Abstract
During infection, both phytopathogenic and endophytic fungi form intimate contact with living plant cells, and need to resist or disable host defences and modify host metabolism to adapt to their host. Fungi can achieve these changes by secreting proteins and enzymes. A comprehensive comparison of the secretomes of both endophytic and pathogenic fungi can improve our understanding of the interactions between plants and fungi. Although Magnaporthe oryzae, Gaeumannomyces graminis, and M. poae are economically important fungal pathogens, and the related species Harpophora oryzae is an endophyte, they evolved from a common pathogenic ancestor. We used a pipeline analysis to predict the H. oryzae, M. oryzae, G. graminis, and M. poae secretomes and identified 1142, 1370, 1001, and 974 proteins, respectively. Orthologue gene analyses demonstrated that the M. oryzae secretome evolved more rapidly than those of the other three related species, resulting in many species-specific secreted protein-encoding genes, such as avirulence genes. Functional analyses highlighted the abundance of proteins involved in the breakdown of host plant cell walls and oxidation-reduction processes. We identified three novel motifs in the H. and M. oryzae secretomes, which may play key roles in the interaction between rice and H. oryzae. Furthermore, we found that expression of the H. oryzae secretome involved in plant cell wall degradation was downregulated, but the M. oryzae secretome was upregulated with many more upregulated genes involved in oxidation-reduction processes. The divergent in planta expression patterns of the H. and M. oryzae secretomes reveal differences that are associated with mutualistic and pathogenic interactions, respectively.
Highlights
Fungi play essential roles in diverse environments, including the establishment of various relationships with host plants with interactions that range from mutualistic to pathogenic [1, 2]
Clavicipitaceous endophytes arose from insect-parasitic ancestors [15], whereas the beneficial endophyte Harpophora oryzae originated from a phytopathogenic ancestor [16]
Contain transmembrane (TM) domain or glycosylphosphatidylinositol (GPI)-anchored proteins were removed. This resulted in predicted secretomes of 1142, 1370, 1001, and 974 proteins for H. oryzae, M. oryzae, G. graminis, and M. poae, respectively (7.8, 10.6, 6.9, and 8.0% of total genomes, respectively) (Fig 1; S1 Table)
Summary
Fungi play essential roles in diverse environments, including the establishment of various relationships with host plants with interactions that range from mutualistic to pathogenic [1, 2]. Fungi can secrete proteins called effectors to manipulate the immunity and physiology of their hosts to prevent host detection, suppress plant defences, and/or induce plant cell death [3,4,5]. Communication between fungi and host plants is achieved by secretion of proteins and enzymes that are either delivered into the plant cells or detected at the plant cell surface [1, 12]. This communication occurs, in particular, at the initial stage of infection [13]. A comprehensive comparison of the secretomes of closely related endophytic and pathogenic fungi sharing a common ancestor will further our understanding of the interactions between fungi and host plants
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