Thieme Michael, Lanciano Sophie, Balzergue Sandrine, Daccord Nicolas, Mirouze Marie, Bucher Etienne
Botanical Institute, Zürich-Basel Plant Science Center, University of Basel, Hebelstrasse 1, 4056, Basel, Switzerland.
Institut de Recherche pour le Développement, UMR232 DIADE Diversité Adaptation et Développement des Plantes, Université Montpellier 2, Montpellier, France.
Genome Biol. 2017 Jul 7;18(1):134. doi: 10.1186/s13059-017-1265-4.
Retrotransposons play a central role in plant evolution and could be a powerful endogenous source of genetic and epigenetic variability for crop breeding. To ensure genome integrity several silencing mechanisms have evolved to repress retrotransposon mobility. Even though retrotransposons fully depend on transcriptional activity of the host RNA polymerase II (Pol II) for their mobility, it was so far unclear whether Pol II is directly involved in repressing their activity.
Here we show that plants defective in Pol II activity lose DNA methylation at repeat sequences and produce more extrachromosomal retrotransposon DNA upon stress in Arabidopsis and rice. We demonstrate that combined inhibition of both DNA methylation and Pol II activity leads to a strong stress-dependent mobilization of the heat responsive ONSEN retrotransposon in Arabidopsis seedlings. The progenies of these treated plants contain up to 75 new ONSEN insertions in their genome which are stably inherited over three generations of selfing. Repeated application of heat stress in progeny plants containing increased numbers of ONSEN copies does not result in increased activation of this transposon compared to control lines. Progenies with additional ONSEN copies show a broad panel of environment-dependent phenotypic diversity.
We demonstrate that Pol II acts at the root of transposon silencing. This is important because it suggests that Pol II can regulate the speed of plant evolution by fine-tuning the amplitude of transposon mobility. Our findings show that it is now possible to study induced transposon bursts in plants and unlock their use to induce epigenetic and genetic diversity for crop breeding.
逆转座子在植物进化中起着核心作用,并且可能成为作物育种中遗传和表观遗传变异的强大内源性来源。为确保基因组完整性,已经进化出几种沉默机制来抑制逆转座子的移动性。尽管逆转座子的移动性完全依赖于宿主RNA聚合酶II(Pol II)的转录活性,但到目前为止尚不清楚Pol II是否直接参与抑制它们的活性。
在这里我们表明,在拟南芥和水稻中,Pol II活性有缺陷的植物在重复序列处失去DNA甲基化,并在受到胁迫时产生更多的染色体外逆转座子DNA。我们证明,DNA甲基化和Pol II活性的联合抑制导致拟南芥幼苗中热响应性ONSET逆转座子强烈的胁迫依赖性动员。这些处理过的植物的后代在其基因组中含有多达75个新的ONSET插入,这些插入在三代自交中稳定遗传。与对照品系相比,在含有增加数量的ONSET拷贝的后代植物中重复施加热胁迫不会导致该转座子的激活增加。具有额外ONSET拷贝的后代表现出广泛的环境依赖性表型多样性。
我们证明Pol II在转座子沉默的根源起作用。这很重要,因为这表明Pol II可以通过微调转座子移动性的幅度来调节植物进化的速度。我们的研究结果表明,现在有可能研究植物中诱导的转座子爆发,并开启它们在诱导作物育种中的表观遗传和遗传多样性方面的应用。