Phylogenomics of Plant-Associated Botryosphaeriaceae Species.

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

doi:10.3389/fmicb.2021.652802

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.

Highlights

The fungal family Botryosphaeriaceae (Botryosphaeriales, Dothideomycetes) was introduced in 1918 by Theissen and Sydow (1918) with Botryosphaeria as the type genus
Our objective is to examine through phylogenomic comparisons this comprehensive set of species on one host, grape, to better understand the evolutionary trends within this important fungal family, especially as it pertains to the gene space involving pathogenesis of woody tissues and fungal virulence
To expand the genomic information for Botryosphaeriaceae, we de novo assembled the genomes of fifteen species isolated from multiple hosts

Summary

Introduction

The fungal family Botryosphaeriaceae (Botryosphaeriales, Dothideomycetes) was introduced in 1918 by Theissen and Sydow (1918) with Botryosphaeria as the type genus. Members of this group have been taxonomically characterized based on the production of large, ovoid to oblong, typically hyaline, aseptate ascospores, which may become brown and septate with age, within bitunicate asci within unilocular or multilocular botryose ascomata known as pseudothecia (Sivanesan, 1984; Phillips et al, 2005). The asexual states of Botryosphaeriaceae exhibit a wide range of conidial morphologies that are taxonomically informative (Phillips et al, 2005). The Botryosphaeriaceae is currently composed of 24 well-defined genera and more than 200 species (Burgess et al, 2019) that are cosmopolitan in distribution and exist primarily as saprobes, endophytes, or pathogens on a wide array of important perennial plant hosts (Slippers and Wingfield, 2007), in both humanaltered (agricultural and urban) and natural ecosystems (forests and riparian areas) (Slippers et al, 2009; Lawrence et al, 2017)

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