Asymmetric inter-kingdom gene transfer and a horizontal transposon invasion in a powdery mildew fungus

Abstract

Horizontal DNA transfer can introduce new genetic material into eukaryotic genomes, but how often recent transfers occur between multicellular lineages and what happens to transferred DNA after integration remain poorly understood. Plants and fungi provide a powerful system to address these questions because of their long-standing and intimate ecological associations. Here, we performed an annotation-independent, bidirectional whole-genome screen across 418 plant and 1,081 fungal genomes and identified 22 high-confidence recent horizontal transfer events. Twenty-one involved fungal DNA acquired by plants and were concentrated in bryophytes and Pooideae grasses, revealing pronounced directional and phylogenetic biases. The evolutionary fate of transferred DNA differed across recipient lineages. In Pooideae, fungal-derived genes underwent duplication, structural remodeling and expression divergence, and showed copy-number variation within species. In Marchantia polymorpha, transferred genes remained mostly single-copy but displayed presence-absence variation and ongoing loss among subspecies and natural accessions. In the opposite direction, we identified a plant-derived DNA transposon integrated into the genome of the tomato powdery mildew fungus Pseudoidium neolycopersici. Following transfer, this element remained active and generated a derived family of miniature inverted-repeat transposable elements that expanded to 172 copies. Recent detectable DNA transfer between plants and fungi is therefore uncommon and strongly asymmetric, but transferred sequences can remain highly dynamic after integration. Their subsequent loss, duplication, structural and regulatory diversification, or transposon-driven amplification links rare cross-kingdom acquisition events to ongoing genome variation and diversification.