Fighting fungi, trojan horse style

Hailing Jin, left, is a professor of genetics in the department of plant pathology and microbiology at the University of California, Riverside. | nature.com/Xiaoming Zhang photo

Troop carriers found: Advance RNA soldiers sent by both sides to soften things up ahead of fungal invasions

New research has revealed a vital step in developing eco-friendly fungicides by taking a cue from how plants launch molecules to fight fungal invaders, and how they suppress the genes that make them dangerous.

Biological cells manufacture tiny round structures called extracellular vesicles, also known as exosomes. Their role in responding to invading micro-organisms in plants was only recognized recently.

At the University of California, Riverside, Hailing Jin, professor of genetics in the department of plant pathology and microbiology, and her team discovered that plants use these vesicles as a transportation system to deliver small RNAs to an intruding fungus to suppress and control infection.

“My lab focuses on small RNA functions in gene regulation during plant-pathogen interactions,” said Jin. “In 2013 we discovered that small RNAs can travel from fungus to plant host and suppress the plant’s immunity. Later, we discovered that this cross-kingdom RNA trafficking is bidirectional. Plants can send small RNAs into fungal cells to silence, or interfere with, fungal virulence-related genes.”

While the actual delivery mechanism was unclear, it was known that extracellular vesicles played an important role in transporting RNAs in mammal systems such as body fluids, the nervous system, and in cancer tissues. Liposomes, spherical vesicles, have been used to deliver double stranded RNA to the Neotropical stink bug and the Queensland fruit fly.

Jin speculated that the extracellular vesicles play a role in delivering small RNAs between interacting organisms such as plants and pathogens. The question arose whether organic nanovesicles could be adapted to further improve the interference of RNA against target pests.

The discovery of how plants use these tiny vesicles to deliver the small RNAs has considerable advantages over conventional fungicides. First, they are more eco-friendly because they are similar to naturally occurring features in plants. Second, they naturally degrade so there are no toxic residues left in the soil. Third, this natural method of combating infectious fungi is far less likely to breed drug-resistant pathogens in the future.

“I think they are important not only for defence against pathogen invasions but they also play an important role in transporting RNAs and other cargoes between cells within a plant,” said Jin.

But the question became how to load desired small RNAs into the vesicles. It was that focus of the research that led to an important finding.

“We discovered a set of RNA-binding proteins including the RNAi pathway component Argonaute protein and DEAD box helicases (enzymes), which contribute to RNA selective loading into extracellular vesicles,” she said. “Plants have receptor proteins and other signalling molecules that can sense an invasion. Previously we saw movement of RNA, but we didn’t know how the small RNAs were selected and transported.”

They were able to see that Arabidopsis plants secrete extracellular vesicles into Botrytis cinerea, a fungus that infects many crop plant species. The fungus infects wine grapes where sit is known as botrytis bunch rot while, in horticulture, it is called grey mould disease infecting a wide range of crops. Infections can result in serious economic losses.

“This was the first example of a host plant using these vesicles to deliver small RNAs to another organism,” said Jin. “The vesicles shuttle small RNAs between cells, like tiny Trojan horses with weapons hidden inside.”

The discovery that RNA-binding proteins attach to specific small molecules and load them into extracellular vesicles could lead to ways to turn off the destructive genes of an invasive fungus and enhance the efficiency of disease control.

In a recent report in the journal PLOS Pathogens, Jin wrote that the discovery of cross-species and cross-kingdom RNA molecules has inspired scientists to design new disease control strategies against pathogens and pests in agriculture, such as host-induced gene silencing (HIGS) and spray-induced gene silencing (SIGS). Studies of extracellular vesicles in silencing RNA trafficking are encouraging development of innovative delivery methods of small RNAs using artificial vesicles, or nanoparticles.

The current research study was published in Nature Plants.

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