The fungal pathogen Alternaria alternata can infect more than 100 plant species, including many economically important crops: citrus, apple, pear, rice, strawberry, tomato, broccoli, cauliflower, carrot, and potato. A. alternata kills host cells before colonizing the plant and obtains nutrients exclusively from dead tissues, which often contain highly toxic reactive oxygen species (ROS) e.g., hydrogen peroxide, superoxide, and hydroxyl radical.
Surviving a toxic environment in the plant
Research has shown that A. alternata must be able to detoxify toxic “ROS” compounds to establish successful plant host colonization. To survive in the oxidizing environment, A. alternata utilizes multiple defense systems, both enzymatic and nonenzymatic, to alleviate oxidative stress.
Autophagy – adapting to stress by “eating” the toxic ROS
Autophagy is a self-digestion pathway required for cell adaptation to environmental stress and survival. A. alternata uses this process to survive a hostile plant environment, surrounded by toxic ROS.
Pexophagy – “eating” bags of toxins
Peroxisomes are essential for the degradation and synthesis of fatty acids and the generation and detoxification of hydrogen peroxide. Like discreet bags for containing toxic waste, these single-membrane-bounded organelles play a protective role in oxidative stress resistance, development, and pathogenicity in the citrus pathotype of A. alternata. The number of peroxisomes is regulated by biogenesis and degradation to adapt to the changing environment. Excess peroxisomes can be degraded through an autophagy-mediated process called “pexophagy”. Peroxisomes containing toxic ROS are encircled by a double-membrane autophagosome that is fused with the vacuole to degrade peroxisomes and detoxify ROS. In other words, the peroxisome “bags” are created and destroyed according to demand: the more toxic ROS in the environment, the more bags are deployed. These filled bags are then consumed by the fungus to process toxic waste and prevent harm.
In this current study, we provide genetic evidence to support the notion that autophagy-mediated degradation of peroxisomes helps Alternaria alternata to survive toxic oxidizing environments inside host plants.
Starvation and toxins trigger pexophagy in A. alternata and allow for disease in host plants.
Our studies have demonstrated that hydrogen peroxide and nutrient starvation set off pexophagy by increasing peroxisome turnover in A. alternata. Further, autophagy-deficient strains fail to degrade peroxisomes effectively, leading to the accumulation of peroxisomes and hydrogen peroxide. As such, the mutants increase sensitivity to toxic ROS and fail to induce necrotic lesions in young leaves of citrus trees. The defective phenotypes can be restored when the mutated gene is re-introduced into the mutant. Thus, we conclude that pexophagy can act as a protective mechanism under oxidative stress. A better understanding of the pathogenic mechanisms utilized by A. alternata could facilitate the development of novel fungicides.
Pei-Ching Wu, Celine Yen Ling Choo, Hsin-Yu Lu, Xian-Yong Wei, Yu-Kun Chen, Jonar I. Yago and Kuang-Ren Chung published this study in Molecular Plant Pathology:
TITLE IMAGE: Fluorescence microscopy images of Alternaria alternata growing under oxidative stress. In the absence of key autophagy genes, the mutuant (right) accumulates hydrogen peroxide (green fluorescence) inside the hyphae and peroxisomes (red fluorescence) containing toxins remain in the cytoplasm (demonstrated by sharper, denser red spots). All images used with permission of the author.