Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

Abstract

Summary Biotrophic fungal plant pathogens can balance their virulence and form intricate relationships with their hosts. Sometimes, this leads to systemic host colonization over long time scales without macroscopic symptoms. However, how plant‐pathogenic endophytes manage to establish their sustained systemic infection remains largely unknown. Here, we present a genomic and transcriptomic analysis of Thecaphora thlaspeos. This relative of the well studied grass smut Ustilago maydis is the only smut fungus adapted to Brassicaceae hosts. Its ability to overwinter with perennial hosts and its systemic plant infection including roots are unique characteristics among smut fungi. The T. thlaspeos genome was assembled to the chromosome level. It is a typical smut genome in terms of size and genome characteristics. In silico prediction of candidate effector genes revealed common smut effector proteins and unique members. For three candidates, we have functionally demonstrated effector activity. One of these, TtTue1, suggests a potential link to cold acclimation. On the plant side, we found evidence for a typical immune response as it is present in other infection systems, despite the absence of any macroscopic symptoms during infection. Our findings suggest that T. thlaspeos distinctly balances its virulence during biotrophic growth ultimately allowing for long‐lived infection of its perennial hosts.

Chromatin Dynamics Contribute to the Spatiotemporal Expression Pattern of Virulence Genes in a Fungal Plant Pathogen

“…Although many necrotrophic effectors have plant-specific targets ( 75 ), others act as nonspecific toxins ( 76 , 77 ), and it is possible that some of them exhibit autotoxicity that could be reduced by tight regulation. Fourth, given the typically high expression levels of effector genes during infection ( 1 , 47 , 78 , 79 ), the possibility cannot be excluded that an extra layer of regulation would reduce the metabolic costs associated with leaky expression at stages when effectors are not needed.…”

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

“…An intriguing example for a de novo gene birth is a virulence effector gene of the barley powdery mildew pathogen, which apparently had originated from a non-autonomous retrotransposon (Nottensteiner et al, 2018). Phytopathogens can also acquire new effector genes by different means (Fouch e et al, 2018), including horizontal gene transfer (HGT; as in the case of ToxA; Friesen et al, 2006), horizontal chromosome transfer (HCT, as in the case of Fusarium oxysporum; Ma et al, 2010;van Dam et al, 2017), or hybridisation between pathogen species (see Section VI below and Fig. 2).…”

“…Similar benefits could be envisaged for pathogenesis. For example, isolates of the smut fungus Thecaphora thlaspeos that are able to infect the same host may carry different effector repertoires (Courville et al, 2019). These isolates are able to mate and form infectious dikaryons, thereby expanding their pathogenicity range to additional host ecotypes.…”

The functionally conserved effector Sta1 is a fungal cell wall protein required for virulence in Ustilago maydis

“…3a). In the Brassicaceae‐infecting smut Thecaphora thlaspeos , belonging to the family Glomosporiaceae that is considered as a sister taxon of the order Urocystales (Vanky et al , 2008; Courville et al , 2019), an orthologue of sta1 could not be detected. In a phylogenetic analysis, T. thlaspeos is placed distantly from the other plant pathogenic smuts (Fig.…”