Comprehensive Annotation of <i>Physcomitrella patens</i> Small RNA Loci Reveals That the Heterochromatic Short Interfering RNA Pathway Is Largely Conserved in Land Plants

Çoruh, Ceyda; Cho, Sung Hyun; Shahid, Saima; Liu, Qikun; Wierzbicki, Andrzej; Axtell, Michael J.

doi:10.1105/tpc.15.00228

Cited by 52 publications

(47 citation statements)

References 56 publications

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“…However, a protein sequence of similar features from P. patens was identified and clustered out of both DCL1 clades (conventional and conifer-specific, Figure S11 and Figure 9), suggesting a potential common origin for all species for these shortened DCL-like sequences. This sequence corresponds to a short variant of DCL1 recently characterized in P. patens and identified as MINIMAL DICER-LIKE (mDCL) (Coruh et al 2015). This gene lacks the N-terminal helicase domain of DCL proteins, and has only PAZ and RNAseIII domains.…”

Section: Resultsmentioning

confidence: 93%

“…The mDCL is specifically required for 23-nt siRNA accumulation associated with genomic repetitive elements. Mutant analysis showed a dependence of this protein on DCL3 for generating the complete set of siRNAs (Coruh et al 2015). Phylogenetic resolution of this protein remained unclear, although it clustered with DCL1 sequences in spite of its association with siRNAs.…”

Section: Resultsmentioning

confidence: 99%

“…We were able to identify a truncated version of S. moellendorffii DCL with only a RNAseIII domain and with sequence similarity to DCL1s that clustered alongside mDCL1, both basal to the overall DCL1 lineage. It has been suggested that shortened versions of DCLs might arise frequently during evolution (Coruh et al 2015). For example, truncated versions of DCLs, which lack the N-terminal helicases and the PAZ domain (similarly to those identified in conifers), also have been described as functional in other non-plant organisms (Malone et al 2005).…”

Section: Resultsmentioning

confidence: 99%

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Assessing the Gene Content of the Megagenome: Sugar Pine (Pinus lambertiana)

González-Ibeas

Martínez-García

Famula

et al. 2016

G3 Genes|Genomes|Genetics

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Sugar pine (Pinus lambertiana Douglas) is within the subgenus Strobus with an estimated genome size of 31 Gbp. Transcriptomic resources are of particular interest in conifers due to the challenges presented in their megagenomes for gene identification. In this study, we present the first comprehensive survey of the P. lambertiana transcriptome through deep sequencing of a variety of tissue types to generate more than 2.5 billion short reads. Third generation, long reads generated through PacBio Iso-Seq have been included for the first time in conifers to combat the challenges associated with de novo transcriptome assembly. A technology comparison is provided here to contribute to the otherwise scarce comparisons of second and third generation transcriptome sequencing approaches in plant species. In addition, the transcriptome reference was essential for gene model identification and quality assessment in the parallel project responsible for sequencing and assembly of the entire genome. In this study, the transcriptomic data were also used to address questions surrounding lineage-specific Dicer-like proteins in conifers. These proteins play a role in the control of transposable element proliferation and the related genome expansion in conifers.

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Section: Resultsmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Assessing the Gene Content of the Megagenome: Sugar Pine (Pinus lambertiana)

González-Ibeas

Martínez-García

Famula

et al. 2016

G3 Genes|Genomes|Genetics

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“…However, homologs of key genes known to be responsible for hcsiRNA biogenesis and function in angiosperms clearly exist in diverse plant lineages (Zong et al, 2009;Banks et al, 2011;Huang et al, 2015;Wang and Ma, 2015;You et al, 2017). Reverse genetic analyses of these homologs, coupled with sRNA-seq analyses of the mutants, has shown that hc-siRNAs exist in the moss P. patens (Cho et al, 2008;Coruh et al, 2015), which implies that the pathway was most likely present in the last common ancestor of all land plants. Whether hc-siRNAs have been specifically lost in the conifers and/or ferns remains an open question, but the presence of high levels of 24 nt RNAs in specific tissues of the conifers Norway spruce (Picea abies) (Nystedt et al, 2013) and Japanese larch (Larix leptolepis) (Zhang et al, 2013) suggests that this may not be the case.…”

Section: Conservation Evolution and Annotations Of Endogenouse Sirnasmentioning

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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“…In this "de novo" scenario, occasional antisense transcripts could form double-stranded RNA by pairing with sense transcripts, which could trigger the production of small interfering RNAs (siRNAs) to target DRM2 for de novo methylation in gene bodies. Although mechanistically feasible, it is difficult to explain why gbM is absent from many nonangiosperm plants (such as the moss Physcomitrella patens) with functional RdDM and MET1 pathways (12).…”

mentioning

confidence: 99%

On the origin and evolutionary consequences of gene body DNA methylation

Bewick

Niederhuth

et al. 2016

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

281

418

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In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum. Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.DNA methylation | gene body methylation | epigenetics | histone modifications | CHROMOMETHYLASE 3 I n angiosperms, cytosine DNA methylation occurs in three sequence contexts: Methylated CG (mCG) is catalyzed by METHYLTRANSFERASE 1 (MET1), mCHG (where H is A/C/T) by CHROMOMETHYLASE 3 (CMT3), and mCHH by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 2 (CMT2) (1). MET1 performs a maintenance function and is targeted by VARIANT IN METHYLATION 1 (VIM1), which binds preexisting hemimethylated CG sites. In contrast, DRM2 is targeted by RNA-directed DNA methylation (RdDM) for the de novo establishment of mCHH. CMT3 forms a self-reinforcing loop with the H3K9me2 pathway to maintain mCHG; however, considering that transformation of CMT3 into the cmt3 background can rescue DNA methylation defects, it is reasonable to also consider CMT3 a de novo methyltransferase (2). Two main lines of evidence suggest that DNA methylation plays an important role in the transcriptional silencing of transposable elements (TEs): that TEs are usually methylated, and that the loss of DNA methylation (e.g., in methyltransferase mutants) is often accompanied by TE reactivation.A large number of plant genes (e.g., ∼13.5% of all Arabidopsis thaliana genes) also contain exclusively mCG in the transcribed region and a depletion of mCG from both the transcriptional start and stop sites (referred to as "gene body DNA methylation"; gbM) ( Fig. 1A) (3)(4)(5). A survey of plant methylome data showed that the emergence of gbM in the plant kingdom is specific to angiosperms (6), whereas nonflowering plants (such as mosses and green algae) have much more diverse genic methylation patterns (7,8). Similar to mCG at TEs, the maintenance of gbM requires MET1. In contrast to DNA methylation at TEs, however, gbM does not appear to be associated with transcriptional repression. Rather, genes containing gbM are ubiquitously expressed at moderate to high levels compared with non-gbM genes (4, 5, 9), and within gbM genes there is a correlation between transcript abundance and methylation levels (10, 11).It has been proposed ...

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Comprehensive Annotation of Physcomitrella patens Small RNA Loci Reveals That the Heterochromatic Short Interfering RNA Pathway Is Largely Conserved in Land Plants

Cited by 52 publications

References 56 publications

Assessing the Gene Content of the Megagenome: Sugar Pine (Pinus lambertiana)

Assessing the Gene Content of the Megagenome: Sugar Pine (Pinus lambertiana)

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

On the origin and evolutionary consequences of gene body DNA methylation

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