Genetic co-option into plant-filamentous pathogen interactions.

Plants are engaged in a coevolutionary arms race with their pathogens that drives rapid diversification and specialization of genes involved in resistance and virulence. However, some major innovations in plant-pathogen interactions, such as molecular decoys, trans-kingdom RNA interference, two-speed genomes, and receptor networks, evolved through the expansion of the functional landscape of genes. This is a typical outcome of genetic co-option, the evolutionary process by which available genes are recruited into new biological functions. Co-option into plant-pathogen interactions emerges generally from (i) cis-regulatory variation, (ii) horizontal gene transfer (HGT), (iii) mutations altering molecular promiscuity, and (iv) rewiring of gene networks and protein complexes. Understanding these molecular mechanisms is key for the functional and predictive biology of plant-pathogen interactions.

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

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 has been reported to parasitize 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. We generated a chromosome-level genome assembly for S. trifoliorum and found near-complete gene space conservation in two representative strains of broad and narrow host range Sclerotinia species. However, S. trifoliorum showed increased sensitivity to the Brassicaceae defense compound camalexin. Comparative analyses revealed a lack of transcriptional response to camalexin in the S. trifoliorum strain and suggest that regulatory variation in detoxification and effector genes at the population level may associate with the genetic accommodation of Brassicaceae in the Sclerotinia host range. Our work proposes transcriptional plasticity and the co-existence of signatures for generalist and polyspecialist adaptive strategies in the genome of a plant pathogen.