Integrative Activity of Mating Loci, Environmentally Responsive Genes, and Secondary Metabolism Pathways during Sexual Development of Chaetomium globosum
Integrative Activity of Mating Loci, Environmentally Responsive Genes, and Secondary Metabolism Pathways during Sexual Development of Chaetomium globosum
复制标题
DOI：
10.1128/mbio.02119-19
复制
发表时间：
2019-12
期刊：
影响因子：
6.4
通讯作者：
Z. Wang;F. López-Giráldez;Junrui Wang;F. Trail;J. Townsend
中科院分区：
文献类型：
--
作者：
Z. Wang;F. López-Giráldez;Junrui Wang;F. Trail;J. Townsend
几十年来，真菌的多样性一直令进化生物学家感到惊讶。这种多样性在社会上的一个重要方面表现在使致病性成为可能的性状上。机会致病菌毛藻（Chaetomium globosum）很好地适应了高湿度的环境，并产生了大量的次生代谢物来保护自己免受捕食。其中许多化学物质会威胁人体健康。了解C. globosum生命周期的各个阶段，这些产品可以更好地控制和利用这种真菌。其有趣的特点之一是，它既能自我繁殖，又缺乏任何以繁殖为基础的无性繁殖方式。通过分析C. globosum有性生殖过程的全基因组基因表达，并将其与模式丝状真菌N. crassa和其他近缘真菌的全基因组基因表达进行比较，揭示了交配型基因、性发育基因、性不相容调节因子、环境响应基因和次生代谢途径之间的关联。真菌丰富多样性的起源和维持一直是进化生物学中长期存在的问题。为了研究表达调控的差异如何导致密切相关物种之间的发育和生态差异，研究人员比较了在高度潮湿生态环境中生长的同源致病菌毛藻（Chaetomium globosum）和异源腐养菌粗神经孢子菌（Neurospora crassa）的转录组。在几乎同步的性发育过程中，基因表达在包皮鞘的九个不同形态阶段被量化。与草草不同的是，所有交配位点的表达都是高度相关的。光刺激下棘草性发育启动的关键调控因子（包括棘草亚-1同源基因、亚-1依赖基因NCU00309和asl-1）在棘草和棘草之间显示出调控动态匹配。在24个次生代谢基因簇中，包括蜗酮生物合成基因簇在内的11个基因簇在囊周发育过程中表现出高度协调的表达。在高渗透反应途径中，C. globosum表现出协调上调的组氨酸激酶表达，这与我们在同类病原体镰刀菌（Fusarium graminearum）中发现的高湿度基因表达反应一致。贝叶斯网络表明，性发育过程中的基因相互作用与无性繁殖和自相容与自不相容的生命周期的能力相一致，改变了与萌发和异核不相容相关的基因的等级作用。这种分化支持了同源物种中由于异核体不亲和性的不利组合而导致条件丧失的进化史。几十年来，真菌的多样性一直令进化生物学家感到惊讶。这种多样性在社会上的一个重要方面表现在使致病性成为可能的性状上。机会致病菌毛藻（Chaetomium globosum）很好地适应了高湿度的环境，并产生了大量的次生代谢物来保护自己免受捕食。其中许多化学物质会威胁人体健康。了解C. globosum生命周期的各个阶段，这些产品可以更好地控制和利用这种真菌。其有趣的特点之一是，它既能自我繁殖，又缺乏任何以繁殖为基础的无性繁殖方式。通过分析C. globosum有性生殖过程的全基因组基因表达，并将其与模式丝状真菌N. crassa和其他近缘真菌的全基因组基因表达进行比较，揭示了交配型基因、性发育基因、性不相容调节因子、环境响应基因和次生代谢途径之间的关联。
Fungal diversity has amazed evolutionary biologists for decades. One societally important aspect of this diversity manifests in traits that enable pathogenicity. The opportunistic pathogen Chaetomium globosum is well adapted to a high-humidity environment and produces numerous secondary metabolites that defend it from predation. Many of these chemicals can threaten human health. Understanding the phases of the C. globosum life cycle in which these products are made enables better control and even utilization of this fungus. Among its intriguing traits is that it both is self-fertile and lacks any means of propagule-based asexual reproduction. By profiling genome-wide gene expression across the process of sexual reproduction in C. globosum and comparing it to genome-wide gene expression in the model filamentous fungus N. crassa and other closely related fungi, we revealed associations among mating-type genes, sexual developmental genes, sexual incompatibility regulators, environmentally responsive genes, and secondary metabolic pathways. ABSTRACT The origins and maintenance of the rich fungal diversity have been longstanding issues in evolutionary biology. To investigate how differences in expression regulation contribute to divergences in development and ecology among closely related species, transcriptomes were compared between Chaetomium globosum, a homothallic pathogenic fungus thriving in highly humid ecologies, and Neurospora crassa, a heterothallic postfire saprotroph. Gene expression was quantified in perithecia at nine distinct morphological stages during nearly synchronous sexual development. Unlike N. crassa, expression of all mating loci in C. globosum was highly correlated. Key regulators of the initiation of sexual development in response to light stimuli—including orthologs of N. crassa sub-1, sub-1-dependent gene NCU00309, and asl-1—showed regulatory dynamics matching between C. globosum and N. crassa. Among 24 secondary metabolism gene clusters in C. globosum, 11—including the cochliodones biosynthesis cluster—exhibited highly coordinated expression across perithecial development. C. globosum exhibited coordinately upregulated expression of histidine kinases in hyperosmotic response pathways—consistent with gene expression responses to high humidity we identified in fellow pathogen Fusarium graminearum. Bayesian networks indicated that gene interactions during sexual development have diverged in concert with the capacities both to reproduce asexually and to live a self-compatible versus self-incompatible life cycle, shifting the hierarchical roles of genes associated with conidiation and heterokaryon incompatibility in N. crassa and C. globosum. This divergence supports an evolutionary history of loss of conidiation due to unfavorable combinations of heterokaryon incompatibility in homothallic species. IMPORTANCE Fungal diversity has amazed evolutionary biologists for decades. One societally important aspect of this diversity manifests in traits that enable pathogenicity. The opportunistic pathogen Chaetomium globosum is well adapted to a high-humidity environment and produces numerous secondary metabolites that defend it from predation. Many of these chemicals can threaten human health. Understanding the phases of the C. globosum life cycle in which these products are made enables better control and even utilization of this fungus. Among its intriguing traits is that it both is self-fertile and lacks any means of propagule-based asexual reproduction. By profiling genome-wide gene expression across the process of sexual reproduction in C. globosum and comparing it to genome-wide gene expression in the model filamentous fungus N. crassa and other closely related fungi, we revealed associations among mating-type genes, sexual developmental genes, sexual incompatibility regulators, environmentally responsive genes, and secondary metabolic pathways.