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Plants Influence Their Microbiomes To Keep Pathogens at Bay

A plant held upside-down, showing the root system.
Credit: Josue Michel/ Unsplash
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New research shows how plants' secretion of chemicals affects the composition of the microbiome in and around plant roots, keeping plant pathogens at bay and making plants less vulnerable to infection. But it's a delicate balance, as too little or too much of the chemicals can adversely affect the composition of beneficial microorganisms. 

The soil contains a wealth of bacteria, fungi and microorganisms such as nematodes. Nematodes live either freely or in close association with plant roots. Many nematode species are plant parasitic and cause major yield losses each year. 

"Microbiome is a common term for the whole community of microorganisms in a given environment. And the microbiome can help to either promote or prevent infections by nematodes or other pests," says Professor Mogens Nicolaisen from the Department of Agroecology at Aarhus University. 

Plants use microbiome for protection

In other words, plants depend on the composition of the microbiome, which is perhaps why they have the ability to secrete various chemical substances that affect the microbiome in ways that are beneficial to the plant itself. 

"We have investigated how either the lack or overproduction of certain chemical compounds by plants can affect the composition of the microbiome in plant roots. In general, we assume that plants attract beneficial microorganisms and try to keep harmful ones away by using specific chemical substances," says Mogens Nicolaisen. 

Flavonoids are a group of substances secreted by plants that have been shown to affect the microbiome around plants. This is why researchers at the Department of Agroecology have been studying this particular group of substances. 

Sorts in microorganisms

Plants can thus influence their associated microorganisms by means of flavonoids, but what happens if the plant secretes more or less of the substance? How does it affect the plant parasitic nematodes around the plant's roots? And what effect does it have on the plant's microbiome? 

These are just some of the questions researchers have been working on. 

"We have been working with mutant plants. That is, plants that either secrete very high or very low amounts of flavonoids. And we could see that there are differences in how flavonoids affects the overall microbiome, just as we could see that in some of the mutant plants there was a different composition of nematodes, and that it was particularly nematodes that are parasites on the roots that reacted. This shows us that the plant's susceptibility to attack by parasitic nematodes changes when there are changes in the plant's secretion of flavonoids," says senior researcher Mette Vestergård Madsen from the Department of Agroecology.

Flavonoids do not affect nematodes directly

According to the researchers, nematodes were not significantly affected when the plant produced large amounts of flavonoids, but there was an effect when the plants produced smaller amounts of flavonoids. 

"It was surprising that the nematodes did not respond to the high flavonoid level, so we decided to look at the whole microbiome from the different mutant plants. That is, we transferred the microbiome from the different mutants to new plants and infected the plants with a parasitic nematode species called Meloidogyne incognita. And to our surprise, we found that the microbiome derived from the flavonoid overproducing mutant, which had otherwise shown no significant effect on the overall nematode community, produced a dramatic increase in Meloidogyne incognita in the new plants. So, something in the microbiome composition requires a strong infection of M. incognita" says Mette Vestergård Madsen.

Fact box - Meloidogyne incognita

M. incognita is the most widespread and economically important plant-parasitic nematode species in tropical and subtropical regions. It is highly problematic as it attacks a very wide. Both cultivated crops and wild plants can be attacked by M. incognita. 

"So, the species is not a big problem in Denmark, but we use it in our experiments because it is a good model organism when you want to experimentally study mechanisms and relationships, as it is easy to keep in culture and easy to work with experimentally," says Mette Vestergård Madsen.

In other words, the overproduction of flavonoids must have affected individual species in the microbiome involved in protecting the plant from the plant parasitic nematode. 

"So, flavonoids do not have a very large direct effect on the overall nematode community, nor on M. incognita, which we worked with in these experiments. Instead, it is the composition of the microbiome itself that has an effect," says Mogens Nicolaisen. That's why another study is looking specifically at which microorganisms are important in regulating M. incognita infestation. 

Bacteria attract nematodes

In fact, a closer look at the different nematode species and different bacteria shows how they interact either positively or negatively. 

"We can see that there are some bacteria and fungi that are affected by flavonoid concentration. When we need to find species of bacteria and fungi that affect M. incognita, they are possible candidates," explains Mette Vestergård Madsen.

The researchers believe that the plants regulate the microbiome via the secretion of flavonoids. This is a very fine balance, as too much flavonoid, as was the case with one of the mutant plants, would impair the microbiome's ability to limit infection by certain nematodes. Conversely, microbiomes from plants secreting either little or no flavonoids have been shown to be significantly better at preventing infection. 

"We can use these results in our future research, where we would like to investigate plants that secrete different amounts of flavonoids, just as there are different types of flavonoids that we would also like to investigate further. Ultimately, we would like to be able to create or find plants with exactly the right excretion of flavonoids, so that they are least vulnerable to infection from nematodes, for example," says Mogens Nicolaisen, continuing, "At the same time, we are interested in determining the specific microorganisms that are able to affect infection with M. incognita."

Reference: Sikder MM, Vestergård M, Kyndt T, Topalović O, Kudjordjie EN, Nicolaisen M. Genetic disruption of Arabidopsis secondary metabolite synthesis leads to microbiome-mediated modulation of nematode invasion. ISME J. 2022;16(9):2230-2241. doi: 10.1038/s41396-022-01276-x

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