The tripeptide thiol glutathione (γ-L-glutamyl-L-cysteinyl-glycine) is the most important sulfur containing antioxidant in plants and essential for plant defense against abiotic and biotic stress conditions. It is involved in the detoxification of reactive oxygen species, redox signaling, the modulation of defense gene expression and important for the regulation of enzymatic activities. Even though changes in glutathione contents are well documented in plants and its roles in plant defense are well established, still too little is known about its compartment specific importance during abiotic and biotic stress conditions. Due to technical advances in the visualization of glutathione and the redox state of plants through microscopical methods some progress was made in the last few years in studying the importance of subcellular glutathione contents during stress conditions in plants. This review summarizes the data available on compartment specific importance of glutathione in the protection against abiotic and biotic stress conditions such as high light stress, exposure to cadmium, drought, and pathogen attack (Pseudomonas, Botrytis, Tobacco Mosaic Virus). The data will be discussed in connection with the subcellular accumulation of ROS during these conditions and glutathione synthesis which are both highly compartment specific (e.g. glutathione synthesis takes place in chloroplasts and the cytosol). Thus this review will reveal the compartment specific importance of glutathione during abiotic and biotic stress conditions.

Glutathione and reactive oxygen species (ROS) play important roles, within different cell compartments, in activating plant defense and the development of resistance. In mitochondria, the accumulation of ROS and the change of glutathione towards its oxidized state leads to mitochondrial dysfunction, activates cell death, and triggers resistance. The accumulation of glutathione in chloroplasts and peroxisomes at the early stages of plant pathogen interactions is related to increased tolerance and resistance. The collapse of the antioxidative system in these two cell compartments at the later stages leads to cell death through retrograde signaling. The cytosol can be considered to be the switchboard during biotic stress where glutathione is synthesized, equally distributed to, and collected from different cell compartments. Changes in the redox state of glutathione and the accumulation of ROS in the cytosol during biotic stress can initiate the activation of defense genes in nuclei through pathways that involve salicylic acid, jasmonic acid, auxins, and abscisic acid. This review dissects the roles of glutathione in individual organelles during compatible and incompatible bacterial, fungal, and viral diseases in plants and explores the subcelluar roles of ROS, glutathione, ascorbate, and related enzymes in the development of resistance.

Compartment specific changes in ascorbate and glutathione contents were studied during drought stress in Arabidopsis thaliana Col-0 and in ascorbate and glutathione deficient mutants vtc2-1 and pad2-1, respectively, over a time period of 10 days. The results of this study revealed a strong decrease of glutathione contents in both mutants (up to 52% in mitochondria of pad2-1 and 40% in nuclei of vtc2-1) at early time points when drought stress was not yet measurable in leaves even though the soil showed a drop in relative water contents. These results indicate that glutathione is used at early time points to signal drought stress from roots to leaves. Such roles could not be confirmed for ascorbate which remained unchanged in most cell compartments until very late stages of drought. During advanced drought stress the strong depletion of ascorbate and glutathione in chloroplasts (up to 50% in Col-0 and vtc2-1) and peroxisomes (up to 56% in Col-0) could be correlated with a strong accumulation of H2O2. The strong increase of H2O2 and ascorbate in vacuoles (up to 111%) in wildtype plants indicates that ascorbate plays an important role for the detoxification of ROS in vacuoles during drought stress.

Summary: Root‐infecting vascular fungi cause wilt diseases and provoke devastating losses in hundreds of crops. It is currently unknown how these pathogens evolved and whether they can also infect nonvascular plants, which diverged from vascular plants over 450 million years ago. We established a pathosystem between the nonvascular plant Marchantia polymorpha (Mp) and the root‐infecting vascular wilt fungus Fusarium oxysporum (Fo). On angiosperms, Fo exhibits exquisite adaptation to the plant xylem niche as well as host‐specific pathogenicity, both of which are conferred by effectors encoded on lineage‐specific chromosomes. Fo isolates displaying contrasting lifestyles on angiosperms – pathogenic vs endophytic – are able to infect Mp and cause tissue maceration and host cell killing. Using isogenic fungal mutants we define a set of conserved fungal pathogenicity factors, including mitogen activated protein kinases, transcriptional regulators and cell wall remodelling enzymes, that are required for infection of both vascular and nonvascular plants. Markedly, two host‐specific effectors and a morphogenetic regulator, which contribute to vascular colonisation and virulence on tomato plants are dispensable on Mp. Collectively, these findings suggest that vascular wilt fungi employ conserved infection strategies on nonvascular and vascular plant lineages but also have specific mechanisms to access the vascular niche of angiosperms.

Fungal interactions with plant roots, either beneficial or detrimental, have a crucial impact on agriculture and ecosystems. The cosmopolitan plant pathogen Fusarium oxysporum (Fo) provokes vascular wilts in more than a hundred different crops. Isolates of this fungus exhibit host-specific pathogenicity, which is conferred by lineage-specific Secreted In Xylem (SIX) effectors encoded on accessory genomic regions. However, such isolates also can colonize the roots of other plants asymptomatically as endophytes or even protect them against pathogenic strains. The molecular determinants of endophytic multihost compatibility are largely unknown. Here, we characterized a set of Fo candidate effectors from tomato (Solanum lycopersicum) root apoplastic fluid; these early root colonization (ERC) effectors are secreted during early biotrophic growth on main and alternative plant hosts. In contrast to SIX effectors, ERCs have homologs across the entire Fo species complex as well as in other plant-interacting fungi, suggesting a conserved role in fungus–plant associations. Targeted deletion of ERC genes in a pathogenic Fo isolate resulted in reduced virulence and rapid activation of plant immune responses, while ERC deletion in a nonpathogenic isolate led to impaired root colonization and biocontrol ability. Strikingly, some ERCs contribute to Fo infection on the nonvascular land plant Marchantia polymorpha, revealing an evolutionarily conserved mechanism for multihost colonization by root infecting fungi.

Significance: Ascorbate is an essential antioxidant in plants. Total contents and its redox state in organelles are crucial to fight and signal oxidative stress. Recent Advances: With quantitative immunoelectron microscopy and biochemical methods, highest ascorbate contents have recently been measured in peroxisomes (23 m M ) and the cytosol (22 m M ), lowest ones in vacuoles (2 m M ), and intermediate concentrations (4–16 m M ) in all other organelles. Critical Issues: The accumulation of ascorbate in chloroplasts and peroxisomes is crucial for plant defense. Its depletion in chloroplasts, peroxisomes, and mitochondria during biotic stress leads to the accumulation of reactive oxygen species (ROS) and the development of chlorosis and necrosis. In the apoplast and vacuoles, ascorbate is the most important antioxidant for the detoxification of ROS. The cytosol acts as a hub for ascorbate metabolism as it reduces its oxidized forms that are produced in the cytosol or imported from other cell compartments. It is a sink for ascorbate that is produced in mitochondria, distributes ascorbate to all organelles, and uses ascorbate to detoxify ROS. As ascorbate and its redox state are involved in protein synthesis and modifications, it can be concluded that ascorbate in the cytosol senses oxidative stress and regulates plant growth, development, and defense. Future Directions: Future research should focus on (i) dissecting roles of ascorbate in vacuoles and the lumen of the endoplasmic reticulum, (ii) identifying the physiological relevance of ascorbate transporters, and (iii) correlating current data with changes in the subcellular distribution of related enzymes, ROS, and gene expression patterns.