Lifestyle changes in Botryosphaeriaceae as evidenced by ancestral genome expansion and horizontal gene transfer

• Published in: Fungal diversity Vol. 125; no. 1; pp. 221 - 241
• Main Authors: Wang, Xuncheng, Zhang, Wei, Peng, Junbo, Manawasinghe, Ishara S., Wu, Linna, Li, Yonghua, Xing, Qikai, Li, Xinghong, Yan, Jiye
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 01-03-2024; Springer Nature B.V
• Subjects: Biodiversity; Biological evolution; Biomedical and Life Sciences; Botryosphaeriaceae; Detoxification; Divergence; Dothideomycetes; Ecological adaptation; Endophytes; Evolution; Gene sequencing; Gene transfer; Genes; Genetic engineering; Genomes; Horizontal transfer; Host plants; Infections; Life Sciences; Lifestyles; Medical Microbiology; Microbial Ecology; Microbiology; Mycology; Offspring; Opportunist infection; Pathogenicity; Pathogens; Phylogeny; Plant Physiology; Sequence analysis; Species; Woody plants; Phenolic degradation; Iron uptake; Plant fungi pathogens
• ISSN: 1878-9129; 1560-2745; 1878-9129
• DOI: 10.1007/s13225-023-00530-7

Botryosphaeriaceae
(Botryosphaeriales, Dothideomycetes, Ascomycota) encompasses commonly encountered opportunistic pathogens that cause stem cankers on woody plants. Lifestyles of
Botryosphaeriaceae
species could vary as endophytes, pathogens and saprobes and one species can have one or more lifestyles. Therefore, this family is an excellent candidate to study the relationships among lifestyles and lifestyle changes. It is postulated that this family has saprobic ancestors, and the mechanisms by which they evolved from nonpathogenic ancestors to woody pathogens remain unclear. Here, we present an analysis of 18
Botryosphaeriaceae
genomes, including four newly generated high-quality genomes of
Botryosphaeriaceae
strains. We compared
Botryosphaeriaceae
genomes with phylogenetically closely related Dothideomycetes taxa including plant pathogens and saprobes which revealed significant net gene family expansion in
Botryosphaeriaceae
. This gene expansion is prominent in the early ancestors before the divergence of genera of
Botryosphaeriaceae
. This expansion affected the pathogenicity-related genes and detoxification genes. Furthermore, we analysed horizontal gene transfer, which is a mechanism of transfer to genetic material between organisms that are not in a parent–offspring relationship and identified widespread putative intra-kingdom horizontal gene transfer events in this family. Most were transferred during the evolution of ancient ancestors of
Botryosphaeriaceae
, before the divergence of the modern genera and were enriched in pathogenicity-related genes and detoxification genes. Furthermore, The RNA sequencing analysis of the
Botryosphaeriaceae
species
Lasiodiplodia theobromae
revealed that pathogenicity-related genes and detoxification genes, including those obtained through gene family expansion and horizontal gene transfers, were significantly induced after the infection of plant hosts rather than before infection. These insights reveal critical roles for gene family expansion and horizontal gene transfers in the evolutionary adaptation of
Botryosphaeriaceae
in the infection of woody plants. We postulate that the pathogenic lifestyle of
Botryosphaeriaceae
species evolved from saprobic or endophytic lifestyles in the early divergence of this family. However, there are few endophytic genomes available for closely related species of
Botryosphaeriaceae
, thus further studies are necessary to clarify the evolutionary relationships of the endophytes.