Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among "white rot" fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates-"brown rot." The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of "decay-stage-dependent" ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brown rot ROS-generating genes with iron ion binding functions were isolated. Moreover, transcription energy was shifted to be invested on the retained GHs in brown rot fungi to strengthen carbohydrate conversion. Collectively, these results support the hypothesis that gene regulation shifts played a pivotal role in brown rot adaptation.IMPORTANCE Fungi dominate the turnover of wood, Earth's largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot "shortcut" often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.

中文翻译：

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基因调控转移了对植物生物质分解器中真菌适应性的关注。

真菌主导着木质生物量中固存的碳的循环利用。这种有机转换的过程首先在降解木质素以获取碳水化合物的“白腐”真菌中发展，然后多次进化为选择性靶向碳水化合物的“棕腐”更有效的策略。褐腐病的适应性通常是通过部署活性氧（ROS）来氧化侵蚀木质结构的机制来解释的。然而，其遗传基础仍然不清楚，特别是在传统碳水化合物活性酶（CAZYs）相对于白腐祖先的基因收缩的情况下。在这里，我们假设尽管基因丢失，但褐腐效率的这些明显提高部分归因于保留基因的上调。我们将比较转录组学应用于在木质薄片上生长的两种腐烂类型的多种物种，以创建渐进式衰减的梯度并能够跟踪时间基因表达。分离了数十个“衰变阶段依赖性”原基因，从而使褐腐真菌独有的时间依赖性调控作用缩小了候选基因库。对CAZY家族表达时间的广泛比较表明，与白腐病相比，木质纤维素氧化基因在棕腐病中向白腐病的早期阶段有暂时的转移，从而能够在水解之前分离出氧化处理。分离出这些具有铁离子结合功能的关键褐腐ROS产生基因。此外，转录能被转移到褐腐真菌中保留的GH上，以增强碳水化合物的转化。总的来说，这些结果支持了基因调控转移在褐腐病适应中起关键作用的假设。重要信息真菌主导着木材的周转，这是地球上最大的地面陆地碳库。真菌首先通过降解木质素来获取和水解嵌入的碳水化合物（白腐菌）来发展这种能力。但是，多个谱系适应了更快的活性氧（ROS）预处理，以使木质纤维素松散并选择性地提取糖（褐腐病）。这种褐色腐烂的“捷径”通常与常规木质纤维素分解基因的丢失（> 60％）相吻合，这表明ROS适应取代了常规途径。我们使用比较转录组学进一步研究了褐腐病的适应，从而阐明了ROS基因的明显瞬时表达变化，以及相对于白腐病，在褐腐病中合成更多GH的转变。这些暗示基因调节变化，而不是简单的ROS创新，是褐腐真菌进化的关键。这些结果不仅揭示了这些独特真菌之间的重要生物学变化，而且还可以阐明将褐腐真菌限制在某些生态位上的特征。