Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

Abstract

The host range of parasites is an important factor in assessing the dynamics of disease epidemics. The evolution of pathogens to accommodate new hosts may lead to host range expansion, a process the molecular bases of which are largely enigmatic. The fungus Sclerotinia sclerotiorum parasitizes more than 400 plant species from diverse eudicot families while its close relative, S. trifoliorum, is restricted to plants from the Fabaceae family. We analyzed S. sclerotiorum global transcriptome reprogramming on hosts from six botanical families and reveal a flexible, host-specific transcriptional program driven by core and host-response co-expression (SPREx) gene clusters. We generated a chromosome-level genome assembly for S. trifoliorum and found near-complete gene space conservation in broad and narrow host range Sclerotinia species. However, S. trifoliorum showed increased sensitivity to the Brassicaceae defense compound camalexin. Inter-specific transcriptome analyses revealed a lack of transcriptional response to camalexin in S. trifoliorum and provide evidence that cis-regulatory variation associates with the genetic accommodation of Brassicaceae in the Sclerotinia host range. Our work demonstrates adaptive plasticity of a broad host range pathogen with specific responses to different host plants and demonstrates the co-existence of signatures for generalist and polyspecialist life styles in the genome of a plant pathogen. We reason that this mechanism enables the emergence of new disease with no or limited gene flow between strains and species, and could underlie the emergence of new epidemics originating from wild plants in agricultural settings.

A broadly conserved fungal alcohol oxidase (AOX) facilitates fungal invasion of plants

“…This runs contrary to many necrotrophic pathosystems in which we expect the pathogen to contend with increasingly lignified plant material and a greater concentration of monolignols over the progression of infection (Huang et al, 2019; Mwape et al, 2021; Westrick et al, 2019). To assess the relative importance of AOX within a specific pathogen across multiple hosts, we additionally evaluated the expression of SsAOX during the infection of six distinct hosts from publicly available transcriptomic data (Kusch et al, 2021). On all hosts SsAOX was found to be up‐regulated between 200‐ and 5000‐fold when compared to an in vitro control, suggesting that SsAOX is highly expressed during infection in a nonhost‐specific manner (Kusch et al, 2021).…”

“…To assess the relative importance of AOX within a specific pathogen across multiple hosts, we additionally evaluated the expression of SsAOX during the infection of six distinct hosts from publicly available transcriptomic data (Kusch et al, 2021). On all hosts SsAOX was found to be up‐regulated between 200‐ and 5000‐fold when compared to an in vitro control, suggesting that SsAOX is highly expressed during infection in a nonhost‐specific manner (Kusch et al, 2021).…”

The evolutionary and molecular features of the broad‐host‐range plant pathogen Sclerotinia sclerotiorum

“…Several of these genes contained domains linked with metabolism and efflux of xenobiotic compounds, such as cytochrome P450, major facilitator superfamily, and tannase domains. Echoing these findings, Kusch et al (2022) showed that colonization of distinct host species led to a specific signature of cytochrome P450 induction. This was in line with a wider observation that infection of different host species induces different transcriptional programmes in S. sclerotiorum .…”

“…A good starting place for this kind of research would be sequencing and comparison of the complete genomes of these species, which could determine which genes are shared and unique and whether this correlates with host preference or other lifestyle attributes, although only one study so far has used this approach. Kusch et al (2022) showed that 67.2% of the S. trifoliorum genome was syntenic with that of S. sclerotiorum . Out of the 10,626 genes predicted in the S .…”

“…Most research on these species is focused on practical means of control and there has, unfortunately, been little to no molecular research on them to date. Given that these pathogens infect diverse host species but with differing host range restrictions, for example, S. trifoliorum is specific to the Fabaceae (Kusch et al, 2022), it would be interesting to compare the molecular mechanisms of their pathogenesis with those of S. sclerotiorum .…”