Silencing and innate immunity in plant defense against viral and non-viral pathogens

Abstract

The frontline of plant defense against non-viral pathogens such as bacteria, fungi and oomycetes is provided by transmembrane pattern recognition receptors that detect conserved pathogen-associated molecular patterns (PAMPs), leading to pattern-triggered immunity (PTI). To counteract this innate defense, pathogens deploy effector proteins with a primary function to suppress PTI. In specific cases, plants have evolved intracellular resistance (R) proteins detecting isolate-specific pathogen effectors, leading to effector-triggered immunity (ETI), an amplified version of PTI, often associated with hypersensitive response (HR) and programmed cell death (PCD). In the case of plant viruses, no conserved PAMP was identified so far and the primary plant defense is thought to be based mainly on RNA silencing, an evolutionary conserved, sequence-specific mechanism that regulates gene expression and chromatin states and represses invasive nucleic acids such as transposons. Endogenous silencing pathways generate 21-24 nt small (s)RNAs, miRNAs and short interfering (si)RNAs, that repress genes post-transcriptionally and/or transcriptionally. Four distinct Dicer-like (DCL) proteins, which normally produce endogenous miRNAs and siRNAs, all contribute to the biogenesis of viral siRNAs in infected plants. Growing evidence indicates that RNA silencing also contributes to plant defense against non-viral pathogens. Conversely, PTI-based innate responses may contribute to antiviral defense. Intracellular R proteins of the same NB-LRR family are able to recognize both non-viral effectors and avirulence (Avr) proteins of RNA viruses, and, as a result, trigger HR and PCD in virus-resistant hosts. In some cases, viral Avr proteins also function as silencing suppressors. We hypothesize that RNA silencing and innate immunity (PTI and ETI) function in concert to fight plant viruses. Viruses counteract this dual defense by effectors that suppress both PTI-/ETI-based innate responses and RNA silencing to establish successful infection.

Figure 1

Zig-zag model for evolution of innate immunity- and silencing-based plant defense against viral and non-viral pathogens (adopted and extended from Jones and Dangl 2006 [10]). The ultimate amplitude of disease resistance or susceptibility is proportional to [PTI + Silencing – ETS + ETI]. In phase 1, plants detect pathogen-associated molecular patterns (PAMPs) and host danger-associated molecular patterns (DAMPs) via pattern-recognition receptors (PRRs) to induce pattern-triggered immunity (PTI) and, in the case of viral pathogens, plants additionally detect viral double-stranded RNA (dsRNA) to trigger RNA silencing. In phase 2, successful viral and non-viral pathogens deliver effectors/suppressors that interfere with both PTI and silencing, resulting in effector-triggered susceptibility (ETS). In phase 3, one effector or suppressor is recognized directly or indirectly by an NB-LRR protein, activating effector-triggered immunity (ETI), an amplified version of PTI that often passes a threshold for induction of hypersensitive response (HR) and programmed cell death (PCD). In phase 4, pathogen isolates are selected that have lost or modified the specifically recognized effector/suppressor, and perhaps gained a new effector that can help the pathogen to suppress ETI. A new plant NB-LRR allele is then evolved and selected that can recognize the newly acquired effector, resulting again in ETI.