Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in Arabidopsis

Chromosome dosage has substantial effects on reproductive isolation (生殖隔离) and speciation in both plants and animals, but the underlying mechanisms are largely obscure (模糊的). Transposable elements in animals can regulate hybridity (杂合) through maternal (母本的) small RNA, whereas small RNAs in plants have been postulated (假定) to regulate dosage response via neighboring imprinted genes (印迹基因). Here we show that a highly conserved microRNA in plants, miR845, targets the tRNAMet primer-binding site (PBS) of long terminal repeat (LTR) retrotransposons in Arabidopsis pollen, and triggers the accumulation of 21–22-nucleotide (nt) small RNAs in a dose-dependent fashion via RNA polymerase IV. We show that these epigenetically activated small interfering RNAs (easiRNAs) mediate hybridization barriers (杂交障碍) between diploid seed parents and tetraploid pollen parents (the ‘triploid block’), and that natural variation for miR845 may account for ‘endosperm balance’ allowing the formation of triploid seeds. Targeting of the PBS with small RNA is a common mechanism for transposon control in mammals and plants, and provides a uniquely sensitive means to monitor chromosome dosage and imprinting in the developing seed.

染色体剂量在动植物的生殖隔离和物种形成中都起到了非常重要的作用，但潜在的机制还模糊不清。转座元件在动物中可以通过母本的小RNA调控杂合，而植物中的小RNA被认为通过邻近的印迹基因调控剂量响应。本文鉴定了一个在植物中高度保守的miRNA，即miR845在拟南芥花粉中靶向长末端（LTR）逆转座子的引物结合位点（PBS）tRNAMet，并且会通过RNA聚合酶IV以剂量依赖性的方式诱导21–22个核酸的小RNA积累。作者表明这些表观激活的小干扰RNA（easiRNA）会介导二倍体种子亲本和四倍体花粉亲本之间的杂交障碍，即被称为三倍体障碍，另外，miR845的天然变异是导致胚乳平衡形成三倍体种子的主要原因。小RNA靶向PBS是动植物转座子调控共同的机制，为在发育中的种子中进行染色体剂量和印迹修饰提供了独特的灵敏方式。

通讯：Robert A. Martienssen (https://www.cshl.edu/research/faculty-staff/rob-martienssen/)

研究方向：染色质上的化学修饰对基因表达的影响，即表观组，以及模式植物拟南芥和模式物种酵母中小RNA对于表观的调控

doi: 10.1038/s41588-017-0032-5

Published online: 15 January, 2018

Paternal easiRNAs regulate parental genome dosage in Arabidopsis

The regulation of parental genome dosage is of fundamental importance in animals and plants, as exemplified by X-chromosome inactivation and dosage compensation (剂量补偿). The ‘triploid block’ is a classic example of dosage regulation in plants that establishes a reproductive barrier (生殖障碍) between species differing in chromosome number. This barrier acts in the embryo-nourishing endosperm tissue and induces the abortion (流产) of hybrid seeds through a yet unknown mechanism. Here we show that depletion (消耗) of paternal epigenetically activated small interfering RNAs (easiRNAs) bypasses (避开) the triploid block in response to increased paternal ploidy in Arabidopsis thaliana. Paternal loss of the plant-specific RNA polymerase IV suppressed easiRNA formation and rescued triploid seeds by restoring small-RNA-directed DNA methylation at transposable elements (TEs), correlating with reduced expression of paternally expressed imprinted genes (PEGs). Our data suggest that easiRNAs form a quantitative signal for paternal chromosome number and that their balanced dosage is required for post-fertilization genome stability and seed viability.

亲本基因组剂量的调控是动植物研究中的基础，正如X染色体失活与剂量补偿。三倍体障碍是植物中剂量调控最为经典的案例，该机制在含有不同染色体数量的物种之间建立起了生殖障碍。这个障碍作用于给胚供给营养的胚乳组织，通过一个未知的机制诱导杂交种子的畸形和夭折。本文显示拟南芥中父本表观激活的小干扰RNA（easiRNA）的消耗会响应于增加的父本倍性避开三倍体障碍。父本丢失植物特异的RNA聚合酶IV会抑制easiRNA的形成，并会通过恢复在转座元件上小RNA定向的DNA甲基化拯救三倍体种子，而这与父本表达的印迹基因的减少相关。本文的结果显示easiRNAs会形成一个父本染色体数量的量化信号，并且其剂量的平衡对于受精后基因组的稳定及种子的活力都是必需的。

通讯：Claudia Köhler (http://kohlerlab.se/people/claudia-kohler/)

个人简介：1999年，德国弗莱堡大学，植物细胞生物学博士；1999-2000年，德国弗莱堡大学，植物细胞生物学博士后；2000-2003年，瑞士苏黎世大学，植物发育遗传学博士后；2003-2005年，瑞士苏黎世大学，植物发育遗传学助理教授；2005-2010年，瑞士苏黎世联邦理工学院，植物发育遗传学助理教授；2010-至今，瑞典农业科学大学，植物分子细胞生物学教授。

doi: 10.1038/s41588-017-0033-4