Abstract
Sooty blotch and flyspeck (SBFS) fungi are unconventional plant pathogens that cause economic losses by blemishing the surface appearance of infected fruit. Here, we introduce the 18.14-Mb genome of Peltaster fructicola, one of the most prevalent SBFS species on apple. This undersized assembly contains only 8,334 predicted protein-coding genes and a very small repertoire of repetitive elements. Phylogenomics and comparative genomics revealed that P. fructicola had undergone a reductive evolution, during which the numbers of orphan genes and genes involved in plant cell wall degradation, secondary metabolism, and secreted peptidases and effectors were drastically reduced. In contrast, the genes controlling 1,8-dihydroxynaphthalene (DHN)-melanin biosynthesis and appressorium-mediated penetration were retained substantially. Additionally, microscopic examination of the surfaces of infected apple indicated for the first time that P. fructicola can not only dissolve epicuticular waxes but also partially penetrate the cuticle proper. Our findings indicate that genome contraction, characterized mainly by the massive loss of pathogenicity-related genes, has played an important role in the evolution of P. fructicola (and by implication other SBFS species) from a plant-penetrating ancestor to a non-invasive ectophyte, displaying a novel form of trophic interaction between plants and fungi.
Highlights
Genetic and biochemical nature of the adaptations that enable survival in this unique niche has not been elucidated, high-throughput sequencing and genome analysis have yielded deep insights into a wide range of traits in many other fungal pathogens and symbionts[17,18,19]
Two main questions were addressed in this work: 1) what genomic features underpin the adaptation of SBFS pathogens to their epicuticular niche? 2) Under the hypothesis that SBFS fungi arose from invasive plant parasites[20], what evolutionary mechanisms led to development of a so-called “epiphyte”?
The Core Eukaryotic Genes (CEGs) Mapping Approach assessed the completeness of the P. fructicola genome to be 97.2% (241 out of 248 CEGs)
Summary
Presence of the same number of cutinase-coding genes in these two fungi suggests that P. fructicola may retain the ability to degrade cuticles, especially considering that two of them were expressed at a moderate level in vivo and have secretion signals (Fig. 3a; Supplementary Table S5). In P. fructicola, we found only 15 SM biosynthesis enzyme-coding genes that belong to four classes: polyketide synthase (PKS), non-ribosomal peptide synthetase (NRPS), polyketide synthase/non-ribosomal peptide synthetase hybrid (PKS-NRPS), and terpene cyclase (TC) (Supplementary Table S7) This number is far smaller than those of non-biotrophic plant pathogenic fungi and even slightly smaller than that of the biotrophic pathogen U. maydis (Fig. 2), in which SM genes should be diminished, probably because their existence compromises host survival[40]. Driving forces for the evolution from classical plant parasitism to external plant parasitism are unclear, but this change may have facilitated escape from host specialization and thereby enhanced survival during periods of rapid environmental and ecological change
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