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1. Reproductive phasiRNA loci and DICER-LIKE5, but not microRNA loci, diversified in monocotyledonous plants

   https://doi.org/10.1093/plphys/kiab001  

   Patel, Parth; Mathioni, Sandra M; Hammond, Reza; Harkess, Alex E; Kakrana, Atul; Arikit, Siwaret; Dusia, Ayush; Meyers, Blake C (January 2021, Plant Physiology)

   null (Ed.)

   Abstract In monocots other than maize (Zea mays) and rice (Oryza sativa), the repertoire and diversity of microRNAs (miRNAs) and the populations of phased, secondary, small interfering RNAs (phasiRNAs) are poorly characterized. To remedy this, we sequenced small RNAs (sRNA) from vegetative and dissected inflorescence tissue in 28 phylogenetically diverse monocots and from several early-diverging angiosperm lineages, as well as publicly available data from 10 additional monocot species. We annotated miRNAs, small interfering RNAs (siRNAs) and phasiRNAs across the monocot phylogeny, identifying miRNAs apparently lost or gained in the grasses relative to other monocot families, as well as a number of transfer RNA fragments misannotated as miRNAs. Using our miRNA database cleaned of these misannotations, we identified conservation at the 8th, 9th, 19th, and 3′-end positions that we hypothesize are signatures of selection for processing, targeting, or Argonaute sorting. We show that 21-nucleotide (nt) reproductive phasiRNAs are far more numerous in grass genomes than other monocots. Based on sequenced monocot genomes and transcriptomes, DICER-LIKE5, important to 24-nt phasiRNA biogenesis, likely originated via gene duplication before the diversification of the grasses. This curated database of phylogenetically diverse monocot miRNAs, siRNAs, and phasiRNAs represents a large collection of data that should facilitate continued exploration of sRNA diversification in flowering plants. 

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2. Small RNA biogenesis and degradation

   https://doi.org/10.1007/978-3-319-55520-1_6  

   Yu, Q.; Liu, Y.; Li, M.; Yu, B. (January 2017, RNA technologies)

   Small RNAs (sRNAs), ~20–25 nucleotide (nt) in size, regulate various biological processes in plants through directing sequence-specific gene silencing. sRNAs are derived from either single- or double-stranded precursor RNAs. Proper levels of sRNAs are crucial for plant growth, development, genomic stability, and adaptation to abiotic and biotic stresses. Studies have identified the machineries controlling sRNA levels through biogenesis and degradation. This chapter covers recent progresses related to mechanisms governing small RNA biogenesis and degradation. 

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3. The evolutionary history of small RNAs in Solanaceae

   https://doi.org/10.1093/plphys/kiac089  

   Baldrich, Patricia; Bélanger, Sébastien; Kong, Shuyao; Pokhrel, Suresh; Tamim, Saleh; Teng, Chong; Schiebout, Courtney; Gurazada, Sai Guna; Gupta, Pallavi; Patel, Parth; et al (February 2022, Plant Physiology)

   Abstract The Solanaceae or “nightshade” family is an economically important group with remarkable diversity. To gain a better understanding of how the unique biology of the Solanaceae relates to the family’s small RNA (sRNA) genomic landscape, we downloaded over 255 publicly available sRNA data sets that comprise over 2.6 billion reads of sequence data. We applied a suite of computational tools to predict and annotate two major sRNA classes: (1) microRNAs (miRNAs), typically 20- to 22-nucleotide (nt) RNAs generated from a hairpin precursor and functioning in gene silencing and (2) short interfering RNAs (siRNAs), including 24-nt heterochromatic siRNAs typically functioning to repress repetitive regions of the genome via RNA-directed DNA methylation, as well as secondary phased siRNAs and trans-acting siRNAs generated via miRNA-directed cleavage of a polymerase II-derived RNA precursor. Our analyses described thousands of sRNA loci, including poorly understood clusters of 22-nt siRNAs that accumulate during viral infection. The birth, death, expansion, and contraction of these sRNA loci are dynamic evolutionary processes that characterize the Solanaceae family. These analyses indicate that individuals within the same genus share similar sRNA landscapes, whereas comparisons between distinct genera within the Solanaceae reveal relatively few commonalities. 

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4. Arabidopsis apoplastic fluid contains sRNA- and circular RNA–protein complexes that are located outside extracellular vesicles

   https://doi.org/10.1093/plcell/koac043  

   Zand Karimi, Hana; Baldrich, Patricia; Rutter, Brian D; Borniego, Lucía; Zajt, Kamil K; Meyers, Blake C; Innes, Roger W (February 2022, The Plant Cell)

   Abstract Previously, we have shown that apoplastic wash fluid (AWF) purified from Arabidopsis leaves contains small RNAs (sRNAs). To investigate whether these sRNAs are encapsulated inside extracellular vesicles (EVs), we treated EVs isolated from Arabidopsis leaves with the protease trypsin and RNase A, which should degrade RNAs located outside EVs but not those located inside. These analyses revealed that apoplastic RNAs are mostly located outside and are associated with proteins. Further analyses of these extracellular RNAs (exRNAs) revealed that they include both sRNAs and long noncoding RNAs (lncRNAs), including circular RNAs (circRNAs). We also found that exRNAs are highly enriched in the posttranscriptional modification N6-methyladenine (m6A). Consistent with this, we identified a putative m6A-binding protein in AWF, GLYCINE-RICH RNA-BINDING PROTEIN 7 (GRP7), as well as the sRNA-binding protein ARGONAUTE2 (AGO2). These two proteins coimmunoprecipitated with lncRNAs, including circRNAs. Mutation of GRP7 or AGO2 caused changes in both the sRNA and lncRNA content of AWF, suggesting that these proteins contribute to the secretion and/or stabilization of exRNAs. We propose that exRNAs located outside of EVs mediate host-induced gene silencing, rather than RNA located inside EVs. 

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5. Phylogenetic analyses of seven protein families refine the evolution of small RNA pathways in green plants

   https://doi.org/10.1093/plphys/kiad141  

   Bélanger, Sébastien; Zhan, Junpeng; Meyers, Blake C (March 2023, Plant Physiology)

   Abstract Several protein families participate in the biogenesis and function of small RNAs (sRNAs) in plants. Those with primary roles include Dicer-like (DCL), RNA-dependent RNA polymerase (RDR), and Argonaute (AGO) proteins. Protein families such as double-stranded RNA-binding (DRB), SERRATE (SE), and SUPPRESSION OF SILENCING 3 (SGS3) act as partners of DCL or RDR proteins. Here, we present curated annotations and phylogenetic analyses of seven sRNA pathway protein families performed on 196 species in the Viridiplantae (aka green plants) lineage. Our results suggest that the RDR3 proteins emerged earlier than RDR1/2/6. RDR6 is found in filamentous green algae and all land plants, suggesting that the evolution of RDR6 proteins coincides with the evolution of phased small interfering RNAs (siRNAs). We traced the origin of the 24-nt reproductive phased siRNA-associated DCL5 protein back to the American sweet flag (Acorus americanus), the earliest diverged, extant monocot species. Our analyses of AGOs identified multiple duplication events of AGO genes that were lost, retained, or further duplicated in subgroups, indicating that the evolution of AGOs is complex in monocots. The results also refine the evolution of several clades of AGO proteins, such as AGO4, AGO6, AGO17, and AGO18. Analyses of nuclear localization signal sequences and catalytic triads of AGO proteins shed light on the regulatory roles of diverse AGOs. Collectively, this work generates a curated and evolutionarily coherent annotation for gene families involved in plant sRNA biogenesis/function and provides insights into the evolution of major sRNA pathways. 

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