Positively selected effector genes and their contribution to virulence in the smut fungusSporisorium reilianum

Abstract

47Plants and fungi display a broad range of interactions in natural and agricultural ecosystems 48 ranging from symbiosis to parasitism. These ecological interactions result in coevolution 49 between genes belonging to different partners. A well-understood example are secreted fungal 50 effector proteins and their host targets, which play an important role in pathogenic 51 interactions. Biotrophic smut fungi (Basidiomycota) are well-suited to investigate the 52 evolution of plant pathogens, because several reference genomes and genetic tools are 53 available for these species. Here, we used the genomes of Sporisorium reilianum f. sp. zeae 54 and S. reilianum f. sp. reilianum, two closely related formae speciales infecting maize and 55 sorghum, respectively, together with the genomes of Ustilago hordei, Ustilago maydis and 56Sporisorium scitamineum to identify and characterize genes displaying signatures of positive 57 selection. We identified 154 gene families having undergone positive selection during species 58 divergence in at least one lineage, among which 77% were identified in the two investigated 59 formae speciales of S. reilianum. Remarkably, only 29% of positively selected genes encode 60 predicted secreted proteins. We assessed the contribution to virulence of nine of these 61 candidate effector genes in S. reilianum f. sp. zeae by deleting individual genes, including a 62 homologue of the effector gene pit2 previously characterized in U. maydis. Only the pit2 63 deletion mutant was found to be strongly reduced in virulence. Additional experiments are 64 required to understand the molecular mechanisms underlying the selection forces acting on 65 the other candidate effector genes, as well as the large fraction of positively selected genes 66 encoding predicted cytoplasmic proteins. 67 68

The genomic determinants of adaptive evolution in a fungal pathogen

“…; Schweizer et al. ). While these studies advanced our understanding of the molecular basis of host‐pathogen coevolution, the amount of candidate genes under positive selection is only an indirect indicator of the rate of adaptive evolution in these organisms, which is confounded by the demographic history of the species under study and the statistical methodology used for inferring selection.…”

The insertion of a mitochondrial selfish element into the nuclear genome and its consequences

“…In the second scenario, the mitochondrial HEG was not ancestral to U. maydis , but was horizontally transferred from S. reilianum (or a related species). The high similarity of the UMAG_11064 gene to the S. reilianum mitochondrial HEG (Figure 3) supports this hypothesis, given the relatively high nucleotide divergence between the two species, which diverged around 20 My ago (Schweizer et al., 2018). We note, however, that intronic HEGs have also been reported to show reduced nucleotide substitution rates, which can potentially explain their comparatively low divergence (Jalalzadeh et al., 2015).…”

High nucleotide substitution rates associated with retrotransposon proliferation drive dynamic secretome evolution in smut pathogens

“…Assemblies of 21.4, 20.8 and 20.4 Mb were obtained in 31, 41 and 32 contigs for U. nuda, U. loliicola and U. tritici, respectively (Table 1). A phylogenetic tree was constructed, which included the newly sequenced species as well as U. brachipodii-distachyi, U. maydis and S. reilianum (Figure 3) (25,27,37,38). U. hordei, U. nuda, U. brachipodii-distachyi and U. tritici cluster together with U. loliicola being the closest outgroup species.…”