precisely, TEEPI focus on the categorization and mapping of transposons and piRNAs within blattodean genomes, to unravel their role during termite eusocial transition.
In order to unravel the role of transposons, along with their evolutionary dynamics with host piRNAs, in the emergence of novel phenotypes, TEEPI focus on the evolution of the insect order Blattodea, which encompasses cockroaches and termites. Those insects were chosen as model system, since they have repeatedly evolved complex phenotypes, such as eusociality in termites (a Major Evolutionary Transition and the highest level of sociality) and wood feeding. Furthermore, only few blattodean species have been sequenced so far (3 cockroach and 6 termite species) and demonstrates that a large part of their genome is made up of transposons. This enhances the potential of TEEPI to bring groundbreaking results and to rely mostly on genomes obtained with long-read sequencing technology, hence allowing a precise categorization of transposons and piRNAs. In addition, several cockroach and termite species are common pests and responsible for billion of euros of damages to human societies, which warrant the need of a better characterization of their resilience and biology at the molecular level to efficiently manage them without hindering other valuable insect species. More precisely, TEEPI focus on the categorization and mapping of transposons and piRNAs within blattodean genomes, to unravel their role during termite eusocial transition.
After careful literature screening, I chose and established a pipeline to detect and categorize transposons within cockroach and termite genomes. We then used those de novo transposon annotations to investigate the role of transposons in shifts of genes expression during the termite eusocial transition. This was motivated for two main reasons, the evolution of eusociality has been linked with enhanced potential of gene expression regulation and transposons are broadly known to impact gene expression when inserted near or within genes. Together with our collaborators in Paris, we then used these de novo transposons annotations along with available transcriptomes in different life-stages (limiting our study to 2 cockroach and 4 termite species). Termite eusociality is characterized by a division of reproductive labor based on different life-stages, with sterile worker caste being juveniles and the reproductive caste being adults. This characteristic of termites allows a direct comparison with non-eusocial cockroaches, since the juvenile and adult stages of cockroaches corresponds to the termite sterile worker and reproductive caste, respectively. We, therefore, compared the proportion of transposons inserted within genes showing an expression bias among the different life-stages and castes in cockroaches and termites, respectively. Those analyses brought the first evidence that transposons are associated with a change of gene expression among castes during termite eusocial transition. Indeed, transposon insertions within genes are linked with gene expression bias between the different castes in termites, but not in cockroaches. Furthermore, different transposon families were found to preferentially insert within genes specific to termite reproductives and sterile workers, while in cockroaches no pattern was found. Finally, our study showed that differentially expressed genes in termite castes with high rates of transposon insertions are associated with functions specific to the phenotype of each caste. Indeed, transposon-rich queen genes were involved in reproduction and ageing (termite queens are known to live up tro 40 years while worker a couple of weeks), while transposon-rich worker genes were involved in behavior and cognition (important for nursing and foraging tasks, as well as communication within the nest). This first canonical study of TEEPI was published in Genes on October 2022 (doi: https://doi.org/10.3390/genes13111948(opens in new window)).
TEEPI project, despite delays in obtaining new genomes and transcriptomes, already unraveled the role of transposons during the adaptation to eusociality in termites, by enabling shifts of gene expression leading to new and divergent phenotypes among worker and reproductive castes. It also highlighted the different role of transposon families in this process. After obtaining and categorizing piRNAs in four cockroach genomes, TEEPI will be able to categorize the evolutionary dynamics of transposons with host defense mechanism (piRNAs) during the adaptation to wood feeding and increased social complexity in cockroaches and termites. Furthermore, along the upcoming availability of new Blattodea genomes and transcriptomes, TEEPI will allow to unravel by which mechanisms transposons can favor blattodean adaptive radiations. Those knowledge will further our global understanding of genome evolution and how it leads to life diversity and increased organismal complexity. The precise categorization of transposons and piRNAs in cockroach and termite genomes, planned with the end of TEEPI, will lead to further understand on how host-transposon interactions can favor the evolutionary benefits of transposon on genome diversity and phenotypic innovations, while mitigating their deleterious effects, not only in blattodea but likely in many other organisms. Furthermore, the focus of TEEPI on cockroaches and termites may, in the future, allow to develop strategies and products mitigating the threats and costs of those species on human societies, as TEEPI will bring a better understanding of the molecular processes underlying the success of those pest species. Finally, understanding the evolutionary dynamics of transposons with piRNAs will allow to understand further how host defense mechanisms target transposons, which may reveal useful to understand and develop technologies, in the long run, to temper the impact of transposons in diseases.