Does the fungus Botrytis cinerea break plants with a sledgehammer or a series of specialised tools?

The grey mould Botrytis cinerea gets its name from how it infects grapevines but can infect over four hundred different plants. How can it be so successful with so many diverse victims? Teruhiko Kuroyanagi and colleagues examined how Botrytis cinerea tackles some plant defence molecules, known as phytoalexins. Study of the genes involved in the fungal response indicates that Botrytis cinerea took these genes from a distant organism, allowing it to infect more species.

Phytoalexins are anti-microbial compounds produced by plants to tackle infections. They are toxic to the attacker and come in many different varieties. Any successful attacker must be able to disable the defences of the plant they’re attacking. However, while the attacker wants to undermine the plant’s defences, it only needs to tackle the few chemicals the plant is sending. Any attempt to combat chemical defences that the plant isn’t using is a waste of effort. So with so many possible defences, how does Botrytis cinerea produce the right tools? Kuroyanangi and colleagues found the answer in a gene called Bccpdh.

Bccpdh is a gene that gets upregulated by a chemical called capsidiol. This is a chemical used by tobacco plants for defence. Kuroyanangi and colleagues created mutant strains of Botrytis cinerea that had defective Bccpdh genes. They released these strains on tobacco as well as potato, tomato, grape, and eggplant. Only tobacco uses capsidiol for defence. The botanists found that the altered strains of Botrytis cinerea could not attack tobacco effectively but still had no trouble with the other plants. The results showed that Bccpdh was part of a tool kit Botrytis cinerea could use only when it needed to infect capsidiol-producing plants.

Kuroyanangi and colleagues searched to see which of Botrytis cinerea’s relatives also had the Bccpdh gene. The answer was none.

A blast search using BcCPDH as query sequence revealed that probable orthologs can be found only in some Pezizomycotina fungi belonging to Ascomycota. Orthologs were found from a taxonomically diverse range of fungal species, including animal and insect pathogens, and there was no correlation between their homology and taxonomic relationship, which might indicate multiple horizontal gene transfer events of the cpdh gene in the diversification of Ascomycota fungi.

Kuroyanagi et al. 2022

Now it has the Bccpdh gene, combined with its ability to detect what defences its host uses, Botrytis cinerea has expanded its range of victims. Additionally, Bccpdh is widely conserved in Botrytis cinerea, meaning that whatever strains of Botrytis cinerea you’re looking at, you’ll find that it has the Bccpdh gene, even if that strain is found not to be running through hosts where the gene would be useful. Kuroyanagi and colleagues write:

Despite capsidiol-producing plants representing only a small fraction of >400 host plants of B. cinerea, CPDH activity was maintained in all investigated B. cinerea strains isolated from plants that do not produce capsidiol. This may hint at the presence of a selection pressure against the loss of CPDH, despite it only affecting a limited number of host plants. This poses the question of whether B. cinerea is able to maintain acquired resistances for a prolonged time, which may explain how it evolved and established itself as the polyxenous pathogen that it is.

Kuroyanagi et al. 2022

READ THE ARTICLE

Kuroyanagi, T., Bulasag, A.S., Fukushima, K., Ashida, A., Suzuki, T., Tanaka, A., Camagna, M., Sato, I., Chiba, S., Ojika, M. and Takemoto, D. (2022) “Botrytis cinerea identifies host plants via the recognition of antifungal capsidiol to induce expression of a specific detoxification gene,” PNAS Nexus, 1(5). Available at: https://doi.org/10.1093/pnasnexus/pgac274.