Phytophthora Have Distinct Endogenous Small RNA Populations That Include Short Interfering and microRNAs

Abstract

In eukaryotes, RNA silencing pathways utilize 20-30-nucleotide small RNAs to regulate gene expression, specify and maintain chromatin structure, and repress viruses and mobile genetic elements. RNA silencing was likely present in the common ancestor of modern eukaryotes, but most research has focused on plant and animal RNA silencing systems. Phytophthora species belong to a phylogenetically distinct group of economically important plant pathogens that cause billions of dollars in yield losses annually as well as ecologically devastating outbreaks. We analyzed the small RNA-generating components of the genomes of P. infestans, P. sojae and P. ramorum using bioinformatics, genetic, phylogenetic and high-throughput sequencing-based methods. Each species produces two distinct populations of small RNAs that are predominantly 21- or 25-nucleotides long. The 25-nucleotide small RNAs were primarily derived from loci encoding transposable elements and we propose that these small RNAs define a pathway of short-interfering RNAs that silence repetitive genetic elements. The 21-nucleotide small RNAs were primarily derived from inverted repeats, including a novel microRNA family that is conserved among the three species, and several gene families, including Crinkler effectors and type III fibronectins. The Phytophthora microRNA is predicted to target a family of amino acid/auxin permeases, and we propose that 21-nucleotide small RNAs function at the post-transcriptional level. The functional significance of microRNA-guided regulation of amino acid/auxin permeases and the association of 21-nucleotide small RNAs with Crinkler effectors remains unclear, but this work provides a framework for testing the role of small RNAs in Phytophthora biology and pathogenesis in future work.

The tRNA-Derived Small RNAs Regulate Gene Expression through Triggering Sequence-Specific Degradation of Target Transcripts in the Oomycete Pathogen Phytophthora sojae

“…However, no canonical miRNAs have been reported (Nunes et al, 2011b). In oomycetes, several miRNAs, a variety of siRNAs, and tsRNAs were discovered recently (Vetukuri et al, 2012; Fahlgren et al, 2013; Qutob et al, 2013; Asman et al, 2014). While miRNAs and siRNAs are known to regulate gene expression, whether and how tsRNAs regulate gene expression remains unclear.…”

“…Little is known about the mode of regulation by sRNAs in the oomycete pathogens, although the presence of sRNAs was increasingly evident in these organisms (Vetukuri et al, 2012; Fahlgren et al, 2013; Qutob et al, 2013; Asman et al, 2014). P. sojae is a model oomycete species and is a destructive soybean pathogen that causes $1–2 billion losses per year (Tyler, 2007).…”

The advance of tomato disease-related microRNAs

“…Severe symptom-inducing PSTVd-I accumulated more sRNAs than mild symptom-inducing PSTVd-D in tomato leaves and stem tissues, which correlated with its higher viroid titers in the tissues (Tsushima et al 2015). MiRNAs have also been discovered in P. infestans Fahlgren et al 2013;Vetukuri et al 2012). During the infection of tomato leaves, the expression level of miR466 and miR1918 altered dramatically.…”

Helitrons , the Eukaryotic Rolling-circle Transposable Elements

“…Small RNAs homologous to Helitron sequences have been described from maize (67), A. thaliana (134), Phytophthora species, (187,188) and Physcosmitrella patens (189). Generally it is surmised that one kind of small RNA (small interfering (siRNA)) regulate TE expression.…”