The pathogenic fungus Verticillium dahliae, which causes wilt disease in many crops, secretes an ‘effector’ molecule that targets the microbiome of plants to encourage infection, according to a team of biologists.
The research was performed by the team of Alexander von Humboldt Professor Dr. Bart Thomma at the University of Cologne (UoC) within the framework of the Cluster of Excellence on Plant Sciences (CEPLAS) in collaboration with the team of Dr. Michael Seidl at the Theoretical Biology & Bioinformatics group of Utrecht University in the Netherlands.
The research, titled “An ancient antimicrobial protein co-opted by a fungal plant pathogen for in planta mycobiome manipulation,” was published in the Proceedings of the National Academy of Sciences (PNAS).
Scientists are rapidly recognizing that an organism’s microbiome, which includes all of the bacteria and other microorganisms that live in and on it, is a crucial part of its overall health. Microbes that live in the gut and on the skin have favorable impacts on humans and other animals.
This is also true for plants; additionally, it has been shown that plants can ‘recruit’ helpful bacteria from their environment, such as the soil surrounding their roots, to aid in disease resistance.
Dr. Thomma of the University of California theorized, in collaboration with Dr. Nick Snelders, the study’s lead author, that if plants can do it, infections may have ‘learned’ to disrupt this ‘call for help’ and disrupt the plant’s microbiome in order to promote invasion. As a result, these viruses can reduce immunity indirectly by altering the plant’s healthy microbiome, in addition to suppressing the plant host’s immune responses directly.
Verticillium dahliae is a well-known disease that affects a variety of plants, including greenhouse crops such as tomatoes and lettuce, as well as olive trees, ornamental trees and flowers, cotton, potatoes, and other plants. According to the findings, the fungus secretes the antimicrobial protein VdAMP3 as an effector to modify the plant’s microbiome.
In terms of evolution, the molecule that is secreted is very old. Homologs also occur in organisms that are not pathogenic on plants. It looks like Verticillium ‘used’ the molecule to ‘exploit’ it during the process of disease development on the host. Interestingly, the molecule does not act like a broad-spectrum antibiotic that targets any microbe, but specifically against ‘competitor’ fungi that have abilities to hinder Verticillium.
Dr. Bart Thomma
Effector molecules, in general, attack components of the host immune system, causing immunological suppression. The authors have now demonstrated that these targets include residents of the host’s microbiome: during host colonization, the VdAMP3 molecule suppresses beneficial organisms in the plant’s microbiome, causing microbiome disturbance or ‘dysbiosis,’ allowing the fungus to complete its life cycle and produce progeny that can spread and start new infections.
“In terms of evolution, the molecule that is secreted is very old. Homologs also occur in organisms that are not pathogenic on plants,” said Thomma. “It looks like Verticillium ‘used’ the molecule to ‘exploit’ it during the process of disease development on the host. Interestingly, the molecule does not act like a broad-spectrum antibiotic that targets any microbe, but specifically against ‘competitor’ fungi that have abilities to hinder Verticillium.”
The researchers were first interested in seeing if Verticilium has antibacterial ‘effectors’ in its arsenal. The capacity of various candidates to prevent the growth of test microorganisms in the laboratory was then investigated.
One of these probable candidates was VdAMP3. Other fungal antagonists could flourish and suppress the creation of Verticillium reproductive structures without the ‘effector,’ according to follow-up investigations. VdAMP3 is most active later in the disease’s progression when Verticillium has to build these new reproductive structures in order to infect new hosts.
However, this isn’t the first time the researchers have discovered such a chemical: a year ago, they discovered a molecule that works against bacterial competitors rather than competitive fungus, similar to VdAMP3.
“Together, these findings demonstrate that pathogens use various molecules at various stages of the disease process to manipulate the healthy microbiome of a host to cause disease. This shows that it is important to look beyond the “binary interaction” between a pathogen and a host if we want to understand the disease.”
“Rather, we must take the entire microbiome of the host into account as well, looking at the host as a “holobiont” the ecological unit formed by the host and all the organisms living in and on it,” Thomma added.
In the long run, a greater understanding of these mechanisms will aid in the development of more resilient plants and improved crop protection techniques. One of the key goals of plant scientists is to enhance the yield of field crops while minimizing our ecological footprint on the environment in the face of an increasing global population, limited farmland, and the need to reduce environmental damage and pollution.
“Learning more about these effector molecules that help pathogenic fungi infect crop plants may lead to new ways to safeguard against them,” said Snelders.
The authors hope to uncover more effector proteins with specific antimicrobial activity from Verticillium, as well as other pathogens with different infection tactics, in future studies.
“Unravelling how these molecules work, and how they can inhibit the one microbe while not affecting the other is important to discover novel mechanisms to target microbes, which may ultimately even lead to the development of novel antibiotics,” Snelders concluded.
The Cluster of Excellence on Plant Sciences (CEPLAS) is a joint initiative of Heinrich Heine University Düsseldorf (HHU), the University of Cologne (UoC), the Max Planck Institute for Plant Breeding Research Cologne (MPIPZ), and Forschungszentrum Jülich (FZJ). In CEPLAS, scientists are developing innovative strategies for sustainable plant production.
Thomma’s recently re-located working group from Wageningen University in the Netherlands to the UoC is focusing on identifying mechanisms that underpin the pathogenicity of fungi on plant hosts, thanks to generous funding from the Alexander von Humboldt foundation through an Alexander von Humboldt professorship.
Computational biology, bioinformatics, modeling, and big data are used by the Theoretical Biology & Bioinformatics group at Utrecht University in the Netherlands to address both basic and applied challenges in the life sciences.
The Fungal Evolutionary Genomics group of Dr. Seidl studies genome evolution and function in order to better understand how fungi evolve and adapt to novel or changing environments over short and long evolutionary periods.
