Can silencing of transposons contribute to variation in effector gene expression in Phytophthora infestans?

Abstract

Transposable elements are ubiquitous residents in eukaryotic genomes. Often considered to be genomic parasites, they can lead to dramatic changes in genome organization, gene expression, and gene evolution. The oomycete plant pathogen Phytophthora infestans has evolved a genome organization where core biology genes are predominantly located in genome regions that have relatively few resident transposons. In contrast, disease effector-encoding genes are most frequently located in rapidly evolving genomic regions that are rich in transposons. P. infestans, as a eukaryote, likely uses RNA silencing to minimize the activity of transposons. We have shown that fusion of a short interspersed element (SINE) to an effector gene in P. infestans leads to the silencing of both the introduced fusion and endogenous homologous sequences. This is also likely to occur naturally in the genome of P. infestans, as transcriptional inactivation of effectors is known to occur, and over half of the translocated "RXLR class" of effectors are located within 2 kb of transposon sequences in the P. infestans genome. In this commentary, we review the diverse transposon inventory of P. infestans, its control by RNA silencing, and consequences for expression modulation of nearby effector genes in this economically important plant pathogen.

Figure 1. Model for silencing of an effector-encoding gene by transcriptional fusion to a SINE in P. infestans. Small RNAs derived from endogenous infSINEm (green) initiate silencing of the transgenic PiAvr3a-infSINEm fusion transcript (yellow-blue) through degradation by Argonaute (Ago). Secondary sRNAs are formed from the fusion transcript through the action of RNA dependent RNA polymerase (RdR) and Dicer-like (Dcl). Secondary sRNAs target the endogenous copies of both infSINEm and PiAvr3a (brown) to initiate (Ago) or reinforce silencing (RdR→Dcl→Ago). Arrows indicate the direction and reinforcement of silencing.

Figure 2. Proposed model for transcriptional repression of effector genes due to proximity to transposon sequences. Transposon sequences (TE; blue box) are strongly targeted for silencing by abundant homologous small RNAs (sRNAs). Inactivation of transposons results from formation of heterochromatin, guided by sRNAs. The heterochromatic region may spread outwards along the genomic DNA (dotted line), and affect nearby effector gene sequences (yellow), either through degradation of mRNAs (Ago) or repression of transcription (histone methylation). The formation of additional sRNAs, maintaining or reinforcing the silenced state, can occur through the action of Rdr and Dcl on mRNAs from the transposon or effector gene.

Figure 3. RXLR effector gene proximity to transposon derived sequences in the P. infestans genome. The Y-axis represents the number of RXLR effector genes in each group. The X-axis represents the distance from RXLR effector to nearest transposon-derived sequence (100 bp window) up to a maximum of 2 kb. The PiAvr2 effector is located in the "300" window, PiAvr4 is in the “1200” window, and PiAvrBlb1 is in the “1500” window. The RXLR encoding gene family encompassing PiAvrBlb2 has three paralogs in each of the “400” and “900” windows.