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.

Botryosphaeriaceae （Botryosphaeriales、Dothideomycetes、Ascomycota）包括常见的机会致病菌，可引起木本植物茎溃疡病。葡萄球菌科物种的生活方式可能因内生菌、病原体和腐生菌而异，并且一个物种可以有一种或多种生活方式。因此，这个家庭是研究生活方式和生活方式改变之间关系的绝佳候选者。据推测，该科具有腐生祖先，但它们从非致病祖先进化为木本病原体的机制仍不清楚。在这里，我们对 18 个葡萄球菌科基因组进行了分析，其中包括四个新生成的葡萄球菌科菌株的高质量基因组。我们将Botryosphaeriaceae基因组与系统发育密切相关的 Dothideomycetes 类群（包括植物病原体和腐生菌）进行了比较，揭示了Botryosphaeriaceae中显着的净基因家族扩张。这种基因扩展在葡萄球菌属分化之前的早期祖先中很突出。这种扩张影响了致病性相关基因和解毒基因。此外，我们分析了水平基因转移，这是一种在不具有亲子关系的生物体之间转移遗传物质的机制，并确定了该家族中广泛存在的假定王国内水平基因转移事件。大多数是在现代属分化之前，在葡萄孢科远古祖先的进化过程中转移的，并且富含致病性相关基因和解毒基因。 此外，对葡萄球菌科物种Lasiodiplodia theobromae的RNA测序分析表明，致病性相关基因和解毒基因，包括通过基因家族扩展和水平基因转移获得的基因，在感染植物宿主后而不是感染前显着诱导。这些见解揭示了基因家族扩展和水平基因转移在葡萄球菌科在木本植物感染中的进化适应中的关键作用。我们假设葡萄球菌科物种的致病生活方式是在该科早期分化过程中从腐生或内生生活方式进化而来的。然而，与葡萄球菌科密切相关的物种的内生基因组很少，因此需要进一步的研究来阐明内生菌的进化关系。