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Title: Aflatoxin biosynthesis is a novel source of reactive oxygen species—a potential redox signal to initiate resistance to oxidative stress?

item ROZE, LUDMILA - Michigan State University
item LAIVENIEKS, MARIS - Michigan State University
item HONG, SUNG-YONG - Michigan State University
item WEE, JOSEPHINE - Michigan State University
item WONG, SHU-SHYAN - Michigan State University
item VANOS, BENJAMIN - Michigan State University
item AWAD, DEENA - Michigan State University
item EHRLICH, KENNETH - Retired ARS Employee
item LINZ, JOHN - Michigan State University

Submitted to: Toxins
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/17/2015
Publication Date: 4/28/2015
Citation: Roze, L.V., Laivenieks, M., Hong, S.-Y., Wee, J., Wong, S.-S., Vanos, B., Awad, D., Ehrlich, K.C., Linz, J.E. 2015. Aflatoxin biosynthesis is a novel source of reactive oxygen species—a potential redox signal to initiate resistance to oxidative stress? Toxins. 7:1411-1430.

Interpretive Summary: As one of the most dangerous natural environmental carcinogens and a strong toxin to humans and animals, it is important to better understand the conditions favoring aflatoxin production by Aspergillus flavus and its benefit to the fungus. To approach this understanding, we have examined the production by A. flavus of reactive oxygen species (ROS) during aflatoxin formation. Reactive oxygen species include peroxides which are known to cause conversion of lipids to rancid and toxic and forms, thus degrading food value. ROS also help the fungus by preventing damage from plant defense agents, thereby making the fungus not only more resistant to antifungal agents but better able to invade and damage crop plants. This study helps to better understand why A. flavus makes aflatoxins and why aflatoxin-producing species have a selective advantage over non-aflatoxin producing fungi. Such considerations are important for evaluating strategies of biocompetitive reduction of aflatoxin in crops by introducing non-aflatoxin-producing fungi in contaminated fields of cotton and maize.

Technical Abstract: Aflatoxin biosynthesis in the filamentous fungus Aspergillus parasiticus involves a minimum of 21 enzymes, encoded by genes located in a 70 kb gene cluster. For aflatoxin biosynthesis to be completed, the required enzymes must be transported to specialized early and late endosomes called aflatoxisomes. Of particular significance, seven aflatoxin biosynthetic enzymes are P450/monooxygenases which catalyze reactions that can produce reactive oxygen species (ROS) as byproducts. Thus, oxidative reactions in the aflatoxin biosynthetic pathway could potentially be an additional source of intracellular ROS. The present work explores the hypothesis that the aflatoxin biosynthetic pathway generates ROS (designated as “secondary” ROS) in endosomes and that secondary ROS possess a signaling function. We used specific dyes that stain ROS in live cells and demonstrated that intracellular ROS levels correlate with the levels of aflatoxin synthesized. Moreover, feeding protoplasts with precursors of aflatoxin resulted in the increase in ROS generation. These data support the hypothesis. Our findings also suggest that secondary ROS may fulfill, at least in part, an important mechanistic role in increased tolerance to oxidative stress in germinating spores (seven-hour germlings) and in regulation of fungal development.