I’ve been tackling a problem. Every so often I get asked “What is botany?” It’s simple enough to answer, it’s the science of plants – but it’s not a very satisfying answer. There are botanists who work with plants, but there are many more who work with cells, or pathogens or whole ecosystems. Botanists have to be able to work with much more than plants. It might be better to say that botany is a science that starts with plants. A paper has come out recently that nicely illustrates this. Molecular networks in plant-pathogen holobiont by Nobori, Mine and Tsuda introduced me to a new word that captures some of this – holobiont.
What is a holobiont?
We need to start with symbiosis. Symbiosis describes a relationship between two or more organisms. For botanists, an obvious example is the symbiosis between mycorrhizal fungi and plants. Fungi associate with the roots of plants. They pass along nutrients like nitrogen and phosphorus and the plants in return pass along sugars to the fungi. By exchanging resources, the two organisms both benefit from the relationship. The two organisms are symbionts, and the whole is a holobiont.
It’s not just mutual symbiosis that creates a holobiont. Bordenstein and Theis define a holobiont as “every macrobe and its numerous microbial associates”. That would include parasites and pathogens. It might seem quite a wide definition. Pitlik and Koren state: “All humans, animals, and plants are holobionts.” If that’s the case, then what does the word holobiont tell us?
The difference between a holobiont and a collection of organisms
The reason a holobiont is a useful concept isn’t just that an organism lives with other organisms, it’s also about the nature of an interaction between them. When a cow eats grass, they aren’t a holobiont because – beyond one eating the other – there’s not much interaction going on. In their paper, Nobori and colleagues show there’s something different going on between plants and pathogens.
Some microbes see plants as a target. They’re a resource to be plundered to enable reproduction. Plants would rather that didn’t happen. So when a pathogen attacks then the plant cells release phytohormones to call for help. That’s no good for the pathogen, so pathogens send their signals into the plant to confuse or confound the plant’s ability to respond to the attack. It’s a useful tool to trigger when you find something to attack. What Nobori et al.’s paper notes is plants aren’t passive when this happens.
One of the pivotal features of a pathogen attack is Quorum Sensing, often abbreviated to QS. When bacteria start an attack, they’ll release chemical signals. These signals allow bacteria to ‘talk’ to each other. Even if a bacterium isn’t sensing an opportunity itself if enough other bacteria are, then it starts producing the tools it needs to attack. Quorum sensing allows bacteria to take the advantage when attacking before the plant can respond.
Nobori’s team notes that when plants release salicyclic acid (SA) and γ-aminobutyric acid (GABA), the chemicals can trigger a quorum-quenching system is some pathogens like Agrobacterium tumefaciens. They also discuss how pattern-triggered immunity by the plants can reduce the ability of Type Three Effectors deployed by bacteria to inject target cells with proteins. Break systems like this and you reduce the virulence of the attacker.
A holobiont as a unit of shared resources?
For Nobiri and colleagues, the existence of a holobiont doesn’t diminish the idea that plants and pathogens evolve. In fact, they argue that both would very much like to have their own molecular signalling networks. However, they’d also both like to interfere with each other’s signalling. The result is that the two parties effectively create a supernetwork that they fight for control over. Instead of two signalling networks there becomes one, unwillingly shared between the attacker and defender.
The idea of sharing also comes out in a Tansley review by Vandenkoornhuyse et al. They argue: “plant microbiota can be seen as a facilitator component providing additional genes to the host, which are involved in the adjustment to local environmental conditions.” It means when you study the plant in the wild you do not see just the plant, but also the result of the many interactions the plant has had with local microbiota.
This kind of cross-talk is a hot topic at the moment. One of the recent papers that got a lot of attention on Twitter was Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes by Cai et al. Cai and colleagues found that plants or at least Arabidopsis thaliana can reduce the virulence of an attacker, or Botrytis cinerea at least, by sending small RNAs (sRNAs) in exosomes. This follows plenty of work by people finding that sRNAs are produced by pathogens to interfere with plants. So RNA is used on both sides to part of a fight. However, neither Cai et al. (2018), Weiberg and Jin (2015) nor Wang et al (2016), use the holobiont concept.
I can see why. Those authors are all interested in the plant-pathogen battle. If you’re studying something where one side is trying to kill the other, it’s quite a leap to look at them through a lens of symbiosis. However, I do wonder if understanding plant-microbe communication in a broader context as a holobiont could suggest new approaches for studying plant-pathogen conflict. This context is what I like about Nobiri et al.’s paper. It adds context to other people’s work. If the holobiont idea proves successful, then it doesn’t wipe out or negate other work, but it does mean that previous work relates to other research in ways that it didn’t before.
Nobori, T., Mine, A., & Tsuda, K. (2018). Molecular networks in plant-pathogen holobiont. FEBS Letters. https://doi.org/10.1002/1873-3468.13071
Bordenstein, S. R., & Theis, K. R. (2015). Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes. PLOS Biology, 13(8), e1002226. https://doi.org/10.1371/journal.pbio.1002226
Pitlik, S. D., & Koren, O. (2017). How holobionts get sick—toward a unifying scheme of disease. Microbiome, 5(1). https://doi.org/10.1186/s40168-017-0281-7
Introduction to Phytohormones. (2010). The Plant Cell, 22(3), tpc.110.tt0310–tpc.110.tt0310. https://doi.org/10.1105/tpc.110.tt0310
Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., & Dufresne, A. (2015). The importance of the microbiome of the plant holobiont. New Phytologist, 206(4), 1196–1206. https://doi.org/10.1111/nph.13312
Cai, Q., Qiao, L., Wang, M., He, B., Lin, F.-M., Palmquist, J., … Jin, H. (2018). Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science, eaar4142. https://doi.org/10.1126/science.aar4142
Edgar, J. R. (2016). Q&A: What are exosomes, exactly? BMC Biology, 14(1). https://doi.org/10.1186/s12915-016-0268-z
Weiberg, A., & Jin, H. (2015). Small RNAs—the secret agents in the plant–pathogen interactions. Current Opinion in Plant Biology, 26, 87–94. https://doi.org/10.1016/j.pbi.2015.05.033
Wang, M., Weiberg, A., Lin, F.-M., Thomma, B. P. H. J., Huang, H.-D., & Jin, H. (2016). Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nature Plants, 2(10), 16151. https://doi.org/10.1038/nplants.2016.151