Phylogenomics of plant-associated Botryosphaeriaceae species

Authors: GARCIA, JADRAN - University Of California, Davis; LAWRENCE, DANIEL - University Of California, Davis; MORALES-CRUZ, ABRAHAM - University Of California; TRAVADON, RENAUD - University Of California, Davis; MINIO, ANDREA - University Of California, Davis; HERNANDEZ-MARTINEZ, RUFINA - Centro De Investigacion Cientifica Y De Educacion Superior De Ensenada; ROLSHAUSEN, PHILLIPPE - University Of California; Baumgartner, Kendra; CANTU, DARIO - University Of California, Davis

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/25/2021
Publication Date: 3/18/2021
Citation: Garcia, J., Lawrence, D.P., Morales-Cruz, A., Travadon, R., Minio, A., Hernandez-Martinez, R., Rolshausen, P.E., Baumgartner, K., Cantu, D. 2021. Phylogenomics of plant-associated Botryosphaeriaceae species. Frontiers in Microbiology. 12. Article 652802. https://doi.org/10.3389/fmicb.2021.652802.
DOI: https://doi.org/10.3389/fmicb.2021.652802

Interpretive Summary: The Botryosphaeriaceae is a fungal family that includes many destructive pathogens of woody plants (e.g., Botryosphaeria dieback of grape, Panicle blight of pistachio). Species in the genera Botryosphaeria, Diplodia, Dothiorella, Lasiodiplodia, Neofusicoccum, and Neoscytalidium attack a range of horticultural crops (e.g., grapevines, orchard trees, rose bushes, street trees), but they vary in aggressiveness and in their abilities to infect their host plants via different entry points (flowers, green shoots, woody twigs). Isolates of seventeen species, originating from symptomatic apricot, grape, pistachio, and walnut were inoculated to the woody stems of grapevines grown in the greenhouse. Results revealed significant variation in virulence in terms of the length of the internal wood lesions caused by these seventeen species. Comparisons of the genes expressed by each species during infection revealed gene families representing putative virulence factors involved in toxin production and mobilization, wood degradation, and nutrient uptake. Statistical analyses of the evolution of the size of gene families revealed expansions of secondary metabolism and transporter gene families in Lasiodiplodia and of secreted cell wall degrading enzymes (CAZymes) in Botryosphaeria and Neofusicoccum genomes. In contrast, Diplodia, Dothiorella, and Neoscytalidium generally showed a contraction in the number of members of these gene families. Overall, species with expansions of gene families, such as secreted CAZymes, secondary metabolism, and transporters, were the most virulent (i.e., were associated with the largest lesions), based on our pathogenicity tests and published reports. This study represents the first comparative phylogenomic investigation into the evolution of possible virulence factors from diverse, cosmopolitan members of the Botryosphaeriaceae.

Technical Abstract: The Botryosphaeriaceae is a fungal family that includes many destructive vascular pathogens of woody plants (e.g., Botryosphaeria dieback of grape, Panicle blight of pistachio). Species in the genera Botryosphaeria, Diplodia, Dothiorella, Lasiodiplodia, Neofusicoccum, and Neoscytalidium attack a range of horticultural crops, but they vary in virulence and in their abilities to infect their hosts via different infection courts (flowers, green shoots, woody twigs). Isolates of seventeen species, originating from symptomatic apricot, grape, pistachio, and walnut were tested for pathogenicity to grapevine wood after four months of incubation in potted plants in the greenhouse. Results revealed significant variation in virulence in terms of the length of the internal wood lesions caused by these seventeen species. Phylogenomic comparisons of the seventeen species of wood-colonizing fungi revealed clade-specific expansion of gene families representing putative virulence factors involved in toxin production and mobilization, wood degradation, and nutrient uptake. Statistical analyses of the evolution of the size of gene families revealed expansions of secondary metabolism and transporter gene families in Lasiodiplodia and of secreted cell wall degrading enzymes (CAZymes) in Botryosphaeria and Neofusicoccum genomes. In contrast, Diplodia, Dothiorella, and Neoscytalidium generally showed a contraction in the number of members of these gene families. Overall, species with expansions of gene families, such as secreted CAZymes, secondary metabolism, and transporters, were the most virulent (i.e., were associated with the largest lesions), based on our pathogenicity tests and published reports. This study represents the first comparative phylogenomic investigation into the evolution of possible virulence factors from diverse, cosmopolitan members of the Botryosphaeriaceae.