PNAS January 2 2018; vol.115; no.1: 210–215
How pathogens manipulate host cellular machinery to enable infection is a major question in biology. The ability of Cochliobolus carbonum race 1 to infect susceptible corn plants relies on production of HC-toxin (HCT). While it is known that HC-toxin is a histone deacetylase inhibitor, knowledge of how HCT actually promotes virulence has remained elusive. Here, we use mass spectrometry to quantify protein abundance and levels of protein acetylation in HCT-treated or pathogen-infected plants. These analyses revealed that the activity of plant-encoded enzymes can be modulated to alter both histone and nonhistone protein acetylation during a susceptible interaction and suggest that virulent C. carbonum utilizes HCT to reprogram the transcriptional response to infection, resulting in an ineffective defense response.
Lysine acetylation is a key posttranslational modification that regulates diverse proteins involved in a range of biological processes. The role of histone acetylation in plant defense is well established, and it is known that pathogen effector proteins encoding acetyltransferases can directly acetylate host proteins to alter immunity. However, it is unclear whether endogenous plant enzymes can modulate protein acetylation during an immune response. Here, we investigate how the effector molecule HC-toxin (HCT), a histone deacetylase inhibitor produced by the fungal pathogen Cochliobolus carbonum race 1, promotes virulence in maize through altering protein acetylation. Using mass spectrometry, we globally quantified the abundance of 3,636 proteins and the levels of acetylation at 2,791 sites in maize plants treated with HCT as well as HCT-deficient or HCT-producing strains of C. carbonum. Analyses of these data demonstrate that acetylation is a widespread posttranslational modification impacting proteins encoded by many intensively studied maize genes. Furthermore, the application of exogenous HCT enabled us to show that the activity of plant-encoded enzymes (histone deacetylases) can be modulated to alter acetylation of nonhistone proteins during an immune response. Collectively, these results provide a resource for further mechanistic studies examining the regulation of protein function by reversible acetylation and offer insight into the complex immune response triggered by virulent C. carbonum.