Phylogenomics of Plant-Associated Botryosphaeriaceae Species

Jadran F Garcia; Daniel P Lawrence; Abraham Morales-Cruz; Renaud Travadon; Andrea Minio; Rufina Hernandez-Martinez; Philippe E Rolshausen; Kendra Baumgartner; Dario Cantu

doi:10.3389/fmicb.2021.652802

Phylogenomics of Plant-Associated Botryosphaeriaceae Species

Front Microbiol. 2021 Mar 18:12:652802. doi: 10.3389/fmicb.2021.652802. eCollection 2021.

Authors

Jadran F Garcia¹, Daniel P Lawrence², Abraham Morales-Cruz^{1

3}, Renaud Travadon², Andrea Minio¹, Rufina Hernandez-Martinez⁴, Philippe E Rolshausen⁵, Kendra Baumgartner⁶, Dario Cantu¹

Affiliations

¹ Department of Viticulture and Enology, University of California, Davis, Davis, CA, United States.
² Department of Plant Pathology, University of California, Davis, Davis, CA, United States.
³ Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, United States.
⁴ Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada, Mexico.
⁵ Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United States.
⁶ Crops Pathology and Genetics Research Unit, United States Department of Agriculture - Agricultural Research Service, Davis, CA, United States.

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 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 on grapevine wood after 4 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.

Keywords: Botryosphaeria dieback; cell wall degrading enzymes; comparative genomics; gene family evolution; grapevine trunk diseases; secondary metabolism; virulence factors.