a Institute of Medicinal Plant Development , Chinese Academy of Medical Sciences & Peking Union Medical College , Beijing , China.
RNA Biol. 2019 Jun;16(6):846-859. doi: 10.1080/15476286.2019.1593744. Epub 2019 Mar 30.
MIRNA (MIR) gene origin and early evolutionary processes, such as hairpin precursor sequence origination, promoter activity acquirement and the sequence of these two processes, are fundamental and fascinating subjects. Three models, including inverted gene duplication, spontaneous evolution and transposon transposition, have been proposed for de novo origination of hairpin precursor sequence. However, these models still open to discussion. In addition, de novo origination of MIR gene promoters has not been well investigated. Here, I systematically investigated the origin of evolutionarily young polyphenol oxidase gene (PPO)-targeting MIRs, including MIR1444, MIR058 and MIR12112, and a genomic region termed AasPPO-as-hp, which contained a hairpin-forming sequence. I found that MIR058 precursors and the hairpin-forming sequence of AasPPO-as-hp originated in an ancient PPO gene through forming short inverted repeats. Palindromic-like sequences and imperfect inverted repeats in the ancient PPO gene contributed to initiate the generation of short inverted repeats probably by causing errors during DNA duplication. Analysis of MIR058 and AasPPO-as-hp promoters showed that they originated in the 3'-flanking region of the ancient PPO gene. Promoter activities were gained by insertion of a CAAT-box and multiple-copper-response element (CuRE)-containing miniature inverted-repeat transposable element (MITE) in the upstream of AT-rich TATA-box-like sequence. Gain of promoter activities occurred before hairpin-forming sequence origination. Sequence comparison of MIR1444, MIR058 and MIR12112 promoters showed frequent birth and death of CuREs, indicating copper could be vital for the origination and evolution of PPO-targeting MIRs. Based on the evidence obtained, a novel model for plant MIR origination and evolution is proposed.
miRNA (miR) 基因的起源和早期进化过程，如发夹前体序列的起源、启动子活性的获得以及这两个过程的序列，是基础和迷人的课题。新生成发夹前体序列的过程中，提出了三个模型，包括反向基因复制、自发进化和转座子转位。然而，这些模型仍然存在争议。此外，miR 基因启动子的新生成起源尚未得到很好的研究。在这里，我系统地研究了进化上年轻的多酚氧化酶基因（PPO）靶向 miR 的起源，包括 miR1444、miR058 和 miR12112，以及一个被称为 AasPPO-as-hp 的基因组区域，该区域包含一个发夹形成序列。我发现 miR058 前体和 AasPPO-as-hp 的发夹形成序列通过形成短的反向重复起源于古老的 PPO 基因。古老的 PPO 基因中的回文样序列和不完全反向重复序列可能通过在 DNA 复制过程中引起错误，有助于启动短反向重复序列的生成。对 miR058 和 AasPPO-as-hp 启动子的分析表明，它们起源于古老 PPO 基因的 3' 侧翼区。通过在富含 A/T 的 TATA 盒样序列上游插入 CAAT 盒和多个含铜反应元件（CuRE）的微型反转录转座元件（MITE），获得了启动子活性。启动子活性的获得发生在发夹形成序列起源之前。对 miR1444、miR058 和 miR12112 启动子序列的比较表明，CuRE 频繁出现和消失，表明铜对 PPO 靶向 miR 的起源和进化至关重要。基于所获得的证据，提出了一个新的植物 miR 起源和进化模型。
