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Symbiosis Report Summary

Project ID: 656853
Funded under: H2020-EU.1.3.2.

Periodic Reporting for period 1 - Symbiosis (Bacterial leaf symbiosis: what environmental factors influence it and does it drive host plant speciation)

Reporting period: 2016-01-01 to 2017-12-31

Summary of the context and overall objectives of the project

Virtually all plants interact with endosymbiotic microorganisms that inhabit various plant organs. In general, plant-bacteria interactions can be beneficial, neutral, or detrimental to the host and may play a larger role in host fitness and survival. If a form of bacterial symbiosis beneficial to the plant partner is established, the fitness of the host plant can be improved by promoting growth through, among others, increased nutrient acquisition, by enhancing plant defence by means of secondary metabolites, or by other forms of antagonistic competition. It is known that associating with bacteria can be a trigger for adaptive radiation and the establishment of new species. This project’s overall goal is to investigate the long-term effect of symbiosis on diversification patterns. Over the course of million years, did plant-bacteria interactions contribute to the establishment of the current biodiversity on our planet?
Specifically, in this project, we study a particular plant-bacteria interaction that is found in the Rubiaceae plant family (or coffee family) where several of its tropical lineages harbour non- pathological endophytic bacteria in their leaves. This specific form of interaction is currently known from hundreds of species in eight genera (around 5% of the species in the family). The current hypothesis regarding the function of this symbiosis is that the endophytes are involved in the biosynthesis of secondary metabolites that provide the host plants with chemical protection against herbivory. If bacterial leaf endophytes indeed provide their hosts with a short-term beneficial effect, they may be able to increase the evolutionary potential of their hosts, which will in turn be reflected in the long-term diversification rates. Because closely related plant species with and without endophytes exist, we are able to compare them to each other and investigate if associating with endophytes influences host plant evolution.

A first objective was to elucidate the likely origin in time of bacterial leaf symbiosis, which indicated when the interaction has been established. A second objective was to investigate whether the presence of endophytes had an impact on the diversification rates of the host plants because the hypothesis is that lineages with endophytes will have deviating diversification rates as a result of the symbiosis.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The hypothesis that interacting with bacterial endophytes influences host plant evolution over long time spans can only be tested by making use of genetic data. The first step is therefore obtaining and gathering this kind of data. The plants we are studying belong to the Vanguerieae tribe within the Rubiaceae or coffee family, and there are around 600 species distributed in the Old World tropics. Of these species, around one third is known to interact with bacterial endophytes, while the other two thirds lack them. The species that possess the symbiosis are restricted to the African tropics and subtropics and we therefore focussed on those species for our sampling. Silica-dried material was already collected during field-work prior to the start of this project and genetic sequence data was obtained from own previous work, other collaborators and newly obtained. Because the inter-species relationships within the tribe are still insufficiently known, in-depth phylogenetic analyses were performed. This enabled us to present a complete overview of the tribe and we even described and published a new genus endemic to South Africa. The next step was to ascertain which of the +600 species within the tribe are associated with bacterial leaf symbiosis and establish when in time this symbiosis has its origin. This was done by performing divergence time analyses and we found that the symbiosis originated in the Late Miocene, a period that started around 11 million years ago. This period coincides with a global cooling and the aridification of Africa. The rainforests that covered the continent gradually made way for more open landscapes such as savannahs. Within these habitats, different types of herbivores evolved and this nicely links with the presumed function of bacterial leaf symbiosis, which is providing chemical defence. If a short-term benefit of leaf symbiosis exists, it is likely to assume that the long-term evolution of the host plants is influenced as well. To test this, diversification rate analyses were performed and indeed, we found diverging evolutionary rates between plants with versus without endophytes. Plants that engage in a symbiotic relationship with endophytic bacteria tend to evolve faster than plants without symbiosis. These results were published in a paper and it confirms the general hypothesis that close interactions between different organisms have a major impact on the evolution of the partners involved.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

One of the main missions of systematic botany is to document the plant diversity on Earth. This responsibility is not to be underestimated and it is a crucial task if we want to safeguard the natural world. We are proud and honoured that this project made as small but valuable contribution to this mammoth task. Although the objectives were quite specific, they can be seen as part of investigating how evolution works in general. Species evolve naturally but biotic interactions with other organisms have a large influence of evolution as well. And it is not only about the obvious interaction between different plants, but even the smallest of organisms such as bacterial endophytes can be a major driver of host plant evolution. This project therefore shows that interactions between plants and other organisms should be taken into account during evolutionary studies, which, with perhaps the exception of associations involved in pollination and seed dispersal, is not the current practice. From a more applied perspective, it is conceivable that biotechnological applications of plant-bacteria interactions can be numerous (e.g., sustainable agriculture through biocontrol and biofertilization). To date, research efforts are mainly focussing on the molecular mechanisms involved in known microbial endosymbiosis and the direct application of plant-bacteria interactions. The specific and special leaf symbiosis within certain Rubiaceae plants is however largely unknown and less explored. We are only beginning to understand this peculiar symbiosis, but if the bacterial endophytes indeed play a crucial role in chemical plants defence, exciting agricultural or industrial applications can be foreseen for the future.

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