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Title: Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs

Author
item FAHLGREN, NOAH - Danforth Plant Science Center
item BOLLMANN, STEPHANIE - Oregon State University
item KASSCHAU, KRISTIN - Oregon State University
item CUPERUS, JOSH - Oregon State University
item Press, Caroline
item SULLIVAN, CHRISTOPHER - Oregon State University
item CHAPMAN, ELISABETH - Oregon State University
item HOYER, JOHN - Danforth Plant Science Center
item GILBERT, KERRIGAN - Danforth Plant Science Center
item Grunwald, Niklaus - Nik
item CARRINGTON, JAMES - Danforth Plant Science Center

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/6/2013
Publication Date: 10/2/2013
Citation: Fahlgren, N., Bollmann, S.R., Kasschau, K.D., Cuperus, J.T., Press, C.M., Sullivan, C.M., Chapman, E.J., Hoyer, J.S., Gilbert, K.B., Grunwald, N.J., Carrington, J.C. 2013. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLoS One. 8(10):e77181.

Interpretive Summary: Phytophthora species, from the Greek ‘plant destroyer’, are among the most important plant pathogens, and are best known for their involvement in the 19th century Irish potato famine and causing modern outbreaks of sudden oak death. Understanding the genetic basis for pathogen development and response to environmental signals, response and interaction with hosts, and host range is a key step to develop strategies for pathogen control. Organisms regulate gene expression through a variety of mechanisms, including the use of small (20–30-nucleotide) RNAs. We investigated the repertoire of small RNAs in three Phytophthora species. We found that the types of small RNAs used by these species are conserved and that they can be generally grouped into two classes, based on length. We hypothesize that the longer small RNAs are used to defend the genome against genetic parasites and the shorter small RNAs are used to regulate gene expression.

Technical 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 are 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.