New insights in belowground drivers of plant performance
Plants interact with a myriad of soil organisms ranging from microscopic bacteria, protists and fungi to animals such as nematodes, micro-arthropods and earthworms. When it comes to plant performance, these soil communities contain both many good and many bad guys. Plants affect the composition of this belowground biodiversity, and in turn soil organisms affect plant performance. This multi-directional process is called ‘plant-soil feedback’, and acts on a plant species-specific level. Because each plant species has its own unique set of root properties, each plant species develops a specific community of organisms in the soil surrounding its roots. In turn, these soil communities have specific effects on plant performance. The ratio between good and bad guys in a plant’s rhizosphere soil will determine whether its plant-soil feedback is positive, neutral or negative. This direction of the plant-soil feedback is a good indicator of a plant’s ability to persist at a certain spot for multiple generations. Therefore, plant-soil feedbacks are important for natural dynamics in vegetation, which is the main reason why we are interested in studying them.
Obvious examples of negative plant-soil feedbacks are found in agricultural fields, where monocultures of crops typically enrich the bad guys in the soil. Root-feeding nematodes, for example, are well known to diminish yield of potatoes and other crop species. Because soil organisms that harm one crop do not always harm others, crops are rotated over the years. At the other side of the spectrum, late-successional vegetation types, such as forests and heathlands, are stabilized by the presence of many good guys – in these cases mainly mycorrhizal fungi - in the soils. Yet, while such extreme opposites in plant-soil feedbacks are well-known, we often fail to explain variation in plant-soil feedbacks we observe in natural systems.
A new approach
In attempts to unravel general drivers of plant-soil feedbacks, research (including our own work) often focusses on very diverse sets of plant species, including many different plant families. Such approaches have resulted in important findings, such as that rare plant species often have more negative plant-soil feedbacks than common plant species. However, the drawback of these wide-range species selections may be that there is simply too much variation to identify plant traits and soil organisms that underlie plant-soil feedback effects. Because we were frustrated with the limited mechanistic insights we got from these studies, we used an alternative approach. In a new study we tried to minimize the diversity in both plant traits and soil communities by studying plant-soil feedbacks of eight very closely related plant species all belonging to the herbaceous plant genus Geranium (Figure 1).
Using DNA-based sequencing techniques we studied how soil communities developed in the soil under each of these eight plant species, and linked this to the performance of a new generation of the same plant species in these soils. We firstly could show that all of these plant species develop negative plant-soil feedbacks, but some more strongly than others (Figure 2). The next step was to identify the organisms driving this plant-soil feedback variation. The overall dissimilarity in the communities of fungi, protists and nematodes between the plants did not give any clue about which organismal group may be behind the observed effects. When we took a more detailed look, however, the abundances of root-feeding nematodes popped up as a predictor of plant performance. A close-up of the nematode DNA-sequences showed that one particular nematode dominated the root-feeding nematode communities – the root-knot nematode Meloidogyne hapla (Figure 3). This nematode species is a close relative of some of the most detrimental nematode-pests in agriculture. While we often used it as a model species for other root-feeding nematodes, we never expected that it would potentially be a key player in plant-soil feedbacks of non-crop species.
Because of our research experience with this Meloidogyne species, we set up a nematode reproduction experiment in which we found that the plant species that accumulated the highest abundances of root-feeding nematodes in the field soils indeed were the best hosts for this particular nematode species. While this still does not prove a causal relationship between root-feeding nematode numbers and plant performance, we are confident that root-feeding nematodes play an important role in plant-soil feedbacks in natural ecosystems.
With our set-up we could also answer the question whether the most closely related plant species develop the most similar soil communities and plant-soil feedbacks. This appeared not to be the case at all. Rather than taxonomic relatedness, the dissimilarity in root traits best predicted how much the soil communities differed between plant species. This was fascinating, given that the two most closely related plant species are almost identical in aboveground appearance. Yet, appearances can be deceiving, as these two plant species did differ a lot in root structure and chemistry, and therefore in their plant-soil feedbacks as well. Altogether, our study shows that it is important to look at many details at the same time to understand what is really happening belowground.
Wilschut, R.A., Putten, W.H. Van Der, Kulkarni, P., Martens, H., Geisen, S., Garbeva, P., Harkes, P., 2019. Root traits and belowground herbivores relate to plant-soil feedback variation among congeners. Nature Communications. doi:10.1038/s41467-019-09615-x