Inception: sRNAs make zombie plants

A paper published last October in Science (1) shows that the fungus Botrytis cinereauses small RNAs (sRNAs) to parasite Argonaute 1 protein and direct the gene silencing machinery of the plant against its own defensive genes, paving the way towards invasion. 

Botrytis in tomato

Botrytis cinerea is the causative agent of grey mold, an infection that affects many economically important crops, like grapevine, tomato or strawberry, causing billionaire losses worldwide. What is the key to success for a pathogen with such a wide range of hosts? Weiberg et al. have discovered the fungus weapon: surprisingly, it is not a protein but a set of small RNAs that will silence host immunity genes.

Botrytis in strawberry

 

Using Arabidopsis thaliana and tomato (S. lycopersicum) leaves infected with B. cinerea, researchers built a library of sRNAs from the fungus (Bc-sRNAs) and selected those induced during infection that were also close in sequence to Arabidopsis or tomato genes, finding 73 Bc-sRNAs that could target genes in both plants. To validate this prediction, three of the most abundant Bc-sRNAs were chosen, measuring the levels of the respective plant transcripts, which were indeed decreased and corresponded to genes involved in plant’s immune response to B. cinerea. 

 Basically, double stranded RNA is diced by DICER. The nuclease RISC then cleaves mRNAs homologous in sequence to the dsRNA.

Intrigued about the mechanism used for the suppression of the defenses, a hijack of the plant silencing machinery by the Bc-sRNAs was postulated. Confirmation came when Argonaute 1 (AGO1) protein, the nuclease in the RISC complex, was immunoprecipitated from infected leaves and sRNAs from the fungus were pulled-down with it.  Further evidence was provided by the reduced susceptibility of ago1 mutants. On the contrary, the double dcl1 dcl2 mutant of B. cinerealacking the proteins involved in processing of sRNAs, were less pathogenic, demonstrating the importance of sRNA production for fungus virulence.

This work by Weiberg et al. presents a double agent at the service of the fungus army, the sRNAs, in charge of occupying Ago1 and use it for their own purpose: plant invasion. Even if it is the first paper showing endogenous sRNAs travelling from fungus to plants, it is not the first report about cross-kingdom RNAi: another work published in Plant Cell (2) three years ago demonstrated that RNAs designed against fungal transcripts can travel to Blumeria graminis cells, the mildew, and specifically silence their targets. However, it is still unknown if plants have endogenous sRNAs in their ranks against fungi.

Mildew in barley

 

The present study raises many questions: are sRNAs a common strategy employed by fungi? Will it be used by other pathogens? How will plants counterattack? For the moment, regarding sRNA, fungi command and plants obey!

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1)      A. Weiberg et al., Science 342, 118 (2013).

2)      D. Nowara et al., Plant Cell 22, 3130 (2010).