Abstract
BACKGROUND: Yeasts are ubiquitous microorganisms thriving in diverse environments. They are prevalent members of the phyllosphere microbiome, but genomic studies of plant-associated yeasts remain limited. RESULTS: We established a taxonomically diverse yeast culture collection from flag leaves of field-grown wheat. This collection captured between 48-56% of the genus-level diversity detected by ITS amplicon sequencing conducted over two consecutive years, including the core members Aureobasidium, Dioszegia, Filobasidium, Papiliotrema, Sporobolomyces, and Vishniacozyma. De novo sequencing of 96 high-quality genomes from this collection, representing 14 yeast genera, and comparative genomics revealed specific signatures associated with life in the phyllosphere, the aboveground part of the plant. These adaptive traits encompass enriched carbohydrate metabolism, secondary metabolite biosynthetic pathways, and pectin degradation. The substantially smaller genomes of the phyllosphere yeast genera Candida and Metschnikowia suggest niche specialization via prioritizing metabolic pathways that are essential for survival in the nutrient-limited phyllosphere. CONCLUSIONS: This study represents a significant advancement in our understanding of the diverse and largely unknown genomic traits of environmental yeasts and their adaptation to life in the phyllosphere environment. Our findings highlight their untapped functional potential for biotechnological applications in sustainable crop production.