Microbial-type terpene synthases significantly contribute to the terpene profile of glandular trichomes of the fern Dryopteris fragrans (L.)

IF 6.2 1区 生物学 Q1 PLANT SCIENCES The Plant Journal Pub Date : 2025-03-14 DOI:10.1111/tpj.70079
Lingling Chen, Rui Gao, Guo Wei, Shihong Luo, Tobias G. Köllner, Houchao Xu, Yifan Jiang, Chi Zhang, Xinlu Chen, Jeroen S. Dickschat, Jonathan Gershenzon, Shenghong Li, Ying Chang, Feng Chen
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Abstract

Ferns, known for their adaptability and widespread presence, form a diverse group of plants. However, the mechanisms underlying terpenoid production, which are often linked to plant adaptation, are not well understood in ferns. Here, we report that Dryopteris fragrans (D. fragans) produces diverse terpenoids in glandular trichomes (GTs) through the activities of microbial-type terpene synthases. Using microscopy methods, capitate GTs were found to occur on various organs throughout the development of D. fragrans. In D. fragrans leaves, 13 terpenoids, most being sesquiterpenoids, were identified. By comparing the terpenoid chemistry of intact leaves, GT-removed leaves, and isolated GTs, GTs were concluded to be the main site of terpenoid storage. Next, transcriptomes of D. fragrans leaves and GTs were created and mined for genes of the terpenoid biosynthetic pathway. Among them were nine putative full-length microbial terpene synthase-like (MTPSL) genes designated DfMTPSL1–9. Using in vitro enzyme assays, six of the nine DfMTPSLs were demonstrated to have sesquiterpene synthase activities. Of them, DfMTPSL1 catalyzes the formation of (−)-9-epi-presilphiperfolan-1-ol, the most abundant sesquiterpenoid in leaves. DfMTPS2 produces α-muurolene, another major sesquiterpenoid from D. fragrans. The catalytic activities of DfMTPSLs together with the GT-enriched expression of their respective genes support that GTs are also the main site of terpenoid biosynthesis in D. fragrans. Methyl jasmonate treatment induced the expression of DfMTPSL genes and the emission of terpenoid volatiles, suggesting that GT-produced terpenoids play a role in defense against biotic stresses in D. fragrans, similar to their counterparts in seed plants.

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蕨类植物以其适应性强和分布广泛而著称,是一个种类繁多的植物群。然而,萜类化合物的产生往往与植物的适应性有关,蕨类植物产生萜类化合物的机制却不甚明了。在这里,我们报告了香干蕨(D. fragans)通过微生物型萜烯合成酶的活性在腺毛(GTs)中产生多种萜类化合物。利用显微镜方法发现,头状毛状体(GTs)出现在香叶木(D. fragrans)各个器官的整个发育过程中。在 D. fragrans 的叶片中,发现了 13 种萜类化合物,其中大部分是倍半萜类化合物。通过比较完整叶片、去除GT的叶片和分离的GT的萜类化合物化学成分,得出结论:GT是萜类化合物的主要储存场所。接下来,研究人员创建了香叶和 GTs 的转录组,并对萜类化合物生物合成途径的基因进行了挖掘。其中有九个推测的全长类微生物萜烯合成酶(MTPSL)基因,命名为 DfMTPSL1-9。通过体外酶测定,证明这九个 DfMTPSL 中的六个具有倍半萜合成酶活性。其中,DfMTPSL1 催化叶片中含量最高的倍半萜类化合物 (-)-9-epi-presilphiperfolan-1-ol 的形成。DfMTPS2 生成α-木欧烯,这是香叶木果中另一种主要的倍半萜类化合物。DfMTPSLs 的催化活性及其各自基因在 GT 中的富集表达证明,GT 也是 D. fragrans 中萜类化合物生物合成的主要场所。茉莉酸甲酯处理诱导了 DfMTPSL 基因的表达和萜类挥发物的释放,表明 GT 产生的萜类化合物在 D. fragrans 中起到了抵御生物胁迫的作用,这与种子植物中的萜类化合物类似。
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来源期刊
The Plant Journal
The Plant Journal 生物-植物科学
CiteScore
13.10
自引率
4.20%
发文量
415
审稿时长
2.3 months
期刊介绍: Publishing the best original research papers in all key areas of modern plant biology from the world"s leading laboratories, The Plant Journal provides a dynamic forum for this ever growing international research community. Plant science research is now at the forefront of research in the biological sciences, with breakthroughs in our understanding of fundamental processes in plants matching those in other organisms. The impact of molecular genetics and the availability of model and crop species can be seen in all aspects of plant biology. For publication in The Plant Journal the research must provide a highly significant new contribution to our understanding of plants and be of general interest to the plant science community.
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