Role of lncRNAs in cis- and trans-regulatory responses to salt in Populus trichocarpa

Role of lncRNAs in cis- and trans-regulatory responses to salt in Populus trichocarpa
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lncRNAs在毛果杨对盐的顺式和反式调节反应中的作用

DOI:
10.1111/tpj.15714
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发表时间:
2022
期刊:
影响因子:
7.2
通讯作者:
Shenkui Liu
Shenkui Liu
中科院分区:
生物学1区
文献类型:
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作者:
Xiaoxue Ye;Shuo Wang;Xijuan Zhao;Ni Gao;Yao Wang;Yanmei Yang;Ernest Wu;Cheng Jiang;Yuxiang Cheng;Wenwu Wu;Shenkui Liu

文献摘要

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长非编码RNA(LncRNAs)是多种生物过程中的多功能调节因子。然而,关于它们在盐胁迫下对基因表达的顺式和反式调节作用,人们知之甚少。利用毛白杨叶片、茎和根的27个RNA-SEQ数据集,我们鉴定了2988个高可信的LncRNAs,其中包括1183个盐诱导的差异表达的LncRNAs。其中,301个lncRNA具有积极影响其邻近基因的潜力,主要是以Acis调控的方式,而不是通过共转录。此外,共表达网络确定了6个显著的盐相关模块,共5639个基因,包括426个lncRNA,并且在这些lncRNA序列中,DNA/RNA结合基序丰富。这表明,lncRNAs可能以反式调节的方式参与了盐相关模块的远程基因表达。此外,我们还发现了30个可能同时调节盐响应同源基因的lncRNAs,并选择在长期盐胁迫下显著诱导的Ptlinc-NAC72来验证其对同源基因PtNAC72.A和PtNAC72.B(PtNAC72.A/B)的表达和功能的调控。Ptlinc-NAC72的瞬时转化和Ptlinc-NAC72和PtNAC72.A/B启动子的双荧光素酶分析证实,Ptlinc-NAC72可以直接上调PtNAC72.A/B的表达,存在/缺失分析进一步表明,这种调控可能是通过Ptlinc-NAC72识别PtNAC72.A/B5‘非翻译区的串联元件(GAAAAA)介导的。最后,Ptlinc-NAC72的过表达产生了盐胁迫下的敏感表型。总之,我们的结果揭示了lncRNAs对植物群体基因表达的顺式和反式调节,并提供了一个长期盐诱导的Ptlinc-NAC72的例子,可以通过赋予植物对盐胁迫的弹性来降低生长成本。
Long non‐coding RNAs (lncRNAs) are emerging as versatile regulators in diverse biological processes. However, little is known about theircis‐ andtrans‐regulatory contributions in gene expression under salt stress. Using 27 RNA‐seq data sets fromPopulus trichocarpaleaves, stems and roots, we identified 2988 high‐confidence lncRNAs, including 1183 salt‐induced differentially expressed lncRNAs. Among them, 301 lncRNAs have potential for positively affecting their neighboring genes, predominantly in acis‐regulatory manner rather than by co‐transcription. Additionally, a co‐expression network identified six striking salt‐associated modules with a total of 5639 genes, including 426 lncRNAs, and in these lncRNA sequences, the DNA/RNA binding motifs are enriched. This suggests that lncRNAs might contribute to distant gene expression of the salt‐associated modules in atrans‐regulatory manner. Moreover, we found 30 lncRNAs that have potential to simultaneouslycis‐andtrans‐regulate salt‐responsive homologous genes, andPtlinc‐NAC72, significantly induced under long‐term salt stress, was selected for validating its regulation of the expression and functional roles of the homologsPtNAC72.AandPtNAC72.B(PtNAC72.A/B). The transient transformation ofPtlinc‐NAC72and a dual‐luciferase assay ofPtlinc‐NAC72andPtNAC72.A/Bpromoters confirmed thatPtlinc‐NAC72can directly upregulatePtNAC72.A/Bexpression, and a presence/absence assay was further conducted to show that the regulation is probably mediated byPtlinc‐NAC72recognizing the tandem elements (GAAAAA) in thePtNAC72.A/B5′ untranslated region (5′‐UTR). Finally, the overexpression ofPtlinc‐NAC72produces a hypersensitive phenotype under salt stress. Altogether, our results shed light on thecis‐ andtrans‐regulation of gene expression by lncRNAs inPopulusand provides an example of long‐term salt‐inducedPtlinc‐NAC72that could be used to mitigate growth costs by conferring plant resilience to salt stress.