Systematic characterization of novel lncRNAs responding to phosphate starvation in Arabidopsis thaliana

Yuan, Jiapei; Zhang, Ye; Dong, Jinsong; Sun, Yuzhe; Lim, Boon Leong; Liu, Dong; Lu, Zhi John

doi:10.1186/s12864-016-2929-2

Cited by 88 publications

(81 citation statements)

References 88 publications

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“…In Arabidopsis thaliana, overexpression of lncRNA npc536 enhances tolerance to salt (Ben Amor et al, 2009). Moreover, genome-wide studies in A. thaliana have revealed hundreds of lncRNAs that respond to various external stimuli (Di et al, 2014;Yuan et al, 2016). Oryza sativa (rice) is an essential crop that grows in a wide range of environments characterized by various temperatures, salinity levels and soil/water conditions.…”

Section: Introductionmentioning

confidence: 99%

Stress‐responsive regulation of long non‐coding RNA polyadenylation in Oryza sativa

Yuan

Yang

et al. 2018

The Plant Journal

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Recently, long non-coding RNAs (lncRNAs) have been demonstrated to be involved in many biological processes of plants; however, a systematic study on transcriptional and, in particular, post-transcriptional regulation of stress-responsive lncRNAs in Oryza sativa (rice) is lacking. We sequenced three types of RNA libraries (poly(A)+, poly(A)- and nuclear RNAs) under four abiotic stresses (cold, heat, drought and salt). Based on an integrative bioinformatics approach and ~200 high-throughput data sets, ~170 of which have been published, we revealed over 7000 lncRNAs, nearly half of which were identified for the first time. Notably, we found that the majority of the ~500 poly(A) lncRNAs that were differentially expressed under stress were significantly downregulated, but approximately 25% were found to have upregulated non-poly(A) forms. Moreover, hundreds of lncRNAs with downregulated polyadenylation (DPA) tend to be highly conserved, show significant nuclear retention and are co-expressed with protein-coding genes that function under stress. Remarkably, these DPA lncRNAs are significantly enriched in quantitative trait loci (QTLs) for stress tolerance or development, suggesting their potential important roles in rice growth under various stresses. In particular, we observed substantially accumulated DPA lncRNAs in plants exposed to drought and salt, which is consistent with the severe reduction of RNA 3'-end processing factors under these conditions. Taken together, the results of this study reveal that polyadenylation and subcellular localization of many rice lncRNAs are likely to be regulated at the post-transcriptional level. Our findings strongly suggest that many upregulated/downregulated lncRNAs previously identified by traditional RNA-seq analyses need to be carefully reviewed to assess the influence of post-transcriptional modification.

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Section: Introductionmentioning

confidence: 99%

Stress‐responsive regulation of long non‐coding RNA polyadenylation in Oryza sativa

Yuan

Yang

et al. 2018

The Plant Journal

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“…In this study, by using strand specific RNA analysis on root tips, we succeeded in identifying thousands of different forms of lncRNAs: lincRNAs, NATs or antisense RNAs expressed from two Arabidopsis accessions, Col and L er . As previously shown in numerous studies, in comparison with mRNAs, lncRNAs observed here were expressed at low levels [62,63]. We opted to focus on root growth as it is a complex trait resulting of the expression of a large number of loci spread across the plant genome and is highly susceptible to the soil environment [64].…”

Section: Discussionmentioning

confidence: 96%

“…It acts as a target mimic for miR399, which regulates PHO2 mRNAs [81,82]. Moreover, Yuan et al [62] identified lncRNAs differentially expressed in root and shoot of plants grown in the presence or absence of Pi for 10 days. The authors suggested that a co-expression between lncRNAs and adjacent coding genes may be linked to a cis-regulation by lncRNAs of target genes involved in Pi starvation processes.…”

Section: Discussionmentioning

confidence: 99%

Two ecotype-related long non-coding RNAs in the environmental control of root growth

Blein¹,

Balzergue²,

Roulé³

et al. 2019

Preprint

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BackgroundRoot architecture varies widely between species and even between ecotypes of the same species despite the strong conservation of the protein-coding portion of their genomes. In contrast, non-coding RNAs evolved rapidly between ecotypes and may control their differential responses to the environment as several long non-coding RNAs (lncRNAs) can quantitatively regulate gene expression.ResultsRoots from Columbia (Col) and Landsbergerecta(Ler) ecotypes respond differently to phosphate starvation. We compared complete transcriptomes (mRNAs, lncRNAs and small RNAs) of root tips from these two ecotypes during early phosphate starvation. We identified thousands of new lncRNAs categorized as intergenic or antisense RNAs that were largely conserved at DNA level in these ecotypes. In contrast to coding genes, many lncRNAs were specifically transcribed in one ecotype and/or differentially expressed between ecotypes independently of the phosphate condition. These ecotype-related lncRNAs were characterized by analyzing their sequence variability among plants and their link with siRNAs. Our analysis identified 675 lncRNAs differentially expressed between the two ecotypes including specific antisense RNAs targeting key regulators of root growth responses. Mis-regulation of several intergenic lncRNAs showed that at least two ecotype-related lncRNAs regulate primary root growth in Col.ConclusionsThe in depth exploration of the non-coding transcriptome of two ecotypes identified thousands of new lncRNAs showing specific expression in root apexes. De-regulation of two ecotype-related lncRNAs revealed a new pathway involved in the regulation of primary root growth. The non-coding genome may reveal novel mechanisms involved in ecotype adaptation of roots to different soil environments.

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“…In plants, various biological processes, including flowering time, immunity, fertility, root development and photomorphogenesis, have been shown to be regulated by lncRNAs (Swiezewski et al ; Heo and Sung ; Ding et al ; Zhou et al ; Bardou et al ; Wang et al ; Kim and Sung ; Seo et al )_ENREF_18_ENREF_23. Increasing evidence also implicates lncRNAs in the regulation of Pi homeostasis (Franco‐Zorrilla et al ; Jabnoune et al ; Shah et al ; Cruz de Carvalho et al ; Xu et al ; Yuan et al ; Wang et al ).…”

Section: Introductionmentioning

confidence: 99%

Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency

Zhang

Zheng

Ham

et al. 2018

JIPB

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In response to phosphate (Pi) deficiency, it has been shown that micro-RNAs (miRNAs) and mRNAs are transported through the phloem for delivery to sink tissues. Growing evidence also indicates that long non-coding RNAs (lncRNAs) are critical regulators of Pi homeostasis in plants. However, whether lncRNAs are present in and move through the phloem, in response to Pi deficiency, remains to be established. Here, using cucumber as a model plant, we show that lncRNAs are enriched in the phloem translocation stream and respond, systemically, to an imposed Pi-stress. A well-known lncRNA, IPS1, the target mimic (TM) of miRNA399, accumulates to a high level in the phloem, but is not responsive to early Pi deficiency. An additional 24 miRNA TMs were also detected in the phloem translocation stream; among them miRNA171 TMs and miR166 TMs were induced in response to an imposed Pi stress. Grafting studies identified 22 lncRNAs which move systemically into developing leaves and root tips. A CU-rich PTB motif was further identified in these mobile lncRNAs. Our findings revealed that lncRNAs respond to Pi deficiency, non-cell-autonomously, and may act as systemic signaling agents to coordinate early Pi deficiency signaling, at the whole-plant level.

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Systematic characterization of novel lncRNAs responding to phosphate starvation in Arabidopsis thaliana

Cited by 88 publications

References 88 publications

Stress‐responsive regulation of long non‐coding RNA polyadenylation in Oryza sativa

Stress‐responsive regulation of long non‐coding RNA polyadenylation in Oryza sativa

Two ecotype-related long non-coding RNAs in the environmental control of root growth

Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency

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