Pavan Flavia, Favory Jacinthe Azevedo, Lacoste Eléanore, Beaumont Chloé, Louis Firas, Blassiau Christelle, Cruaud Corinne, Labadie Karine, Gallina Sophie, Genete Mathieu, Kumar Vinod, Kramer Ute, Batista Rita A, Patiou Claire, Debacker Laurence, Ponitzki Chloé, Houzé Esther, Durand Eléonore, Aury Jean-Marc, Castric Vincent, Legrand Sylvain
Univ. Lille, CNRS, UMR 8198, Evo-Eco-Paleo, Lille F-59000, France.
CNRS, Laboratoire Génome et Développement des Plantes, UMR 5096, Perpignan 66860, France.
Plant Cell. 2025 Jul 1;37(7). doi: 10.1093/plcell/koaf168.
MicroRNAs (miRNAs) are a class of small non-coding RNAs that play important regulatory roles in plant genomes. While some miRNA genes are deeply conserved, the majority appear to be species-specific, raising the question of how they emerge and integrate into cellular regulatory networks. To address this question, we first performed a detailed annotation of miRNA genes in the closely related Arabidopsis halleri and A. lyrata, then evaluated their phylogenetic conservation across 87 plant species. We then characterized the process by which newly emerged miRNA genes progressively acquire the properties of "canonical" miRNA genes, in terms of size and stability of the hairpin precursor, loading of their cleavage products into Argonaute proteins, and potential to regulate downstream target genes. Analysis of nucleotide polymorphism distribution along the hairpin sequence (stem, mature miRNA, terminal loop) revealed that the selective constraints on recently emerged miRNA genes were initially weak, gradually increasing toward evolutionarily conserved miRNA genes. Our results illustrate the rapid birth-and-death of miRNA genes in plant genomes, and provide a detailed picture of the evolutionary progression toward canonical miRNAs by which a small fraction of de novo formed miRNA genes eventually integrate into "core" biological processes.
微小RNA（miRNA）是一类小的非编码RNA，在植物基因组中发挥重要的调控作用。虽然一些miRNA基因高度保守，但大多数似乎具有物种特异性，这就引发了它们如何出现并融入细胞调控网络的问题。为了解决这个问题，我们首先对近缘物种琴叶拟南芥和琴叶鼠耳芥中的miRNA基因进行了详细注释，然后评估了它们在87种植物物种中的系统发育保守性。接着，我们从发夹前体的大小和稳定性、其切割产物加载到AGO蛋白中的情况以及调控下游靶基因的潜力等方面，对新出现的miRNA基因逐渐获得“典型”miRNA基因特性的过程进行了表征。沿着发夹序列（茎、成熟miRNA、末端环）的核苷酸多态性分布分析表明，对最近出现的miRNA基因的选择限制最初较弱，朝着进化上保守的miRNA基因逐渐增强。我们的结果说明了植物基因组中miRNA基因的快速生灭，并提供了一幅向典型miRNA进化进程的详细图景，通过这一过程，一小部分新形成的miRNA基因最终融入“核心”生物学过程。
