Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense

Abstract

Reactive oxygen species (ROS) are both signal molecules and direct participants in plant defense against pathogens. Many fungi synthesize mannitol, a potent quencher of ROS, and there is growing evidence that at least some phytopathogenic fungi use mannitol to suppress ROSmediated plant defenses. Here we show induction of mannitol production and secretion in the phytopathogenic fungus Alternaria alternata in the presence of host-plant extracts. Conversely, we show that the catabolic enzyme mannitol dehydrogenase is induced in a non-mannitol-producing plant in response to both fungal infection and specific inducers of plant defense responses. This provides a mechanism whereby the plant can counteract fungal suppression of ROS-mediated defenses by catabolizing mannitol of fungal origin.Compelling evidence has arisen over the last decade demonstrating that reactive oxygen species (ROS) play a central role in pathogen defense in both animals and plants. In animals, ROS production by phagocytic leukocytes (macrophages͞ neutrophils) is a well characterized antimicrobial defense mechanism (1). Plants produce an analogous, localized oxidative burst (2), wherein massive amounts of antimicrobial ROS [e.g., superoxide, ⅐O 2 Ϫ ; and hydrogen peroxide (H 2 O 2 )] are generated by a pathogen-induced NADPH oxidase localized on the plant plasma membrane (3). In addition to its direct antimicrobial activity, H 2 O 2 also triggers the hypersensitive response, in which plant programmed, localized cell death at the site of infection limits pathogen spread (4). H 2 O 2 also plays a central role in signaling a unique phenomenon known as systemic acquired resistance, in which localized infection of a plant confers enhanced systemic resistance to subsequent attack by the same or unrelated pathogens (5, 6). Systemic acquired resistance is correlated with the systemic induction of a large number of defense-related proteins collectively labeled pathogenesis-related (PR) proteins. In addition to H 2 O 2 , the endogenous signal molecule salicylic acid (SA) is implicated in PR protein induction and has been used extensively as an exogenous stimulator of the systemic acquired resistance response (7,8).A successful pathogen must be able to overcome or suppress this complex array of ROS-mediated host defenses. In fact, microbial suppression of ROS-mediated defenses by secretion of ROS-scavenging enzymes such as superoxide dismutase and catalase, which convert ROS into less reactive species, has been extensively documented in both plant and animal pathogens (9-12). Evidence also is emerging that pathogens suppress ROS-mediated defenses by nonenzymatic quenching of ROS. Mannitol has long been recognized as a potent ROS quencher in vitro (13) and has widely been used as a laboratory reagent to scavenge hydroxyl radicals (HO⅐) generated by the phagocyte respiratory burst or by cell-free oxidant systems (14). In vivo, increased mannitol production protects Saccharomyces cerevisiae from oxidative injury (15). Furthermore, it was recently show...

Mannitol Is Required for Stress Tolerance inAspergillus nigerConidiospores

“…Our results are in agreement with other reports describing fungal mannitol production to prevent oxidative damage, such as mannitol production during infection of the host by the human fungal pathogen C. neoformans (6) and excretion of mannitol by the phytopathogenic fungus A. alternata during plant infection (20). Interestingly, the plant induces MTD in response to fungal infection, presumably for the removal of mannitol to counteract the fungal protection mechanism (20). Since A. niger is a sapropytic fungus and is pathogenic only in immunocompromised individuals, it probably FIG.…”

“…These findings indicate that mannitol is essential for the protection of spores against cell damage which occurs under these stress conditions and that inactivation of mpdA results in conditional mannitol auxotrophy. Our results are in agreement with other reports describing fungal mannitol production to prevent oxidative damage, such as mannitol production during infection of the host by the human fungal pathogen C. neoformans (6) and excretion of mannitol by the phytopathogenic fungus A. alternata during plant infection (20). Interestingly, the plant induces MTD in response to fungal infection, presumably for the removal of mannitol to counteract the fungal protection mechanism (20).…”

“…An example is the phytopathogenic fungus A. alternata, which excretes mannitol during plant infection or in the presence of host plant extracts (20). This fungus appears to use mannitol as an antioxidant to suppress ROS-mediated plant defense.…”

Dissecting the role of G-protein signalling in primary metabolism in the wheat pathogen Stagonospora nodorum

“…Mannitol secretion has been reported in other phytophathogenic species including Alternaria alternata, and is believed to play a role in quenching the reactive oxygen species of the plant defence response (Jennings et al, 1998(Jennings et al, , 2002. This is the first reported evidence of mannitol secretion by S. nodorum.…”

Crystal Structure of Pseudomonas fluorescens Mannitol 2-Dehydrogenase Binary and Ternary Complexes

“…Produced in plants, fungi, protozoa, and bacteria as a storage compound for carbon and reducing equivalents, it also functions in response to oxidative stress and as an osmoregulator (1)(2)(3)(4)(5). D-Mannitol is used extensively in the food and pharmaceutical industry because of its favorable bulking properties and the fact that it does not cause tooth decay and is safe for diabetics.…”