Editors' ChoiceHost-Pathogen Interactions

Plants kill pathogens with cyanide

Sci. Signal.  22 Sep 2015:
Vol. 8, Issue 395, pp. ec272
DOI: 10.1126/scisignal.aad4595

To discourage grazing, some plants constitutively produce cyanogenic glycosides, sugars that are covalently bound to a cyanide group, and store them in the vacuole. These compounds are released from the vacuole and cleaved by cytoplasmic enzymes to release hydrogen cyanide when the tissue is damaged. Rajniak et al. found that Arabidopsis thaliana can produce a cyanogenic compound in response to microbial pathogens. Various pathogens stimulated transcription of CYP82C2, which encodes a P450 cytochrome. A combination of metabolomic, biochemical, and genetic experiments demonstrated that CYP82C2 hydroxylates indole-3-carbonyl nitrile (ICN) to form 4-hydroxyindole-3-carbonyl nitrile (4-OH-ICN) in plants expressing the Pseudomonas syringae pv. tomato effector Psta. ICN and 4-OH-ICN contain a reactive α-ketonitrile group that releases a cyanide ion upon nucleophilic attack. The authors identified the three enzymes that synthesize ICN from tryptophan (Trp) in vivo and used purified recombinant forms of these enzymes to synthesize ICN in vitro. They also reconstituted the biosynthesis of 4-OH-ICN from Trp in vivo by transiently expressing all four biosynthetic enzymes in Nicotiana benthamiana. P. syringae pv. tomato exhibited increased growth on the leaves of cyp82C2 and other ICN biosynthetic mutants compared with wild-type plants. Inoculation of leaves with the spores of either of two different species of necrotrophic fungi caused more leaf damage to ICN biosynthetic mutants than to wild-type plants, but infection with spores of a biotrophic fungus affected wild-type and ICN biosynthetic mutants similarly. In aqueous solution, the half-life of 4-OH-ICN is only about 3 minutes, and ICN rapidly degrades to indole-3-carboxylic acid (ICA). These findings imply that the pathogen-mediated induction of CYP82C2 in Arabidopsis shunts some of the ICN that would otherwise be converted to ICA into the generation of a short-lived cyanogenic compound that inhibits pathogen growth.

J. Rajniak, B. Barco, N. K. Clay, E. S. Sattely, A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence. Nature 525, 376–379 (2015). [PubMed]