Transposable Elements in the Genome of the Lichen-Forming Fungus Umbilicaria pustulata and Their Distribution in Different Climate Zones along Elevation

SIMPLE SUMMARY: Accumulating evidence suggests that transposable elements—DNA sequences that can ‘jump’ from one location to another in the genome—may not be randomly distributed in the genome. They might in fact be an important source of adaptive evolution through genome diversification. In this study we present the first in-depth investigation of transposable element content in a lichen-forming fungus. The species we chose is Umbilicaria pustulata—an ascomycete that forms symbiotic associations with green algae of the genus Trebouxia and is able to inhabit a broad latitudinal and elevational range throughout the European continent. Additionally, we studied the distribution of transposable elements in several populations of the fungus across three mountains in the Mediterranean region. We found several transposable element insertions that display a climate-specific distribution along the elevational gradients. Our study contributes to expanding our understanding of transposable element content and evolution in fungal obligate biotrophs. Particularly, it may serve as a foundation for assessing the impact of transposon dynamics on fungal adaptation to the abiotic environment and the impact of transposon activity on the evolution and maintenance of a symbiotic lifestyle. ABSTRACT: Transposable elements (TEs) are an important source of genome plasticity across the tree of life. Drift and natural selection are important forces shaping TE distribution and accumulation. Fungi, with their multifaceted phenotypic diversity and relatively small genome size, are ideal models to study the role of TEs in genome evolution and their impact on the host’s ecological and life history traits. Here we present an account of all TEs found in a high-quality reference genome of the lichen-forming fungus Umbilicaria pustulata, a macrolichen species comprising two climatic ecotypes: Mediterranean and cold temperate. We trace the occurrence of the newly identified TEs in populations along three elevation gradients using a Pool-Seq approach to identify TE insertions of potential adaptive significance. We found that TEs cover 21.26% of the 32.9 Mbp genome, with LTR Gypsy and Copia clades being the most common TEs. We identified 28 insertions displaying consistent insertion frequency differences between the two host ecotypes across the elevation gradients. Most of the highly differentiated insertions were located near genes, indicating a putative function. This pioneering study of the content and climate niche-specific distribution of TEs in a lichen-forming fungus contributes to understanding the roles of TEs in fungal evolution.