Do plant growth promoting Streptomyces endophytes evolve into pathogens?

Context. Streptomyces bacteria are present in all soils and often enriched in the rhizosphere, i.e., the region of soil immediately surrounding plant roots. There are >1100 verified Streptomyces species but our work suggests only 2% of these enter plant roots and survive inside the endosphere, i.e. inside the roots. Ten of these endophyte species are pathogenic, including S. scabies, S. acidiscabies and S. turgidiscabies, and contain a pathogenicity island (PAI), while the rest are beneficial and receive food and housing in return for plant growth promoting (PGP) benefits, including defence against disease. This proposal is based on our discovery that a major PGP endophyte clade in wheat is closely related to pathogenic S. acidiscabies but lacks the PAI and protects plants against disease. We hypothesise that there is selective pressure for beneficial endophytes to evolve into pathogens by acquiring the PAI. This needs to be tested because, if correct, it could negate the use of PGP Streptomyces strains in agriculture. Challenge. Streptomyces plant pathogens cause common scab, which results in big economic losses to the potato industry worldwide. The origin of the Streptomyces PAI remains mysterious as it has not been identified in any other bacteria, but it is generally accepted that S. scabies was the first pathogen to arise, and the PAI spread from S. scabies to other species to give rise to pathogens such as S. acidiscabies and S. turgidiscabies. However, for reasons that have never been explained, not all Streptomyces species become pathogens when they acquire the PAI. We hypothesise that endophytes are more likely to become pathogens upon acquiring the PAI because they can already enter and colonise plant roots. Aims and Objectives. We used deep sequencing to identify three endophytic clades in wheat which, in order of abundance, are most closely related to S. turgidiscabies > S. acidiscabies > S. canus. We isolated and genome sequenced representative strains from the latter two clades but, despite extensive efforts, have been unable to culture the S. turgidiscabies clade suggesting it could be host dependent. Strikingly, the S. acidiscabies clade looks almost identical to the sequenced S. acidiscabies strains at the genome level but the endophytes do not contain the PAI and do not cause disease. Here we will test the following hypotheses: Endophytes all confer plant-growth promoting properties. The S.turgidiscabies endophyte clade is host dependent. Endophytes make antifungal compounds to protect wheat against Take-all. Endophytes are more likely to become pathogens after acquiring the PAI. Disrupting the att site in endophyte genomes prevents them acquiring the PAI. Deleting the S.acidiscabies PAI will convert it to a beneficial endophytic lifestyle. Potential applications and benefits. Numerous studies have shown that Streptomyces bacteria confer benefits to plants, including PGP through provision of nutrients such as iron and phosphate, and defence against disease. Indeed, we have shown that the endophytes related to S. acidiscabies protect wheat plants against the Take-all fungus, which is the most economically important disease of wheat in the UK and Western Europe. Streptomyces bacteria sporulate such that we can incorporate their spores into seed coatings so they colonise the plant roots after the seeds germinate. Here we will determine if all endophytes are beneficial compared to rhizosphere strains, if they are more likely to become pathogens and if we can block this adaptation through genome engineering.