A parasitic bacterium has found a way to turn its host plant sterile, forcing it to grow leaves instead of flowers. This change makes the plant more attractive as feeding and breeding grounds for insects called leafhoppers, and after the bugs eat the plants, the bacteria hitch a ride in their saliva and on to the next plant.
Pathogens that rely on more than one host to complete their life cycle often modify the behavior and development of each, coercing them into improving the parasite's survival and reproduction. These sorts of parasitic mind control take all kinds of forms: from sexually-transmitted viruses that sterilize crickets but leaves them horny to liver flukes that compel ants to climb a blade of grass into a cow’s mouth. Fascinating, yes, but there are surprisingly few studies that describe the mechanisms behind host coercion. How do parasites actually do this?
“We know these parasites are puppet masters but the strings they are pulling have yet to be identified,” Saskia Hogenhout from the John Innes Centre in Norwich, U.K., says in news release.
So, Hogenhout and colleagues figured out how it works in one particular host-parasite relationship. A bacterial plant parasite called phytoplasma relies on insects like leafhoppers (Macrosteles quadrilineatus) for its dispersal to crops like grapes, coconuts, and oilseed rape. Once there, the insect-transmitted pathogen alters the floral development, converting flowers into vegetative tissue and causing a proliferation of stems known as “witches' broom.” All these parasite-induced transformations end up sterilizing the plant and turning it into more attractive sites for the egg-laying of their leafhopper vectors. The bacteria colonize the bugs when they eat the plants, and later when they dribble saliva as they suck the sap of another plant, the bacteria spread into new plant tissue. It’s a simple tragic love triangle, really.
“The plant appears alive, but it’s only there for the good of the pathogen,” Hogenhout tells Nature. “In an evolutionary sense, the plant is dead and will not produce offspring.”
First, the team identified the virulence protein behind all the transformations: SAP54. It exerts its effect by degrading proteins that regulate important developmental processes in flowering plants. (Reducing the activity of those proteins in the lab generated sterile plants.) Then, they discovered that their degradation process relies on the manipulation of a single plant protein called RAD23, which shuttles molecules to the protein degradation machinery. That's normally necessary for waste disposal in the plant, but in this case, RAD23 sends the flower-making proteins off for destruction.
Additionally, choice tests showed how leafhoppers lay more eggs in infected plants with leaf-like flowers than healthy plants. They seem to prefer the new vegetative biomass over the wild floral whorls, possibly because the new arrangement lowers the plant’s natural defenses against the insects. An effector that targets and suppresses flowering while simultaneously promoting insect colonization is unprecedented. “This parasite is incapable of surviving without its insect and plant hosts and we can reveal for the first time how it is able to manipulate them both,” Hogenhout says.
The work was published in PLOS Biology this week.
Images: JIC Photography (top), A.M. MacLean et al. PLOS 2014 via Wageningen UR