Contribution of maize polyamine and amino acid metabolism toward resistance against Aspergillus flavus infection and aflatoxin production

Authors: Majumdar, Raj; MINOCHA, RAKESH - Us Forest Service (FS); Lebar, Matthew; Rajasekaran, Kanniah - Rajah; LONG, STEPHANIE - Us Forest Service (FS); Carter-Wientjes, Carol; MINOCHA, SUBHASH - University Of New Hampshire; Cary, Jeffrey

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/8/2019
Publication Date: 5/24/2019
Citation: Majumdar, R., Minocha, R., Lebar, M.D., Rajasekaran, K., Long, S., Carter-Wientjes, C.H., Minocha, S., Cary, J.W. 2019. Contribution of maize polyamine and amino acid metabolism toward resistance against Aspergillus flavus infection and aflatoxin production. Frontiers in Plant Science. 10:692. https://doi.org/10.3389/fpls.2019.00692.
DOI: https://doi.org/10.3389/fpls.2019.00692

Interpretive Summary: Aspergillus flavus (A. flavus) infects maize and other economically important crop plants such as peanut and produces aflatoxins that are potent carcinogens. Aflatoxins pose serious threat to human and animal health and reduce crop value. Different approaches including breeding for aflatoxin resistance traits, transgenic expression of resistance-associated proteins, ‘Host Induced Gene Silencing’ (HIGS), and biocontrol are currently being evaluated to improve pre-harvest aflatoxin resistance in maize. In the present study, we explored the role of polyamines in maize host resistance against the fungus. Polyamines are nitrogenous molecules that are widely distributed in plants, microbes, and all other living organisms. They are well known for their stress ameliorating roles in plants. To investigate the role of polyamines in maize aflatoxin resistance we used known susceptible and resistant maize varieties and challenged them with a high aflatoxin producing A. flavus strain. The results presented here show distinct roles of polyamines and other associated nitrogenous compounds in the resistant lines possibly contributing to resistance to A. flavus growth and aflatoxin production. The current work provides future opportunities to alter polyamine metabolism in maize during A. flavus infection in agronomically important susceptible varieties to improve aflatoxin resistance and overall stress tolerance.

Technical Abstract: Polyamines (PAs) are ubiquitous polycations found in plants and other organisms that are essential for growth, development, and resistance against abiotic and biotic stresses. The role of PAs in plant disease resistance depends on the relative abundance of higher PAs [spermidine (Spd), spermine (Spm)] vs. the diamine putrescine (Put) and PA catabolism. With respect to the pathogen, PAs are required to achieve successful pathogenesis of the host. Maize is an important food and feed crop, which is highly susceptible to Aspergillus flavus infection. Upon infection, the fungus produces carcinogenic aflatoxins and numerous other toxic secondary metabolites that adversely affect human health and crop value worldwide. To evaluate the role of PAs in aflatoxin resistance in maize, in vitro kernel infection assays were performed using maize lines that are susceptible (SC212) or resistant (TZAR102, MI82) to aflatoxin production. Results indicated significant induction of both PA biosynthetic and catabolic genes upon A. flavus infection. As compared to the susceptible lines, the resistant maize lines showed higher basal expression of PA metabolism genes in mock-inoculated kernels that increased upon fungal infection. In general, increased biosynthesis and conversion of Put to Spd and Spm along with their increased catabolism was evident in the resistant lines vs. the susceptible line SC212. There were higher concentrations of amino acids such as glutamate (Glu), glutamine (Gln) and '-aminobutyric acid (GABA) in SC212. The resistant lines were significantly lower in fungal load and aflatoxin production as compared to the susceptible line. The data presented here demonstrate an important role of PA metabolism in the resistance of maize to A. flavus colonization and aflatoxin contamination. These results provide future direction for the manipulation of PA metabolism and/or the use of Spd/Spm as biomarkers to screen maize genotypes for improved aflatoxin resistance and overall stress tolerance.