Potato blight can hijack the plant autophagic system

By Wang Guo

Plant pathogens secrete molecules not only to neutralise the immune system of the host, but also to make the host work for them.

Oomycota is a group of around 500 species that date back to the Cretaceous period (144 – 66 million years ago). These are unicellular eukaryotic organisms that absorb nutrients from the surrounding environment. Some oomycetes are free-living organisms and saprotrophic, which means that they obtain nutrients from decomposing organic material. But oomycetes are better known for causing diseases in plants. 1

Figure 1 From Wiki Images Potato infected with Phytophthora infestans

A species of Oomycota termed Phytophthora infestans is infamously known to cause a disease called late blight in potatoes. This malady was the culprit of The Great Irish Famine of 1846, spoiling the majority of the potato crops in Ireland, which was the main source of food, especially amongst the poorest people. The consequences were catastrophic, one million Irish lost their lives and another one and a half million emigrated to America. This last event was key in the development of the United States as a future international power. A single organism managed to change the history of mankind.1

A species of Oomycota termed Phytophthora infestans is infamously known to cause a disease called late blight in potatoes. This malady was the culprit of The Great Irish Famine of 1846, spoiling the majority of the potato crops in Ireland, which was the main source of food, especially amongst the poorest people. The consequences were catastrophic, one million Irish lost their lives and another one and a half million emigrated to America. This last event was key in the development of the United States as a future international power. A single organism managed to change the history of mankind. 1

200 years later, Phytophthora infestans is still threatening our crops of potatoes. Approximately, 20% of potatoes are lost due to late (or early) blight, causing a loss of more than 3.5 billion pounds worldwide each year.2 Farmers combat this parasite mainly using pesticides, but this solution is temporary and expensive. Moreover, It pollutes the environment and is harmful to local species. This situation is aggravated by the fact that domestic crops have low genetic variability because of the artificial selection over generations of the crops with the most desirable traits for humans like high production of seeds. Meanwhile, plant pathogens are under constant modifications and improvements through natural selection in the wild. This greatly increases the chances of successful pathogenic invasions. An effective solution must be found as soon as possible in a world with a growing population to feed.

Figure 2 From Wiki Images Basic structure of a haustorium

Phytophthora infestans uses a modified filament called haustorium to penetrate through the plant cell wall but not the cell membrane to absorb its nutrients. Also, it secretes effector proteins that neutralise the plant immune system. Some of these effector proteins are accumulated in the haustorium interface, so they are termed perihaustorial effectors. A particular perihaustorial effector, PexRD54, could manipulate the plant autophagy system in order to ease infection and nutrient absorption.3

Autophagy is a regulated cellular process in which the cell uses lysosomes to digest its deteriorated or unutilised structures, reutilising them again for other anabolic processes. Also, they can be degraded to release energy, which is stored in form of ATP. It starts with the formation of a double bilayer in the cytosol called phagophore (Xie et al., 2008). Then, the phagophore associates with the cargo and develops into the autophagosome. These bind lysosomes, which contains hydrolytic enzymes that degrade the cargo inside the autophagosome.

The PexRD54 of Phytophthora infestans binds to hosts’ ubiquitin group AT8CL, activating autophagy pathways in plants. This is because the ubiquitin group AT8CL controls the movement of other proteins responsible for autophagy regulatory mechanisms inside the cell.4 PexrRD54 acts on proteins located in the autophagosomes and also the autophagic structures surrounding the haustorium. It causes the movement of autophagosomes to their feeding areas, where they can absorb nutrients from the plant. Apart from a nutritional purpose, the hijack of the plant autophagic system by PexRD54 also has a virulence effect, because autophagy can be used to destroy antimicrobial substances. For example, a protein called Rab8a is located in regions close to the haustorium and is involved in defence-related secretions. PexrD54 triggers the autophagy of Rab8a.3 Paradoxically, in animal pathogens, PexRD54 does not promote the formation of autophagosomes but inhibits autophagy.5

This proves that the function of effector protein in pathogenic invasions goes beyond what we expected it to be. Effectors can be used to disrupt host metabolic pathways for the benefit of the pathogen. An understanding of the metabolic pathways and cellular structures affected by the effectors of plant pathogens may help us to develop new treatments more sustainable and effective based on the modification of these metabolic pathways in order to make them immune to the effectors.

REFERENCE LIST

1.         Sleigh MA. Protozoa and other protists. Cambridge: Cambridge Univ. Press; 1991. 342 p.

2.         Lal M, Sharma S, Yadav S, Kumar S. Management of Late Blight of Potato. Potato – From Incas to All Over the World. IntechOpen; 2018. Available from: https://www.intechopen.com/chapters/58251

3.         Pandey P, Leary AY, Tumtas Y, Savage Z, Dagvadorj B, Duggan C, et al. An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface. eLife. 2021 Aug 23;10:e65285.

4.         Maqbool A, Hughes RK, Dagdas YF, Tregidgo N, Zess E, Belhaj K, et al. Structural Basis of Host Autophagy-related Protein 8 (ATG8) Binding by the Irish Potato Famine Pathogen Effector Protein PexRD54. Journal of Biological Chemistry. 2016 Sep;291(38):20270–82.

5.         Kimmey JM, Stallings CL. Bacterial Pathogens versus Autophagy: Implications for Therapeutic Interventions. Trends in Molecular Medicine. 2016 Dec;22(12):1060–76.

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