CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.
BMC Genomics. 2019 Mar 8;20(1):198. doi: 10.1186/s12864-019-5575-7.
Genomes of lethal Amanita and Galerina mushrooms have gradually become available in the past ten years; in contrast the other known amanitin-producing genus, Lepiota, is still vacant in this aspect. A fatal mushroom poisoning case in China has led to acquisition of fresh L. venenata fruiting bodies, based on which a draft genome was obtained through PacBio and Illumina sequencing platforms. Toxin-biosynthetic MSDIN family and Porlyl oligopeptidase B (POPB) genes were mined from the genome and used for phylogenetic and statistical studies to gain insights into the evolution of the biosynthetic pathway.
The analysis of the genome data illustrated that only one MSDIN, named LvAMA1, exits in the genome, along with a POPB gene. No POPA homolog was identified by direct homology searching, however, one additional POP gene, named LvPOPC, was cloned and the gene structure determined. Similar to ApAMA1 in A. phalloides and GmAMA1 in G. marginata, LvAMA1 directly encodes α-amanitin. The two toxin genes were mapped to the draft genome, and the structures analyzed. Furthermore, phylogenetic and statistical analyses were conducted to study the evolution history of the POPB genes. Compared to our previous report, the phylogenetic trees unambiguously showed that a monophyletic POPB lineage clearly conflicted with the species phylogeny. In contrast, phylogeny of POPA genes resembled the species phylogeny. Topology and divergence tests showed that the POPB lineage was robust and these genes exhibited significantly shorter genetic distances than those of the house-keeping rbp2, a characteristic feature of genes with horizontal gene transfer (HGT) background. Consistently, same scenario applied to the only MSDIN, LvAMA1, in the genome.
To the best of our knowledge, this is the first reported genome of Lepiota. The analyses of the toxin genes indicate that the cyclic peptides are synthesized through a ribosomal mechanism. The toxin genes, LvAMA1 and LvPOPB, are not in the vicinity of each other. Phylogenetic and evolutionary studies suggest that HGT is the underlining cause for the occurrence of POPB and MSDIN in Amanita, Galerina and Lepiota, which are allocated in three distantly-related families.
在过去十年中，致命鹅膏菌和鹅膏菌属的基因组逐渐被揭示；相比之下，其他已知的产生鹅膏肽的属——环柄菇属，在这方面仍然是空白。中国发生了一起致命蘑菇中毒事件，导致采集到了新鲜的环柄菇属毒蕈，在此基础上，通过 PacBio 和 Illumina 测序平台获得了一个基因组草图。从基因组中挖掘出毒素生物合成 MSDIN 家族和脯氨酰寡肽酶 B（POPB）基因，并进行系统发育和统计研究，以深入了解生物合成途径的进化。
基因组数据分析表明，基因组中仅存在一个 MSDIN，命名为 LvAMA1，以及一个 POPB 基因。通过直接同源搜索未鉴定出 POPA 同源物，但是克隆并确定了一个额外的 POP 基因，命名为 LvPOPC。与鹅膏菌属的 ApAMA1 和鹅膏菌属的 GmAMA1 相似，LvAMA1 直接编码α-鹅膏肽。将这两个毒素基因定位到基因组草图上，并对其结构进行了分析。此外，还进行了系统发育和统计分析，以研究 POPB 基因的进化历史。与我们之前的报告相比，系统发育树明确表明，一个单系的 POPB 谱系与物种系统发育明显冲突。相比之下，POPA 基因的系统发育与物种系统发育相似。拓扑和分歧测试表明，POPB 谱系是稳健的，与经历了水平基因转移（HGT）的基因的特征一致，这些基因的遗传距离明显短于管家基因 rbp2。同样的情况也适用于基因组中唯一的 MSDIN，LvAMA1。
据我们所知，这是环柄菇属的第一个基因组报道。毒素基因的分析表明，环状肽是通过核糖体机制合成的。毒素基因 LvAMA1 和 LvPOPB 彼此不相邻。系统发育和进化研究表明，HGT 是鹅膏菌属、鹅膏菌属和环柄菇属中出现 POPB 和 MSDIN 的根本原因，这三个属分别属于三个远缘相关的科。
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