Plants speak ‘roundworm’ for self-defense, study shows

Nematodes are tiny, ubiquitous roundworms that infect plant roots, causing more than $100 billion in crop damage worldwide each year. New research has found that plants manipulate the worms’ pheromones to repel infestations, providing insights into how farmers could fight these pests.

 

Led by faculty member Frank Schroeder, the group studied a group of chemicals called ascarosides, which the worms produce and secrete to communicate with each other. As described in a paper published Jan. 10 in Nature Communications, the researchers have shown that plants also “talk” to nematodes by metabolizing ascarosides and secreting the metabolites back into the soil.

 

“It’s not only that the plant can ‘sense’ or ‘smell’ a nematode,” said Schroeder, a professor at Boyce Thompson Institute and a professor of chemistry and chemical biology in Cornell’s College of Arts and Sciences. “It’s that the plant learns a foreign language, then broadcasts something in that language to spread propaganda that ‘this is a bad place.’ Plants mess with nematodes’ communications system to drive them away.”

 

The study built on the team’s previous work, which showed that plants react to ascr#18 – the predominant ascaroside secreted by plant-infecting nematodes – by bolstering their own immune defenses, thereby protecting them from many types of pests and pathogens.

 

“We also saw [in those earlier studies] that when ascr#18 was given to plants, the chemical disappears over time,” said lead author Murli Manohar, a senior research associate at BTI.

 

That observation, along with published literature suggesting plants could modify pest metabolites, led the team to hypothesize that “plants and nematodes interact via small molecule signaling and alter one another’s messages,” Schroeder said.

 

To probe that idea, the team treated three plant species – Arabidopsis (small flowering plants), wheat and tomato – with ascr#18 and compared compounds found in treated and untreated plants. They identified three ascr#18 metabolites, the most abundant of which was ascr#9.

 

The researchers also found Arabidopsis and tomato roots secreted the three metabolites into the soil, and that a 10-to-1 mixture of ascr#9 and ascr#18 added to the soil steered nematodes away from the plant’s roots, thereby reducing infection.

 

The team hypothesized that nematodes in the soil perceive the mixture as a signal, sent by plants already infected with nematodes, to “go away” and prevent overpopulation of a single plant. Worms may have evolved to hijack plant metabolism to send this signal.

 

Plants, in turn, may have evolved to tamper with the signal to appear as heavily infected as possible, thereby fooling would-be invaders.

 

“This is a dimension of their relationship that no one has seen before,” said Daniel Klessig, a BTI faculty member and adjunct professor in the Department of Plant Pathology in Cornell’s College of Agriculture and Life Sciences, who is also a co-author on the paper. “And plants may have similar types of chemical communication with other pests.”

 

The team also showed that plants metabolize ascr#18 via the peroxisomal beta-oxidation pathway, a system conserved across many plant species.

 

“This paper uncovers an ancient interaction,” Schroeder said. “All nematodes make ascarosides, and plants have had millions of years to learn how to manipulate these molecules.

 

“Plants aren’t passive green things,” he said. “They are active participants in an interactive dialogue with the surrounding environment, and we will continue to decipher this dialogue.”

 

These discoveries are being commercialized by a BTI and Cornell-based startup Ascribe Bioscience as a family of crop protection products named Phytalix.

 

Co-authors include Xiaohong Wang, courtesy professor in the Plant Pathology and Plant-Microbe Biology Section of CALS; and Shiyan Chen, a research associate in Wang’s lab. Other contributors were from the USDA’s Robert W. Holley Center for Agriculture and Health, and the University of California, Davis.

 

This work was supported by grants from the U.S. Department of Agriculture and the National Institutes of Health.