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The evolution of the allorecognition gene repertoire in the Podospora anserina species complex
(Johannesson's Lab)
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för organismbiologi, Systematisk biologi. (Johannesson's Lab)
Uppsala universitet, Science for Life Laboratory, SciLifeLab. Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi. Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för immunologi, genetik och patologi, Medicinsk genetik och genomik.ORCID-id: 0000-0003-1037-7904
(Ecologie Systematique Evolution, Batiment 360, AgroParisTech, CNRS, Universite Paris‐Saclay, Orsay, France)ORCID-id: 0000-0002-9365-4008
Vise andre og tillknytning
(engelsk)Manuskript (preprint) (Annet vitenskapelig)
Abstract [en]

Across the Tree of Life, self/non-self recognition is typically achieved through highly polymorphic loci under balancing selection. In fungi, vegetative conspecific recognition, or allorecognition, is defined by the compatibility interactions between loci known as het genes. In this study we explore the evolution of the het genes in the model fungus Podospora anserina and its closest relatives (the Podospora anserina species complex). First, we used chromosome-level genome assemblies to resolve their phylogenetic relationships. We found that the species in the complex are well defined but diversified recently and rapidly, leading to high degrees of conflict at deep branches of the phylogeny. Unlike typical orthologous genes from the complex, some allorecognition genes (het-z and het-s) show trans-species polymorphism, a hallmark of long-term balancing selection. By contrast, the het genes belonging to the HNWD family exhibit a high turn-over, with losses and duplications happening often. In particular, the species P. pseudocomata has a considerable increase of HNWD genes. Unexpectedly, we show that the HNWD paralogs have clean defined boundaries flanked by a target site duplication (TSD), implicating a DNA transposon-like mechanism in the genesis of new duplicates. Overall, our data highlights the diversity of evolutionary histories behind individual self/non-self recognition genes at short evolutionary timescales.

Emneord [en]
Podospora, Allorecognition, heterokaryon incompatibility, vegetative incompatibility, balancing selection, Transposable elements, NLRs
HSV kategori
Forskningsprogram
Biologi med inriktning mot evolutionär genetik
Identifikatorer
URN: urn:nbn:se:uu:diva-406881OAI: oai:DiVA.org:uu-406881DiVA, id: diva2:1417403
Tilgjengelig fra: 2020-03-27 Laget: 2020-03-27 Sist oppdatert: 2020-03-28
Inngår i avhandling
1. Drivers of evolutionary change in Podospora anserina
Åpne denne publikasjonen i ny fane eller vindu >>Drivers of evolutionary change in Podospora anserina
2020 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
Abstract [en]

Genomic diversity is shaped by a myriad of forces acting in different directions. Some genes work in concert with the interests of the organism, often shaped by natural selection, while others follow their own interests. The latter genes are considered “selfish”, behaving either neutrally to the host, or causing it harm. In this thesis, I focused on genes that have substantial fitness effects on the fungus Podospora anserina and relatives, but whose effects are very contrasting. In Papers I and II, I explored the evolution of a particular type of selfish genetic elements that cause meiotic drive. Meiotic drivers manipulate the outcome of meiosis to achieve overrepresentation in the progeny, thus increasing their likelihood of invading and propagating in a population. In P. anserina there are multiple meiotic drivers but their genetic basis was previously unknown. In Paper I, we demonstrated that drive is caused by members of the Spok gene family. We discovered two new Spok genes, Spok3 and Spok4, which locate in different chromosomes in different strains. In Paper II, we showed that Spok3 and Spok4 are found on a gigantic (up to 247 Kb long) variant of Enterprise, a Crypton-like transposable element. Enterprise likely mobilize through the action of a putative tyrosine-recombinase that we call Kirc. When carrying the Spoks, this element has double selfish properties: transposition and meiotic drive. In addition, we found that homologs of the Spoks (Paper I) and of Kirc (Paper II) are widespread in fungi but their phylogenies are discordant with that of the species, suggesting that they have undergone horizontal gene transfer. In Papers III and IV, I turned the focus into genes that have an adaptive function. In fungi, the het genes control conspecific self/non-self recognition. Such genes are expected to evolve under frequency-dependent balancing selection. In Paper III, we found evidence of balancing selection acting on some het genes across the P. anserina species complex. Unexpectedly, we also discovered that het genes of the HNWD gene family are duplicated in a transposon-like manner, broadening our understanding of their potential fitness effects. Finally, in Paper IV we show how het genes with pleiotropic effects on sexual recognition lead to the evolution of strong reproductive isolation, and hence speciation. Overall, the results of my thesis highlight the functional intersection between mobile selfish genetic elements and other genes, either selfish or adaptive, and their effects on genome architecture and population structure.

sted, utgiver, år, opplag, sider
Uppsala: Acta Universitatis Upsaliensis, 2020. s. 63
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1923
Emneord
Podospora, Meiotic drive, Spore killing, vegetative incompatibility, heterokaryon incompatibility, allorecognition, speciation, Transposable elements, selfish genetic elements, fungi
HSV kategori
Forskningsprogram
Biologi med inriktning mot evolutionär genetik
Identifikatorer
urn:nbn:se:uu:diva-407766 (URN)978-91-513-0921-7 (ISBN)
Disputas
2020-05-19, Ekmansalen, Evolutionary Biology Centre (EBC), Norbyvägen 18D, Uppsala, 10:00 (engelsk)
Opponent
Veileder
Tilgjengelig fra: 2020-04-29 Laget: 2020-03-28 Sist oppdatert: 2020-04-29

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