RNA degradomes reveal substrates and importance for dark and nitrogen stress responses of Arabidopsis XRN4

RNA degradomes reveal substrates and importance for dark and nitrogen stress responses of Arabidopsis XRN4
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DOI:
10.1093/nar/gkz712
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发表时间:
2019-09-26
影响因子:
14.9
通讯作者:
Green, Pamela J.
Green, Pamela J.
中科院分区:
生物学2区
文献类型:
--
作者:
Nagarajan, Vinay K.;Kukulich, Patrick M.;Green, Pamela J.

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XRN4是酵母和后生动物XRN1的植物细胞质同源物,可催化5'端无帽mrna的外核糖核酸降解。大多数细胞质XRN底物的研究都集中在聚腺苷化转录物上,尽管许多底物可能首先是死基化的。在这里,我们报告了XRN4底物在多聚腺苷化和非多聚腺苷化RNA中的全球研究,以更好地了解该酶在拟南芥中的影响。RNA降解分析表明,xrn4突变体比那些聚腺苷化的突变体过度积累了更多的去头死烯化中间体。在这些5'端恰好位于帽位的XRN4底物中,与光合作用、氮响应和生长素响应相关的底物富集。此外,在补氮过程中,发现xrn4在暗胁迫响应和侧根生长中存在缺陷,表明这两个过程都需要xrn4。XRN4也参与无义介导的衰变(NMD),尽管在植物中缺乏后生动物核糖核酸内切酶SMG6,但XRN4积累了选定的NMD靶点的3'片段。除了证明XRN4在多种衰变途径中起主要作用外,本研究还发现了该酶的有趣的分子影响,包括那些导致mRNA衰变的新见解以及在整个植物水平上发现功能贡献的影响。
XRN4, the plant cytoplasmic homolog of yeast and metazoan XRN1, catalyzes exoribonucleolytic degradation of uncapped mRNAs from the 5' end. Most studies of cytoplasmic XRN substrates have focused on polyadenylated transcripts, although many substrates are likely first deadenylated. Here, we report the global investigation of XRN4 substrates in both polyadenylated and nonpolyadenylated RNA to better understand the impact of the enzyme in Arabidopsis. RNA degradome analysis demonstrated that xrn4 mutants overaccumulate many more decapped deadenylated intermediates than those that are polyadenylated. Among these XRN4 substrates that have 5' ends precisely at cap sites, those associated with photosynthesis, nitrogen responses and auxin responses were enriched. Moreover, xrn4 was found to be defective in the dark stress response and lateral root growth during N resupply, demonstrating that XRN4 is required during both processes. XRN4 also contributes to nonsense-mediated decay (NMD) and xrn4 accumulates 3' fragments of select NMD targets, despite the lack of the metazoan endoribonuclease SMG6 in plants. Beyond demonstrating that XRN4 is a major player in multiple decay pathways, this study identified intriguing molecular impacts of the enzyme, including those that led to new insights about mRNA decay and discovery of functional contributions at the whole-plant level.