Ecology and Evolution, Research School of Biology, The Australian National University, Acton, Australia.
Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI, USA.
Ann Bot. 2019 Jun 24;123(6):1053-1066. doi: 10.1093/aob/mcz013.
The processes of gene duplication, followed by divergence and selection, probably underpin the evolution of floral volatiles crucial to plant-insect interactions. The Australian sexually deceptive Chiloglottis orchids use a class of 2,5-dialkylcyclohexan-1,3-dione volatiles or 'chiloglottones' to attract specific male wasp pollinators. Here, we explore the expression and evolution of fatty acid pathway genes implicated in chiloglottone biosynthesis.
Both Chiloglottis seminuda and C. trapeziformis produce chiloglottone 1, but only the phylogenetically distinct C. seminuda produces this volatile from both the labellum callus and glandular sepal tips. Transcriptome sequencing and tissue-specific contrasts of the active and non-active floral tissues was performed. The effects of the fatty acid synthase inhibitor cerulenin on chiloglottone production were tested. Patterns of selection and gene evolution were investigated for fatty acid pathway genes.
Tissue-specific differential expression of fatty acid pathway transcripts was evident between active and non-active floral tissues. Cerulenin significantly inhibits chiloglottone 1 production in the active tissues of C. seminuda. Phylogenetic analysis of plant β-ketoacyl synthase I (KASI), a protein involved in fatty acid biosynthesis, revealed two distinct clades, one of which is unique to the Orchidaceae (KASI-2B). Selection analysis indicated a strong signal of positive selection at the split of KASI-2B followed by relaxed purifying selection in the Chiloglottis clade.
By capitalizing on a phylogenetically distinct Chiloglottis from earlier studies, we show that the transcriptional and biochemical dynamics linked to chiloglottone biosynthesis in active tissues are conserved across Chiloglottis. A combination of tissue-specific expression and relaxed purifying selection operating at specific fatty acid pathway genes may hold the key to the evolution of chiloglottones.
基因复制、分歧和选择的过程可能是植物与昆虫相互作用中关键的花挥发性物质进化的基础。澳大利亚有性欺骗兰花 Chiloglottis 使用一类 2,5-二烷基环己烷-1,3-二酮挥发性物质或“chiloglottones”来吸引特定的雄性黄蜂传粉者。在这里,我们探索了与 chiloglottone 生物合成相关的脂肪酸途径基因的表达和进化。
Chiloglottis seminuda 和 C. trapeziformis 都产生 chiloglottone 1,但只有在系统发育上不同的 C. seminuda 从 labellum 愈伤组织和腺状萼片尖端产生这种挥发性物质。进行了转录组测序和活跃和非活跃花组织的组织特异性对比。测试了脂肪酸合酶抑制剂 cerulenin 对 chiloglottone 产生的影响。研究了脂肪酸途径基因的选择模式和基因进化。
活跃和非活跃花组织之间的脂肪酸途径转录物的组织特异性差异表达明显。Cerulenin 显著抑制 C. seminuda 活跃组织中 chiloglottone 1 的产生。参与脂肪酸生物合成的植物β-酮酰基合酶 I (KASI)的系统发育分析显示出两个不同的分支,其中一个分支是兰花独有的 (KASI-2B)。选择分析表明,在 KASI-2B 分裂后,存在强烈的正选择信号,随后在 Chiloglottis 分支中出现了放松的纯化选择。
通过利用早期研究中具有系统发育差异的 Chiloglottis,我们表明活跃组织中与 chiloglottone 生物合成相关的转录和生化动态在 Chiloglottis 中是保守的。特定脂肪酸途径基因的组织特异性表达和放松的纯化选择的结合可能是 chiloglottones 进化的关键。