Multiple RNA recognition patterns during microRNA biogenesis in plants

Bologna, Nicolas Gerardo; Schapire, Arnaldo L.; Zhai, Jixian; Chorostecki, Uciel; Boisbouvier, Jérôme; Meyers, Blake C.; Palatnik, Javier F.

doi:10.1101/gr.153387.112

Cited by 121 publications

(201 citation statements)

References 65 publications

(120 reference statements)

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“…Several lines of evidence indicate that Iw1 and Iw2 are evolutionarily young MIRNA genes that arose by inverted duplication of their target gene (39,49). First, the foldback region of Iw1 has extended similarity (>80%) with the target W1-COE beyond that of the miRW1 region.…”

Section: Discussionmentioning

confidence: 99%

Long noncoding miRNA gene represses wheat β-diketone waxes

Huang

Feurtado

Smith

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The cuticle of terrestrial plants functions as a protective barrier against many biotic and abiotic stresses. In wheat and other Triticeae, β-diketone waxes are major components of the epicuticular layer leading to the bluish-white glaucous trait in reproductive-age plants. Glaucousness in durum wheat is controlled by a metabolic gene cluster at the WAX1 (W1) locus and a dominant suppressor INHIBITOR of WAX1 (Iw1) on chromosome 2B. The wheat D subgenome from progenitor Aegilops tauschii contains W2 and Iw2 paralogs on chromosome 2D. Here we identify the Iw1 gene from durum wheat and demonstrate the unique regulatory mechanism by which Iw1 acts to suppress a carboxylesterase-like protein gene, W1-COE, within the W1 multigene locus. Iw1 is a long noncoding RNA (lncRNA) containing an inverted repeat (IR) with >80% identity to W1-COE. The Iw1 transcript forms a miRNA precursor-like long hairpin producing a 21-nt predominant miRNA, miRW1, and smaller numbers of related sRNAs associated with the nonglaucous phenotype. When Iw1 was introduced into glaucous bread wheat, miRW1 accumulated, W1-COE and its paralog W2-COE were down-regulated, and the phenotype was nonglaucous and β-diketone-depleted. The IR region of Iw1 has >94% identity to an IR region on chromosome 2 in Ae. tauschii that also produces miRW1 and lies within the marker-based location of Iw2. We propose the Iw loci arose from an inverted duplication of W1-COE and/or W2-COE in ancestral wheat to form evolutionarily young miRNA genes that act to repress the glaucous trait.glaucous | inhibitor of wax | small RNA | long noncoding RNA | WAX1 P lant epicuticular waxes deposited on the outer surface of the plant cuticle produce a water-resistant layer that serves to reduce nonstomatal water loss and mitigate the effects of heat and UV radiation as well as pathogen and insect attacks (1). Grasses in the Triticeae tribe, subfamily Pooideae, which include the cultivated species barley (Hordeum vulgare; 2n = 2x = 14), rye (Secale cereale, 2n = 2x = 14), durum wheat (Triticum durum; 2n = 4x = 28, AABB), and bread wheat (Triticum aestivum; 2n = 6x = 42, AABBDD), have two predominant pathways for wax production: (i) an alcohol-and alkane-rich wax pathway and (ii) a pathway leading to β-diketones and derivatives including hydroxy-β-diketones (2). The alcohol and alkane waxes are prevalent in earlier development and on leaves, whereas β-diketones dominate during the reproductive phase, particularly on leaf sheaths and flower heads (3, 4). β-Diketone wax is predominantly hentriacontane-14, 16-dione, which consists of a 31-carbon chain with carbonyl groups at C 14 and C 16 . In durum wheat, about 20% of the β-diketone is hydroxylated to form 25-hydroxy-β-diketone, whereas in bread wheat hydroxylation is at C 8 or C 9 (5). β-Diketone wax deposition manifests visibly as glaucousness, a bluish-white coloration on stems, leaves, and flower heads. However, the relationship between a glaucous appearance and the total amount of cuticular wax can be inconsistent, especially during t...

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Section: Discussionmentioning

confidence: 99%

Long noncoding miRNA gene represses wheat β-diketone waxes

Huang

Feurtado

Smith

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In particular, we observe that 5' and especially 3' positional variants of miRNAs and miRNA*s are quite common in sRNA-seq data. These variants likely result from a combination of DCL cleavage at different positions (including DCL imprecision, perhaps a characteristic of recently-evolved miRNAs (Bologna et al, 2013b)), post-dicing modifications of the 3' end (Zhai et al, 2013), and sample degradation. Thus the revised calculation of precision includes the counts of the exact mature miRNA and its corresponding exact miRNA*, as well as all one-nucleotide variants thereof.…”

Section: Update On Criteria For Plant Mirna Annotations: the Urgent Nmentioning

confidence: 99%

“…However, our own research experiences in the intervening time suggest the following improvements (summarized in Table 1): 1: The hairpin of a miRNA precursor is a defining characteristic and a component of all reliable miRNAidentification algorithms. Using conserved miRNAs as exemplars, there are key features of the foldback or hairpin that are important for Dicer recognition and consistent processing (Cuperus et al, 2011;Bologna et al, 2013b;2013a;Chorostecki et al, 2017): (i) typically a single miRNA:miRNA* duplex (thus far not more than three duplexes, a number observed in miR319/159); (ii) the region of this foldback that gives rise to the miRNA duplex should not contain secondary stems or large internal loops (larger than five nucleotides) that interrupt the miRNA:miRNA* duplex; (iii) while miRNA foldbacks of plants are often longer than those of animals, most foldbacks are just a few hundred nucleotides. These structural characteristics govern processing including the base-to-loop versus loop-to-base direction of duplex production.…”

Section: Update On Criteria For Plant Mirna Annotations: the Urgent Nmentioning

confidence: 99%

Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data

2018

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MicroRNAs (miRNAs) are ~21 nucleotide-long regulatory RNAs that arise from endonucleolytic processing of hairpin precursors. Many function as essential post-transcriptional regulators of target mRNAs and long non-coding RNAs. Alongside miRNAs, plants also produce large numbers of short interfering RNAs (siRNAs), which are distinguished from miRNAs primarily by their biogenesis (typically processed from long double-stranded RNA instead of single-stranded hairpins) and functions (typically via roles in transcriptional regulation instead of posttranscriptional regulation). Next-generation DNA sequencing methods have yielded extensive datasets of plant small RNAs, resulting in many miRNA annotations. However, it has become clear that many miRNA annotations are questionable. The sheer number of endogenous siRNAs compared to miRNAs has been a major factor in the erroneous annotation of siRNAs as miRNAs. Here, we provide updated criteria for the confident annotation of plant miRNAs, suitable for the era of "big data" from DNA sequencing. The updated criteria emphasize replication, the minimization of false positives, and they require next-generation sequencing of small RNAs. We argue that improved annotation systems are needed for miRNAs and all other classes of plant small RNAs. Finally, to illustrate the complexities of miRNA and siRNA annotation, we review the evolution and functions of miRNAs and siRNAs in plants.

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“…PARE and degradome sequencing have been widely applied in the identification of small RNA-guided cleavage sites in various plant species (Addo-Quaye et al, 2008;German et al, 2008;Zhou et al, 2010;Shamimuzzaman and Vodkin, 2012;Zhao et al, 2012;Li et al, 2013a). Specific PARE has been developed for the study of plant miRNA processing by specifically amplifying miRNA processing intermediates (Bologna et al, 2013). Although these approaches have been used to profile mRNA degradation intermediates in mutants impaired in XRNs or proteins with endonucleolytic activity (German et al, 2008;Harigaya and Parker, 2012;Schmidt et al, 2015), the interpretations of some results remain challenging because the complexity of the RNA degradome is currently still largely uncharacterized.…”

Section: Introductionmentioning

confidence: 99%

Global Analysis of Truncated RNA Ends Reveals New Insights into Ribosome Stalling in Plants

et al. 2016

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High-throughput approaches for profiling the 59 ends of RNA degradation intermediates on a genome-wide scale are frequently applied to analyze and validate cleavage sites guided by microRNAs (miRNAs). However, the complexity of the RNA degradome other than miRNA targets is currently largely uncharacterized, and this limits the application of RNA degradome studies. We conducted a global analysis of 59-truncated mRNA ends that mapped to coding sequences (CDSs) of Arabidopsis thaliana, rice (Oryza sativa), and soybean (Glycine max). Based on this analysis, we provide multiple lines of evidence to show that the plant RNA degradome contains in vivo ribosome-protected mRNA fragments. We observed a 3-nucleotide periodicity in the position of free 59 RNA ends and a bias toward the translational frame. By examining conserved peptide upstream open reading frames (uORFs) of Arabidopsis and rice, we found a predominance of 59 termini of RNA degradation intermediates that were separated by a length equal to a ribosome-protected mRNA fragment. Through the analysis of RNA degradome data, we discovered uORFs and CDS regions potentially associated with stacked ribosomes in Arabidopsis. Furthermore, our analysis of RNA degradome data suggested that the binding of Arabidopsis ARGONAUTE7 to a noncleavable target site of miR390 might directly hinder ribosome movement. This work demonstrates an alternative use of RNA degradome data in the study of ribosome stalling.

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Multiple RNA recognition patterns during microRNA biogenesis in plants

Cited by 121 publications

References 65 publications

Long noncoding miRNA gene represses wheat β-diketone waxes

Long noncoding miRNA gene represses wheat β-diketone waxes

Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data

Global Analysis of Truncated RNA Ends Reveals New Insights into Ribosome Stalling in Plants

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