Abstract
Replicating circular RNAs are independent plant pathogens known as viroids, or act to modulate the pathogenesis of plant and animal viruses as their satellite RNAs. The rate of discovery of these subviral pathogens was low over the past 40 years because the classical approaches are technical demanding and time-consuming. We previously described an approach for homology-independent discovery of replicating circular RNAs by analysing the total small RNA populations from samples of diseased tissues with a computational program known as progressive filtering of overlapping small RNAs (PFOR). However, PFOR written in PERL language is extremely slow and is unable to discover those subviral pathogens that do not trigger in vivo accumulation of extensively overlapping small RNAs. Moreover, PFOR is yet to identify a new viroid capable of initiating independent infection. Here we report the development of PFOR2 that adopted parallel programming in the C++ language and was 3 to 8 times faster than PFOR. A new computational program was further developed and incorporated into PFOR2 to allow the identification of circular RNAs by deep sequencing of long RNAs instead of small RNAs. PFOR2 analysis of the small RNA libraries from grapevine and apple plants led to the discovery of Grapevine latent viroid (GLVd) and Apple hammerhead viroid-like RNA (AHVd-like RNA), respectively. GLVd was proposed as a new species in the genus Apscaviroid, because it contained the typical structural elements found in this group of viroids and initiated independent infection in grapevine seedlings. AHVd-like RNA encoded a biologically active hammerhead ribozyme in both polarities, and was not specifically associated with any of the viruses found in apple plants. We propose that these computational algorithms have the potential to discover novel circular RNAs in plants, invertebrates and vertebrates regardless of whether they replicate and/or induce the in vivo accumulation of small RNAs.
Highlights
Viroids and a group of satellite RNAs have singlestranded circular RNA genomes that range in size from 220 to 457 nucleotides [1,2,3,4]
Filtering terminal small RNAs (TSRs) derived from linear non-repeat precursor RNAs takes up more than 90% of progressive filtering of overlapping small RNAs (PFOR) running time
To shorten the computing time required for filtering TSRs and to improve the performance of PFOR, PROR2 was developed by converting the previous algorithm written in the explanatory PERL language into the C++ language and adopting the parallel programming technology of OpenMP [24]
Summary
Viroids and a group of satellite RNAs (satRNAs) have singlestranded circular RNA genomes that range in size from 220 to 457 nucleotides (nt) [1,2,3,4]. Recent studies have revealed the production of thousands of non-replicating circular RNAs (circRNAs) across species from Archaea to humans [10,11]. These circRNAs are largely generated from back-spliced exons, in which splice junctions are formed by an acceptor splice site at the 5’ end of an exon and a donor site at the downstream 3’ end [10,12,13]. The functions of circRNAs are largely unknown, a few circRNAs have recently been shown to play regulatory roles as, for example, microRNA sponges [10,12,13]
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