Large-scale transcriptomics to dissect two years of life of a fungal phytopathogen in interaction(s) with its host plant

The fungus Leptosphaeria maculans has an exceptionally long and complex relationship with its host plant, Brassica napus, during which it switches between different lifestyles including asymptomatic, biotrophic, necrotrophic, and saprotrophic stages. The fungus is also exemplary of two-speed genome organisms in which the genome alternates between gene-rich regions and repeat-rich regions, which define respectively core and rapidly evolving genomic compartments. So far, apart for a few stages of the plant interaction under controlled conditions, nothing is known about the genes mobilized by the fungus during all stages of its two-year or longer interaction with plant tissues under controlled conditions or in the field, or about the regulation of their expression. Here, we show that ca. 9% of genes of the fungal genome are highly over-expressed uniquely during its life with the plant, that fall into eight well-defined expression profiles. These eight waves of expression correspond to specific infection lifestyles or to tissue-specific genes. Whatever the wave, the genomic environment of the genes they contain are regions enriched in heterochromatin, either constitutive or facultative. In addition, all but two waves are enriched in effector genes. Importantly, the same set of 148 genes, including genes already known to be involved in the first phase of asymptomatic fungal growth in leaves, is re-used at each asymptomatic growth stage, regardless of the type of infected organ; their expression is turned on/off multiple times during the infection, illustrating the importance of chromatin dynamics for pathogenicity. Lastly, one wave of expression, also enriched in effector genes, is typical of the saprophytic lifestyle on leftover plant residues. These findings reinforce the postulate that fungal genes involved in niche adaptation are located in heterochromatic regions of the genomes, thus providing them with an extreme plasticity of expression and reactivity to changes of the plant environment. This work opens new avenues for plant disease control by identifying stage-specific effectors that may be used as targets to identify novel durable disease resistance genes, or by in-depth analysis of chromatin remodeling during plant infection, which could be manipulated to interfere with global expression of effector genes at crucial stages of plant infection.