Abstract
MicroRNAs (miRNAs) and secondary small interfering RNAs (principally phased siRNAs or trans-acting siRNAs) are two distinct subfamilies of small RNAs (sRNAs) that are emerging as key regulators of posttranscriptional gene expression in plants. Both miRNAs and secondary-siRNAs (sec-siRNAs) are processed from longer RNA precursors by DICER-LIKE proteins (DCLs). Gossypium arboreum L., also known as tree cotton or Asian cotton, is a diploid, possibly ancestral relative of tetraploid Gossypium hirsutum L., the predominant type of commercially grown cotton worldwide known as upland cotton. To understand the biological significance of these gene regulators in G. arboreum, a bioinformatics analysis was performed on G. arboreum small RNAs produced from G. arboreum leaf, flower, and boll tissues. Consequently, 263 miRNAs derived from 353 precursors, including 155 conserved miRNAs (cs-miRNAs) and 108 novel lineage-specific miRNAs (ls-miRNAs). Along with miRNAs, 2,033 miRNA variants (isomiRNAs) were identified as well. Those isomiRNAs with variation at the 3’-miRNA end were expressed at the highest levels, compared to other types of variants. In addition, 755 pha-siRNAs derived 319 pha-siRNA gene transcripts (PGTs) were identified, and the potential pha-siRNA initiators were predicted. Also, 2,251 non-phased siRNAs were found as well, of which 1,088 appeared to be produced by so-called cis- or trans-cleavage of the PGTs observed at positions differing from pha-siRNAs. Of those sRNAs, 148 miRNAs/isomiRNAs and 274 phased/non-phased siRNAs were differentially expressed in one or more pairs of tissues examined. Target analysis revealed that target genes for both miRNAs and pha-siRNAs are involved a broad range of metabolic and enzymatic activities. We demonstrate that secondary siRNA production could result from initial cleavage of precursors by both miRNAs or isomiRNAs, and that subsequently produced phased and unphased siRNAs could result that also serve as triggers of a second round of both cis- and trans-cleavage of additional siRNAs, leading to the formation of complex sRNA regulatory networks mediating posttranscriptional gene silencing. Results from this study extended our knowledge on G. arboreum sRNAs and their biological importance, which would facilitate future studies on regulatory mechanism of tissue development in cotton and other plant species.
Highlights
Small regulatory RNAs, have been found in a wide variety of plants from mosses to eudicots [1,2,3,4,5,6,7,8] and mediate a broad range of biological processes, including growth, development, and stress responses [1,2,9,10,11]
MiRNAs appear to be processed from single-stranded precursors that are transcribed by RNA polymerase II (PolII), which are capable of self-folding into hair-pin shaped secondary structures and are subsequently processed by a specific set of nucleases referred to as DICER-LIKE proteins (DCLs) [13,14] with assistance of DRB (Double-stranded RNA Binding) proteins [15,16]
Other types of small interfering RNAs (siRNAs) include heterochromatic siRNAs, sometimes referred to as repeat-associated siRNAs that are typically 24 nt in length [22,23] and nat-siRNAs are produced from a pair of natural antisense transcripts (NAT pairs) that are independently transcribed from sense and antisense strands that are either produced from NAT pairs derived from the same genomic locus or derived from NAT pairs transcribed from distinct genomic loci [8,24]
Summary
Small regulatory RNAs (sRNAs), have been found in a wide variety of plants from mosses to eudicots [1,2,3,4,5,6,7,8] and mediate a broad range of biological processes, including growth, development, and stress responses [1,2,9,10,11]. Based on origin and biogenesis, these gene regulators can be divided into at least two major classes [12], microRNAs (miRNAs) and small interfering RNAs (siRNAs), each of which can be further divided into subsequent groups. MiRNAs appear to be processed from single-stranded precursors that are transcribed by RNA polymerase II (PolII), which are capable of self-folding into hair-pin shaped secondary structures (known as hairpins or stem-loops) and are subsequently processed by a specific set of nucleases referred to as DICER-LIKE proteins (DCLs) [13,14] with assistance of DRB (Double-stranded RNA Binding) proteins [15,16]. Canonical miRNAs, typically ~21 nt or 22 nt in length, are processed by the DCL1/AGO1 pathway [13,14] and apparently mediate gene expression posttranscriptionally by either cleavage of or translation suppression of target mRNAs, respectively [17,18]. The mechanism by which these classes of small RNA mediate gene expression is less well understood at this time their length distribution suggests that they most likely work other than posttranscriptionally
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