Abstract

BackgroundEctophytic fungi occupy the waxy plant surface, an extreme environment characterized by prolonged desiccation, nutrient limitation, and exposure to solar radiation. The nature of mechanisms that facilitate adaptation to this environment remains unclear. In this study, we sequenced the complete genome of an ectophytic fungus, Ramichloridium luteum, which colonizes the surface of apple fruit, and carried out comparative genomic and transcriptome analysis.ResultsThe R. luteum genome was 28.18 Mb and encoded 9466 genes containing 1.85% repetitive elements. Compared with cell-penetrating pathogens, genes encoding plant cell wall degrading enzymes (PCWDEs), PTH11-like G protein-coupled receptors (GPCRs) and effectors were drastically reduced. In contrast, genes encoding cutinases and secretory lipases were strikingly expanded, and four of nine secretory lipases were probably acquired by horizontal gene transfer from Basidiomycota. Transcriptomic analysis revealed elevated expression of genes involved in cuticle degradation (cutinase, secretory lipase) and stress responses (melanin biosynthesis, aquaporins, lysozymes and HOG pathway).ConclusionsTaken together, our results highlight genomic features associated with evolution of surface niche adaptation by the ectophytic fungus R. luteum, namely the contraction of PCWDEs, PTH11-like GPCRs and effectors, and the expansion of cuticle degradation and stress tolerance.

Highlights

  • Ectophytic fungi occupy the waxy plant surface, an extreme environment characterized by prolonged desiccation, nutrient limitation, and exposure to solar radiation

  • Sooty blotch and flyspeck (SBFS) fungi, which descended from invasive plant pathogens, colonize epicuticular layers of plants as ectophytes [6]

  • R. luteum genome size was considerably smaller than the average genome size of Ascomycota (36.91 Mb) [19], but over 55% larger than the sooty blotch and flyspeck (SBFS) fungus P. fructicola [6]

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Summary

Introduction

Ectophytic fungi occupy the waxy plant surface, an extreme environment characterized by prolonged desiccation, nutrient limitation, and exposure to solar radiation. On the other hand, colonize primarily the surface niche. Sooty blotch and flyspeck (SBFS) fungi, which descended from invasive plant pathogens, colonize epicuticular layers of plants as ectophytes [6]. They can extract required nutrients from living hosts without killing cells and tissues. During the evolutionary transition from invasive plant pathogenesis to an ectophytic niche [6, 7], most pathogenicity-related genes except some associated with cuticle penetration were lost in SBFS fungus Peltaster fructicola [6].

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