Plant MicroRNAs Display Differential 3' Truncation and Tailing Modifications That Are ARGONAUTE1 Dependent and Conserved Across Species

Zhai, Jixian; Zhao, Yuanyuan; Simon, Stacey A.; Huang, Sheng; Petsch, Katherine; Arikit, Siwaret; Pillay, Manoj; Ji, Lijuan; Xie, Meng; Cao, Xiaofeng; Yu, Bin; Timmermans, Marja C.P.; Yang, Bing; Meyers, Blake C.

doi:10.1105/tpc.113.114603

Cited by 91 publications

(120 citation statements)

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“…Consistent with this notion, miRNA uridylation is blocked when AGO1 function is impaired in hen1 (Fig. 5A) (32), and extensive complementarity between targets and miRNAs triggers miRNA tailing in animals (34). However, the majority of miRNAs are normally methylated in plants, which prevents HESO1 function and, therefore, maintains the recycling of the miRNA-AGO1 complex (15,20,21,35).…”

Section: Discussionsupporting

confidence: 56%

Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage

Ren

Xie

Zhang

et al. 2014

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

107

122

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In plants, methylation catalyzed by HEN1 (small RNA methyl transferase) prevents microRNAs (miRNAs) from degradation triggered by uridylation. How methylation antagonizes uridylation of miRNAs in vivo is not well understood. In addition, 5′ RNA fragments (5′ fragments) produced by miRNA-mediated RNA cleavage can be uridylated in plants and animals. However, the biological significance of this modification is unknown, and enzymes uridylating 5′ fragments remain to be identified. Here, we report that in Arabidopsis, HEN1 suppressor 1 (HESO1, a miRNA nucleotidyl transferase) uridylates 5′ fragments to trigger their degradation. We also show that Argonaute 1 (AGO1), the effector protein of miRNAs, interacts with HESO1 through its Piwi/Argonaute/Zwille and PIWI domains, which bind the 3′ end of miRNA and cleave the target mRNAs, respectively. Furthermore, HESO1 is able to uridylate AGO1-bound miRNAs in vitro. miRNA uridylation in vivo requires a functional AGO1 in hen1, in which miRNA methylation is impaired, demonstrating that HESO1 can recognize its substrates in the AGO1 complex. On the basis of these results, we propose that methylation is required to protect miRNAs from AGO1-associated HESO1 activity that normally uridylates 5′ fragments. S mall interfering RNAs (siRNAs) and microRNAs (miRNAs), ∼20-25 nucleotides (nt) in size, are important regulators of gene expression. miRNAs and siRNAs are derived from imperfect hairpin transcripts and perfect long double-stranded RNAs, respectively (1, 2). miRNAs and siRNAs are then associated with Argonaute (AGO) proteins to repress gene expression through target cleavage and/or translational inhibition (3). The cleavage of target mRNAs usually occurs at a position opposite the tenth and eleventh nucleotides of miRNAs, resulting in a 5′ RNA fragment (5′ fragment) and a 3′ fragment (4). In Arabidopsis, the major effector protein for miRNA-mediated gene silencing is AGO1, which possesses the endonuclease activity required for target cleavage (5-7). In Drosophila, the exosome removes the 5′ fragments through its 3′-to-5′ exoribonuclease activity (8). How 5′ fragments are degraded in higher plants remains unknown. It has been shown that the 5′ fragments are subject to untemplated uridine addition at their 3′ termini (uridylation) in both animals and plants (9). However, the biological significance of this modification remains unknown because of a lack of knowledge of the enzymes targeting 5′ fragments for uridylation.Uridylation plays important roles in regulating miRNA biogenesis. In animals, TUT4, a terminal uridyl transferase, is recruited by Lin-28 (an RNA binding protein) to the let-7 precursor (prelet-7), resulting in uridylation of prelet-7 (10, 11). This modification impairs the stability of prelet-7, resulting in reduced levels of let-7. In addition, monouridylation has been shown to be required for the processing of some miRNA precursors (12). Deep sequencing analysis reveals that precursor uridylation is a widespread phenomenon occurring in many miRNA families in ani...

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Section: Discussionsupporting

confidence: 56%

Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage

Ren

Xie

Zhang

et al. 2014

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

107

122

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“…3C and Dataset S4B). Tailing involves the nontemplated addition of bases to the 3′ end of sRNAs through adenylation or uridylation (41)(42)(43). Taking these findings together, we conclude that the miRW1 precursor forms a long hairpin structure that is processed to produce miRW1 and other sRNAs that specifically target W1-COE.…”

Section: Rna−seq Mappingmentioning

confidence: 84%

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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“…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%

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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Plant MicroRNAs Display Differential 3' Truncation and Tailing Modifications That Are ARGONAUTE1 Dependent and Conserved Across Species

Cited by 91 publications

References 46 publications

Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage

Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage

Long noncoding miRNA gene represses wheat β-diketone waxes

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

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