The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte

Abstract

The fungus Harpophora oryzae is a close relative of the pathogen Magnaporthe oryzae and a beneficial endosymbiont of wild rice. Here, we show that H. oryzae evolved from a pathogenic ancestor. The overall genomic structures of H. and M. oryzae were found to be similar. However, during interactions with rice, the expression of 11.7% of all genes showed opposing trends in the two fungi, suggesting differences in gene regulation. Moreover, infection patterns, triggering of host defense responses, signal transduction and nutritional preferences exhibited remarkable differentiation between the two fungi. In addition, the H. oryzae genome was found to contain thousands of loci of transposon-like elements, which led to the disruption of 929 genes. Our results indicate that the gain or loss of orphan genes, DNA duplications, gene family expansions and the frequent translocation of transposon-like elements have been important factors in the evolution of this endosymbiont from a pathogenic ancestor.

Reactive oxygen species metabolism and plant-fungal interactions

“…For example, future gains in understanding plant-microbe interactions might come from molecular comparisons of plant pathogens versus endophytes with regards to redox balance. For example, functional comparisons of the endophyte, Harpophora oryzae (Xu et al, 2014;Yuan et al, 2010), with its pathogenic relative, M. oryzae, might unpack differences in how Molina and Kahmann (2007) metabolism, nutrient signaling, growth, and antioxidation are connected in two fungi with opposing lifestyles. The importance and interconnectivity of host and pathogen ROS metabolism is becoming evident, but molecular understanding of the underlying mechanisms are still lacking.…”

Computational Identification and Comparative Analysis of Secreted and Transmembrane Proteins in Six Burkholderia Species

“…This indicated that the functional features of the secreted proteins in the Burkholderia species are most likely species-specific rather than lifestyle-specific, and thus would lead to distinct characteristics in their communication process with the host cells. Another study also demonstrated that although virulent microorganisms and endophytes seem to possess genetically similar weaponry, their expression and regulatory mechanisms are different (Lòpez-Fernàndez et al, 2015; Xu et al, 2014). Further studies of the expressions of specific proteins in each species and their interactions during communication with host cells might explain the differences between these pathogenic and mutualistic bacteria (Lòpez-Fernàndez et al, 2015; Seo et al, 2015).…”

Host-dependent fungus-fungus competition suppresses fungal pathogenesis inArabidopsis thaliana

“…Beneficial bacteria and fungi also indirectly protect hosts by increasing local and/or systemic pathogen resistance (Van Wees et al ., 2008; Pieterse et al ., 2014; de Lamo & Takken, 2020). The endophytic ascomycete fungus Harpophora oryzae confers local and systemic rice resistance to rice blast fungi ( Magnaporthe oryzae ) (Xu et al ., 2014). The basidiomycete Serendipita indica (formerly known as Piriformospora indica ) induces systemic resistance in Arabidopsis thaliana against biotrophic powdery mildew, through the phytohormone jasmonic acid (JA) (Stein et al ., 2008).…”

“…High relatedness between beneficial and pathogenic species seems to be widespread, rather than exceptional, in plant-inhabiting fungi (Rodriguez et al ., 2009). Pathogenic species/strains are often found, without displaying virulence, in microbial communities on apparently healthy plants (García et al ., 2012; Xu et al ., 2014). In Arabidopsis thaliana , root-inhabiting bacteria may contribute to asymptomatic accommodation of filamentous microbial eukaryotes, by antagonizing their negative impacts on the host (Duran et al ., 2018).…”