Salicylic acid stimulates secretion of the normally symplastic enzyme mannitol dehydrogenase: a possible defense against mannitol-secreting fungal pathogens

Abstract

The sugar alcohol mannitol is an important carbohydrate with well-documented roles in both metabolism and osmoprotection in many plants and fungi. In addition to these traditionally recognized roles, mannitol is reported to be an antioxidant and as such may play a role in host-pathogen interactions. Current research suggests that pathogenic fungi can secrete mannitol into the apoplast to suppress reactive oxygen-mediated host defenses. Immunoelectron microscopy, immunoblot, and biochemical data reported here show that the normally symplastic plant enzyme, mannitol dehydrogenase (MTD), is secreted into the apoplast after treatment with the endogenous inducer of plant defense responses salicylic acid (SA). In contrast, a cytoplasmic marker protein, hexokinase, remained cytoplasmic after SA-treatment. Secreted MTD retained activity after export to the apoplast. Given that MTD converts mannitol to the sugar mannose, MTD secretion may be an important component of plant defense against mannitol-secreting fungal pathogens such as Alternaria. After SA treatment, MTD was not detected in the Golgi apparatus, and its SA-induced secretion was resistant to brefeldin A, an inhibitor of Golgi-mediated protein transport. Together with the absence of a known extracellular targeting sequence on the MTD protein, these data suggest that a plant's response to pathogen challenge may include secretion of selected defensive proteins by as yet uncharacterized, non-Golgi mechanisms.

A novel motif in the NaTrxh N-terminus promotes its secretion, whereas the C-terminus participates in its interaction with S-RNase in vitro

“…It has been demonstrated that proteins without signal peptide, such as celery mannitol dehydrogenase in A. thaliana , traffic to the apoplast while bypassing the classical ER/Golgi secretion pathway [56]. Another example is the hygromycin phosphotransferase in A. thaliana , which is secreted through a Golgi-independent route mediated by the Golgi-localized synaptotagmin 2 [57].…”

EXPO, an Exocyst-Positive Organelle Distinct from Multivesicular Endosomes and Autophagosomes, Mediates Cytosol to Cell Wall Exocytosis inArabidopsisand Tobacco Cells

“…Whereas clear functions have been ascribed to this form of unconventional secretion in mammals, such as recycling of transferrin and its receptor (Harding et al, 1984;Pan et al, 1985) and antigen presentation (Denzer et al, 2000;Van Niel et al, 2003), the nature of the molecules released through multivesicular body-PM fusion in plants in still unclear, although there seems to be a connection to the plant pathogen response . In this regard, EXPO-mediated exocytosis might be responsible for the secretion of apoplastic mannitol dehydrogenase upon salicylic acid treatment in plant cells (Cheng et al, 2009).…”

Apoplastic exosome-like vesicles: A new way of protein secretion in plants?

“…1,2 In other words, some extracellular proteins have been discovered that do not make use of the classical signal peptide-dependent secretory pathway. In plants, non-classical secretion has been poorly explored, although Cheng et al 3 have provided evidence on the salycilic acid-induced secretion of mannitol dehydrogenase, a normally symplastic enzyme, using a non-Golgi dependent pathway. In fact, plant non-classical protein secretion is recognized taking into account the large number of leaderless proteins detected in extracellular compartments, and has recently been discussed based on the concepts developed in other eukaryotic systems.…”