Reuniting crop plants with their lost microbial partners makes them more resistant to diseases

Reuniting crop plants with the micro-organisms that their ancestors live with in the wild is a promising way to make crops more resilient against pathogens. PhD candidate Dario Ramirez Villacis collected soil and micro-organisms in the Andes Mountains in Ecuador, the center of origin of wild potato plants. He showed that cultivated potato plants grown in soil with restored microbial communities develop fewer symptoms when infected with potato late blight (Phytophthora infestans). Ramirez Villacis recently defended his PhD and will continue the line of research at Utrecht University.

High in the Andes live the ancestors of the potato plants now growing on Dutch soil. But these wild potato plants are quite different from the ones we know. “The tubers of the wild potato plants are small and taste bitter, “ says Ramirez Villacis. “Over centuries, we have domesticated the plants, selecting for big and tasty tubers.”

Different plants, communities and environments

This process did not just change the plant itself. In the wild, plants live in communities. Not only with other plants and animals, but also with a whole range of micro-organisms such as bacteria and fungi. Some of these microbes do not have much effect on the plants, but others can be beneficial or detrimental to the plants.
 

By selecting against bitterness, we took away the plant’s ability to control its surroundings.

“The chemicals that make the tubers taste bitter are actually antimicrobials,” explains Ramirez Villacis. “They give the plant the ability to control the microbes in their surroundings. By selecting against bitterness, we took away the plant’s ability to control its surroundings.”

What is more, crop plants are grown in environments that are highly modified by humans. “We till the soil, add fertilizer, and use pesticides. All these interventions destroy the microbiome, the collection of micro-organisms, in the soil,” says Ramirez Villacis. “Not all plants do well under such conditions. People selected for tough plants that, along the way, lost other capabilities.”

Back to the center of origin

To try to gain insights into how agriculture impacted the soil microbiome, Ramirez Villacis decided to go back to the center of origin of the potato plants: the highlands of his home-country Ecuador. “I looked for locations where you have a natural site and an agricultural site right next to each other. We drove along a 700 kilometer long transect and were able to find 14 suitable locations. At each location, we collected soil from both the natural and the agricultural site. In total, we ended up with about two tons of soil.”

This will hopefully help us narrow it down to just two or three microbes that together do the same things as this collection of microbes.

Greenhouse experiments

Next, he grew potato plants in pots filled with either the natural or the agricultural soils, all under the same conditions in the same greenhouse. To test for possible differences in resistance to pathogens, he infected the plants with potato late blight (Phytophthora infestans). “We found that the plants growing in the natural soil showed less symptoms, like spots and lesions, compared to those in agricultural soil.”

When the natural soils were treated with heat to reduce the number of microbes, the protective effect of the natural soils was lost. Also, mixing natural soil into agricultural soil made plants more resistant to the pathogen. All these findings supports the idea that the beneficial effect of the natural soil was caused by the microbes living in it.

DNA analysis

To gain insight into how the composition of the microbiome differs between agricultural and natural soils, Ramirez Villacis analyzed the microbial DNA found in the soil from the different sites. “Across these fourteen very diverse and different locations, we identified around 150 microbes that were present in the natural soils but consistently reduced in the agricultural soils. From those 150, we identified 50 that were likely to have a protective effect against pathogens. Of the 50, we identified fourteen that can be cultivated in the lab.”

If we identify which chemicals are no longer released by the domesticated plants, we can try to breed those back into the plants.

Ramirez Villacis then demonstrated that adding these fourteen microbes to agricultural soil also boosts the resistance of potato plants to late blight infection. “We found that adding just this subset of lost microbes leads to an increase in resistance of about seventy percent of the effect seen in natural soils,” says Ramirez Villacis.

Missing functions

So could simply adding these microbes to farmland increase the resilience of potato plants to diseases? “We would like to do field trials to test this,” says Ramirez Villacis. “But in terms of a real world application, things get complicated: it is very difficult to register an agricultural product with more than two microbes, as regulators require detailed information on how each microbe interacts with the others. And with fourteen microbes, you have a very high number of interactions.”

But Ramirez Villacis and his colleagues have a plan. “By mapping the complete DNA of these microbes, which will tell us what genes they have, we want to gain insight into what these microbes exactly do in the soil. This will hopefully help us narrow it down to just two or three microbes that together do the same things as this collection of microbes.”

Plants regain control

Understanding the missing functions of these microbes also opens up other strategies for boosting plant resistance. “We could enrich the soil with prebiotics, compounds that promote the growth of beneficial microbes in the soil,” explains Ramirez Villacis. 

“Also, we need to understand what the plants themselves do to recruit and activate these functions. Domesticated crop plants release very few chemicals in the soil, which hampers their ability to attract and maintain a healthy microbiome. If we identify which chemicals are no longer released by the domesticated plants, we can try to breed those back into the plants. This will enable them to regain control of their own surroundings.”