Comparative Genomics Reveals Evolutionary Traits, Mating Strategies, and Pathogenicity-Related Genes Variation of Botryosphaeriaceae

Abstract

Botryosphaeriaceae, as a major family of the largest class of kingdom fungi Dothideomycetes, encompasses phytopathogens, saprobes, and endophytes. Many members of this family are opportunistic phytopathogens with a wide host range and worldwide geographical distribution, and can infect many economically important plants, including food crops and raw material plants for biofuel production. To date, however, little is known about the family evolutionary characterization, mating strategies, and pathogenicity-related genes variation from a comparative genome perspective. Here, we conducted a large-scale whole-genome comparison of 271 Dothideomycetes, including 19 species in Botryosphaeriaceae. The comparative genome analysis provided a clear classification of Botryosphaeriaceae in Dothideomycetes and indicated that the evolution of lifestyle within Dothideomycetes underwent four major transitions from non-phytopathogenic to phytopathogenic. Mating strategies analysis demonstrated that at least 3 transitions were found within Botryosphaeriaceae from heterothallism to homothallism. Additionally, pathogenicity-related genes contents in different genera varied greatly, indicative of genus-lineage expansion within Botryosphaeriaceae. These findings shed new light on evolutionary traits, mating strategies and pathogenicity-related genes variation of Botryosphaeriaceae.

Pathogenicity Factors of Botryosphaeriaceae Associated with Grapevine Trunk Diseases: New Developments on Their Action on Grapevine Defense Responses

“…Species belonging to the Macrophomina, Botryosphaeria and Neofusicoccum genera are described as containing between 922 and 1118 SPs compared to only 671 to 866 SP in the genera Diplodia. In the same study, the authors indicate that two Botryosphaeriaceae genera (Macrophomina and Botryosphaeria) may be able to release over 250 SSPs while all Diplodia species considered produce less than 200 SSPs [33]. The most studied small effectors are probably the small cysteine-rich secreted proteins (SCSP).…”

“…Thus, it has been postulated that these symptoms are due to phytotoxins and secreted proteins (SP) produced by the fungi in the perennial part of the plant and then translocated to the leaves through the transpiration stream [31,32]. Moreover, for many pathogens, particularly in fungi and oomycetes, the excretion of proteins is essential for pathogenicity [33].…”

“…These SSPs play an important role in the plant-fungal interaction and in pathogen virulence mechanisms [34]. Few studies have been conducted on these effectors in the Botryosphaeriaceae family, but Yu et al (2022) reported that the number of SP widely varies between genera of Botryosphaeriaceae [33]. Species belonging to the Macrophomina, Botryosphaeria and Neofusicoccum genera are described as containing between 922 and 1118 SPs compared to only 671 to 866 SP in the genera Diplodia.…”

“…These enzymes can be intra-or extracellular, the latter being the most involved in the degradation of primary and secondary plant cell walls [27,[43][44][45][46][47][48]. Compared to other Dothideomycetes, Botryosphaeriaceae genomes are richer in CAZymes-related genes [46,49,50], such as Colletotrichum and Fusarium species which share the same lifestyle plasticity and broad host range [10,25,33]. This high content of CAZymes in Botryosphaeriaceae genomes is closely similar to that of opportunistic fungi, more than pathogenic fungi [10].…”

Intraspecific Comparative Analysis Reveals Genomic Variation of Didymella arachidicola and Pathogenicity Factors Potentially Related to Lesion Phenotype

“…Next-generation sequencing technologies have been widely used to study plant pathogens and greatly facilitated understanding of fungal evolution and virulence factors [ 22 , 23 , 24 , 25 , 26 , 27 ]. The lifestyle of fungal species in Dothideomycetes evolves in four major transitions from non-phytopathogenic to phytopathogenic, along with the pathogenicity-related genes carried in different genera varying considerably [ 28 ]. Fungi virulence has been revealed to be associated with the number of certain secreted proteins, including CAZy proteins [ 29 ].…”