An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress

An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress
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DOI:
10.1038/nature09861
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发表时间:
2011-04-07
期刊:
影响因子:
64.8
通讯作者:
Paszkowski, Jerzy
Paszkowski, Jerzy
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Ito, Hidetaka;Gaubert, Herve;Paszkowski, Jerzy

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真核基因组在很大程度上由逆转录转座子组成,逆转录转座子被宿主表观遗传机制抑制,防止其不受控制的繁殖(1,2)。然而,尚不清楚这是如何实现的。在这里,我们表明,在拟南芥幼苗受到热应激,copia型反转录转座子命名为ONSEN(日本'温泉')不仅成为转录活性,但也合成染色体外DNA拷贝。在小干扰RNA(siRNA)生物合成受损的突变体中,热诱导的ONSEN积累受到刺激;然而,没有证据表明营养组织中发生了转座。在胁迫后,ONSEN转录物和染色体外DNA都逐渐衰减,并且在20-30天后不再检测到。令人惊讶的是,在siRNA缺陷的胁迫植物的后代中观察到高频率的新ONSEN插入。插入模式显示,这种跨代逆转录转座发生在花发育和配子发生之前。因此,在具有受损siRNA生物发生的植物中,胁迫记忆在整个发育过程中得以维持,从而引发ONSEN在生殖器官分化期间转座。在受到胁迫的野生型植物的后代或非胁迫突变对照中没有观察到逆转录转座,这表明SiRNA途径在限制环境胁迫引发的逆转录转座中发挥着至关重要的作用。最后,我们发现ONSEN插入中的天然和实验诱导的变体赋予附近基因热响应性,因此流动性爆发可能会产生新的应激反应调控基因网络。
Eukaryotic genomes consist to a significant extent of retrotransposons that are suppressed by host epigenetic mechanisms, preventing their uncontrolled propagation(1,2). However, it is not clear how this is achieved. Here we show that in Arabidopsis seedlings subjected to heat stress, a copia-type retrotransposon named ONSEN (Japanese 'hot spring') not only became transcriptionally active but also synthesized extrachromosomal DNA copies. Heat-induced ONSEN accumulation was stimulated in mutants impaired in the biogenesis of small interfering RNAs (siRNAs); however, there was no evidence of transposition occurring in vegetative tissues. After stress, both ONSEN transcripts and extrachromosomal DNA gradually decayed and were no longer detected after 20-30 days. Surprisingly, a high frequency of new ONSEN insertions was observed in the progeny of stressed plants deficient in siRNAs. Insertion patterns revealed that this transgenerational retrotransposition occurred during flower development and before gametogenesis. Therefore in plants with compromised siRNA biogenesis, memory of stress was maintained throughout development, priming ONSEN to transpose during differentiation of generative organs. Retrotransposition was not observed in the progeny of wild-type plants subjected to stress or in non-stressed mutant controls, pointing to a crucial role of the siRNA pathway in restricting retrotransposition triggered by environmental stress. Finally, we found that natural and experimentally induced variants in ONSEN insertions confer heat responsiveness to nearby genes, and therefore mobility bursts may generate novel, stress-responsive regulatory gene networks.