Genomic evidence for convergent evolution of gene clusters for momilactone biosynthesis in land plants

Genomic evidence for convergent evolution of gene clusters for momilactone biosynthesis in land plants
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DOI:
10.1073/pnas.1914373117
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发表时间:
2020-06-02
影响因子:
11.1
通讯作者:
Okada, Kazunori
Okada, Kazunori
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Mao, Lingfeng;Kawaide, Hiroshi;Okada, Kazunori

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木霉内酯是一类具有生物活性的二萜类化合物,有助于植物对病原菌的防御和植物之间的化感作用。栽培种和野生种的水稻和藜草都利用其基因组中的生物合成基因簇(BGC)产生菊内酮。苔藓植物Calothnum plumiforme(前身为Hypnum plumaeforme)也产生双内酯类化合物,并对负责产生二萜骨架的双功能二萜环化酶基因CpDTC1/HpDTC1进行了鉴定。为了了解苔藓基因组中丁香内酯生物合成基因的分子结构,以及它们与其他产生丁香内酯的植物的进化关系,我们对丁香内酯的基因组进行了测序和注释。数据显示了一个150kb的基因组区域,其中包含两个细胞色素P450基因,CpDTC1/HpDTC1基因和“脱氢酶-双乳糖酯A合成酶”基因,它们在应激暴露后被随机排列并诱导转录。在酵母和重组实验中预测的酶功能,以及在本氏烟草中成功的途径重组表明,它是一个负责产生莫米内酯的功能性BGC。此外,在对广泛的植物物种的基因组序列的调查中,我们发现吗丁内酯BGC仅限于两种禾本科植物(水稻和棘豆)和蒲公英,这些基因组之间没有同系性。这些结果表明,虽然鸭茅中的基因簇在功能上与水稻和偃麦草中的基因簇相似,但它可能是收敛进化的产物。据我们所知,这份关于苔藓植物中一种特殊植物防御代谢物的BGC报告是独一无二的。
Momilactones are bioactive diterpenoids that contribute to plant defense against pathogens and allelopathic interactions between plants. Both cultivated and wild grass species of Oryza and Echinochloa crus-galli (barnyard grass) produce momilactones using a biosynthetic gene cluster (BGC) in their genomes. The bryophyte Calohypnum plumiforme (formerly Hypnum plumaeforme) also produces momilactones, and the bifunctional diterpene cyclase gene CpDTC1/HpDTC1, which is responsible for the production of the diterpene framework, has been characterized. To understand the molecular architecture of the momilactone biosynthetic genes in the moss genome and their evolutionary relationships with other momilactone-producing plants, we sequenced and annotated the C. plumiforme genome. The data revealed a 150-kb genomic region that contains two cytochrome P450 genes, the CpDTC1/HpDTC1 gene and the "dehydrogenase momilactone A synthase" gene tandemly arranged and inductively transcribed following stress exposure. The predicted enzymatic functions in yeast and recombinant assay and the successful pathway reconstitution in Nicotiana benthamiana suggest that it is a functional BGC responsible for momilactone production. Furthermore, in a survey of genomic sequences of a broad range of plant species, we found that momilactone BGC is limited to the two grasses (Oryza and Echinochloa) and C. plumiforme, with no synteny among these genomes. These results indicate that while the gene cluster in C. plumiforme is functionally similar to that in rice and barnyard grass, it is likely a product of convergent evolution. To the best of our knowledge, this report of a BGC for a specialized plant defense metabolite in bryophytes is unique.