Experts reveal pest, plant, pathogen interaction

Bacteria called phytoplasmas alter a plant’s development so that it is attractive to leaf hoppers

LINDELL BEACH, B.C. — British scientists have shed new light on a plant pathogen that causes yield losses in crops worldwide.

The research at the John Innes Centre shows how a plant, an insect and a bacterium have a three-way relationship to the detriment of the crop.

Leaf hoppers are tiny sap-sucking, highly mobile and opportunistic agricultural pests. Some species can acquire and transmit pathogens such as viruses and phytoplasmas, which are small bacteria.

Their relationship with phytoplasmas can cause severe yield losses in crops such as sugar beets, oilseeds, fruit trees, vegetables, corn and grapevines.

“The leafhopper is the form of transport for the aster yellows witches’ broom phytoplasma,” said Saskia Hogenhout, a research scientist with the John Innes Centre.

“The phytoplasma produces a protein effector to reduce the production of a plant’s defence hormone that regulates the plant’s defence against leafhopper attack. As a result, leafhoppers produce more eggs on the phytoplasma-infected plants.

“The offspring that hatch from the eggs feed from the infected plants and become colonized with the phytoplasmas.

“As adults, these leafhoppers migrate to other plants, transporting the phytoplasmas (and spreading infection).”

The witches’ broom strain of the phytoplasma used in the research was isolated from infected lettuce fields in North America.

Hogenhout said that while infected plants show the presence of witches’ broom bacteria, they still have no evidence that the phytoplasma actually attracts leafhoppers. Nor does the reduction in the plant’s defence hormone influence the leafhoppers.

What attracts leafhoppers to infected trees are the egg-laying opportunities in its multiple stems, whose growth is triggered by the phytoplasma. The research shows that leafhoppers lay more eggs and generate more offspring when living on infected plants and plants that produce fewer defence hormones.

This study is particularly important because the scientists have identified a specific molecule in the parasite that manipulates plant development to the advantage of the insect host. It can reach beyond its host to alter a third organism, the crop plant.

It is well known that pathogens can alter their hosts, sometimes in spectacular ways. For example, malaria parasites can make humans more attractive to mosquitoes, but just how they do it has always been a mystery.

Vector-born animal pathogens can alter blood viscosity to aid blood ingestion by insects. Fungus can induce the formation of “pretend” flowers to attract insects that enable the reproduction of the fungus.

In this triage of plant, bug and bacteria, the infected plants are triggered to grow clusters of multiple stems that make them look like a scraggly witches’ broom, or in the case of trees, like a bird’s nest.

This phytoplasma-induced clustered growth, along with green colouration of non-green flower tissues, elongated stalks and bunchy, fibrous secondary roots, makes them more attractive to leafhoppers for egg-laying.

More eggs result in more insects that can spread the parasite further to infect more plants. In addition, the leafhopper survives longer on phytoplasma infected plants, which adds to its progeny production.

“This is the first evidence that phytoplasma produce effectors that interact with specific plant proteins,” Hogenhout said.

“If we find ways to interfere with this interaction, then we can generate plants that are more resistant to phytoplasma colonization.”

She said that while the bacteria produce many effectors to reduce a plant’s defence hormone, only a few are responsible for the extreme symptoms, such as interference with flower development in witches’ broom.

“This is a problem for seed production of, for example, canola and many other crops,” Hogenhout said.

“We are investigating the mechanism by which the effector interferes with flower development. This will help us to define strategies to breed for crops with reduced symptom development upon phytoplasma infection.”

The leafhoppers had to be kept under quarantine under research conditions because they were originally exotic plant pests.

“We have a quarantine insectary on site,” said Hogenhout.

“(It) is licensed for maintaining exotic insects and there is sufficient room for experiments. Moreover, we have a knowledgeable and dedicated insectary management team on site, (so) my lab did not face great challenges working with these organisms.”

In the lab, the scientists sequenced and examined the genome of the witches’ broom phytoplasma, which is invisible to the naked eye and can be seen only with specialized staining techniques and a microscope to visualize the bacteria in plants and insects. They identified 56 candidate molecules, or protein effectors, which could be key to the complex biological interaction.

“So far, the genomes of four different phytoplasmas have been sequenced to completion,” she said.

“This revealed interesting information about the biology of phytoplasmas. However, there are hundreds of phytoplasmas that infect various economically important crops worldwide and little genome sequence information is available for the vast majority of them. My colleagues and I recently initiated the Phytoplasma Genome Sequencing Initiative to sequence more phytoplasma genomes.”

The research produced clear evidence that leafhoppers reared on infected plants laid more eggs, produced more offspring and generated an increased rate in transmission of the witches’ broom phytoplasma through the new generation of leafhoppers to other plants.

This complex biological relationship gives the phytoplasmas a competitive advantage.

“Leafhoppers are found on almost every plant species,” said Hogenhout.

“There are at least 15,000 leafhopper species worldwide. However, relatively few are agricultural pests that can transmit phytoplasmas. In general, leafhoppers tend to like warmer climates and do not survive harsh winters.”

Some species, such as the insect vector of aster yellows witches’ broom phytoplasma, survive throughout the year in the southern U.S.

Global warming enables leafhoppers to survive, migrate north to Canada and transmit phytoplasmas for longer periods of time. They are also becoming a problem in Europe with northward migration as a result of milder temperatures.

“We are analyzing and comparing the genome sequences of multiple phytoplasmas. This will unravel which effectors are conserved among phytoplasmas and may present the (bacteria’s) Achilles heel that can be targeted to control multiple phytoplasmas simultaneously.”

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