Silencing and innate immunity in plant defense against viruses

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 microbe-associated molecular patterns (MAMPs), 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. RNA silencing (RNA interference, RNAi) is 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 function in concert to fight plant viruses. Viruses counteract this dual defense by effectors that suppress both PTI/ETI innate responses and silencing to establish successful infection. We further propose that plant pararetroviruses encode two types of effectors, a viral protein-based and a viral RNA-based. We are testing these hypotheses by studying various DNA and RNA viruses in model plants including Arabidopsis thaliana and Nicotiana benthamiana as well as crop plants including tomato, cassava, banana, rice and grapevine.

Selected Publications

Rajeswaran R, Golyaev V, Seguin J, Zvereva A, Farinelli L, Pooggin MM. 2014. Interactions of rice tungro bacilliform pararetrovirus and its protein P4 with plant RNA silencing machinery. Molecular Plant Microbe Interactions  Aug 14. [Epub ahead of print

Rajeswaran R, Seguin J, Chabannes M, Duroy PO, Laboureau N, Farinelli L, Iskra-Caruana ML, and  Pooggin MM. 2014. Evasion of siRNA-directed antiviral silencing in Musa acuminata persistently infected with six distinct banana streak pararetroviruses. J. Virol. published ahead of print 23 July 

Pooggin MM. 2013. How Can Plant DNA Viruses Evade siRNA-Directed DNA Methylation and Silencing? International Journal of Molecular Sciences 14: 15233-15259

Zvereva AS, Pooggin MM. 2012. Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4: 2578-2597

Aregger M, Borah BK, Seguin J, Rajeswaran R, Gubaeva EG, Zvereva AS, Windels D, Vazquez F, Blevins T, Farinelli L, Pooggin MM. 2012. Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathogens 8: e1002941.

Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M, Baerlocher L, Farinelli L, Meins F Jr, Hohn T, Pooggin MM. 2011. Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Research 39:5003-14.

Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D,  Si-Ammour A, Park H-S, Vazquez F, Robertson D, Meins F, Hohn T and Pooggin MM. 2006. Multiple plant dicers mediate viral small RNA biogenesis and DNA virus induced gene silencing. Nucleic Acids Research 34: 6233-6246.

Pooggin M, Shivaprasad PV, Veluthambi K and Hohn T. 2003. RNAi targeting of DNA virus in plants. Nature Biotechnology 21, 131-132.