Effects of elevated CO2 on maize defense against mycotoxigenic Fusarium verticillioides

Authors: Vaughan, Martha; Huffaker, Alisa; Schmelz, Eric; Dafoe, Nicole; Christensen, Shawn; Sims, James; Martins, Vitor; Swerbilow, Jay; Romero, Maritza; Alborn, Hans; Allen Jr, Leon; Teal, Peter

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/24/2014
Publication Date: 5/13/2014
Publication URL: http://onlinelibrary.wiley.com/doi/10.1111/pce.12337/full
Citation: Vaughan, M.M., Huffaker, A., Schmelz, E.A., Dafoe, N.J., Christensen, S.A., Sims, J.W., Martins, V.F., Swerbilow, J.C., Romero, M.I., Alborn, H.T., Allen Jr, L.H., Teal, P.E. 2014. Effects of elevated CO2 on maize defense against mycotoxigenic Fusarium verticillioides. Plant Cell and Environment. doi: 10.1111/pce.12337.

Interpretive Summary: Fusarium verticillioides is an important mycotoxigenic fungal pathogen of maize (Zea mays). Mycotoxin, fumonisins produced by F. verticillioides pose a serious risk to food safety and are among the top concerns with regard to climate change because environmental conditions, such as drought, contribute to disease development and fumonisin production. Scientists at the USDA-ARS Center for Medical, Agricultural and Veterinary Entomology in Gainesville, Florida, investigated the combined impact of projected double ambient [CO2] and drought on the interaction between maize and F. verticillioides. Double ambient [CO2] (2x[CO2]) enhanced fungal proliferation, but did not affect the quantity of fumonisin contaminants in maize stem tissue. The combination of both 2x[CO2] and drought further exasperated the accumulation of F. verticillioides biomass, while severe drought reduced fungal biomass at 1x[CO2]. Growth at 2x[CO2] did not significantly alter the nutritional quality of maize stalk tissue. However, in response to pathogen infection the concentration of soluble carbohydrates, total proteins and fatty acids were increased at 1x[CO2] but not at 2x[CO2]. The accumulation of defense metabolites (MBOA and phytoalexins) were also reduced in infected maize plants at 2x[CO2]. Examination of early jasmonic acid (JA) levels in response to F. verticillioides infection, indicated that the defense hormone defense response maybe dampened at 2x[CO2]. Maize plants at 2x[CO2] that accumulated significantly less JA and phytoalexins had the highest amount of pathogen biomass. The attenuation of JA signaling and the reduction of fumonisin produced per unit F. verticillioides biomass are potentially a result of limited free fatty acid substrate for oxylipin biosynthesis. By stimulating the defense response prior to F. verticillioides infection, maize plants grown at 2x[CO2] were capable of restricting pathogen proliferation to comparable levels as maize at 1x[CO2]. The adaptation of new disease management strategies may be necessary to improve the production and safety of the future maize crop at higher [CO2].

Technical Abstract: Elevated atmospheric carbon dioxide concentration ([CO2]) increased maize susceptibility to Fusarium verticillioides stalk rot. Even though the pathogen biomass accumulated to significantly higher levels at double ambient [CO2] (2x[CO2]), the projected [CO2] concentration to occur at the end of this century, the quantity of fumonisin mycotoxin contaminants were unaltered. Combined effects of [CO2] and drought on pathogen infection were contradictory; drought reduced F. verticillioides biomass in maize stalks at ambient [CO2] (1x[CO2]), but increased pathogen biomass in stems at 2x[CO2]. In the absence of the host plant, 2x[CO2] hindered F. verticillioides growth but enhanced fuminison production on media. The soluble carbohydrate, starch, protein and fatty acid content of the maize stem tissues were not significantly altered by 2x[CO2]. However, in response to F. verticillioides infection, the accumulation of soluble carbohydrates, total proteins, fatty acids, MBOA and phytoalexins was absent or reduced in maize plants at 2x[CO2]. Examination of early JA levels in response to F. verticillioides infection, indicated that the phytohormone defense response maybe dampened at 2x[CO2]. There was a direct correlation between JA levels and the levels of defense metabolites, and an inverse correlation with pathogen proliferations. The attenuation of JA signaling and the reduction of fumonisin produced per unit F. verticillioides biomass are potentially a result of limited free fatty acid substrate for oxylipin biosynthesis. By stimulating the defense response prior to F. verticillioides infection, maize plants grown at 2x[CO2] were capable of restricting pathogen proliferation to comparable levels as maize at 1x[CO2]. The adaptation of new disease management strategies, such as priming, may be necessary to improve the production and safety of the future maize crop at higher [CO2].