PHYTOPHONUS · From male-killers to plant pathogens: Investigation of cross-kingdom host-symbiont interactions in the Arsenophonus clade”

From male-killers to plant pathogens: Investigation of cross-kingdom host-symbiont interactions in the Arsenophonus clade”

Bacterial symbionts are ubiquitous and influential partners of all metazoan life forms, including humans. In insects, this is exemplified by a high number of species harbouring heritable bacterial symbionts which provide important services to their hosts (e.g. nutrients or protection against pathogens). After millions of years of co-evolution, these bacteria are specifically adapted to living inside their host and often can no longer survive on their own. In addition, numerous insect species are vectors of plant-pathogenic bacteria, which cause devastating crop diseases and important economic losses. The insect vectors are generally hemipteran insects (e.g. leafhoppers, planthoppers or psyllids), which acquire and transmit the bacteria while feeding on plants. It is thus evident that certain bacteria have evolved adaptations to very different host environments from two kingdoms of life and are able to switch frequently between these contrasting lifestyles. However, a detailed understanding of the adaptations allowing an insect symbiont to become a plant pathogen is still lacking, due to the scarcity of bacterial model organisms at the early stages of transition from a purely insect-associated to a multi-host lifestyle. The project PHYTOPHONUS investigated the genomic adaptations allowing an initially insect-associated bacterial symbiont to successfully switch between insect and plant hosts and to become a plant pathogen. This was achieved using the phytopathogenic strain ‘Candidatus Phlomobacter fragariae’ belonging to the widespread Arsenophonus clade of insect symbionts as a model system. Despite being firmly established as insect symbionts, two different strains belonging to the clade have become insect-vectored plant pathogens, causing either Marginal Chlorosis Disease of strawberry or the disease “basses richesses” (=low sugar content) of sugar beet. In both cases, the bacteria are vectored by planthoppers and accumulate in the plant phloem, ultimately causing yellows, necrosis and plant death. Considering that both diseases first appeared less than 30 years ago and to date have only been observed in restricted and disconnected localities (France, Italy and Japan), it can be assumed (a) that the switch from an ancestral, purely insect-associated, to a multi-host lifestyle occurred very recently and (b) that it occurred independently multiple times within the Arsenophonus clade. These symbionts therefore represent outstanding model systems to investigate bacterial adaptations and cross-kingdom host interactions at the early stages of transition towards an insect-vectored phytopathogen. The specific objectives within this project were: (i) to test whether the ability of ‘Ca. P. fragariae’ to infect plant tissues was achieved via genomic adaptations compared to other Arsenophonus strains or whether the genetic repertoire of this clade is sufficiently versatile to allow rapid adaptations to plant hosts; (ii) to investigate the symbiotic interactions of ‘Ca. P. fragariae’ with both its insect and plant hosts and their respective microbiomes, thereby providing a holistic picture of this multi-partite relationship.

Data: CORDIS, © European Union