Population dynamics of Xylella fastidiosa subsp. pauca indicate that coffee strains are the founding populations for the olive-Xylella infections in Brazil

Xylella fastidiosa subsp. pauca (X.f. pauca) is a multi-host pathogen responsible for significant disease outbreaks in the agro-ecosystem worldwide. In Brazil, the species causes severe economic losses in coffee and sweet orange productions and was recently identified as causing the olive quick syndrome decline (OQSD), a newly emerging disease. We lack information on the evolutionary potential of this new olive-infecting population, and its relationship with established populations from other hosts. We showed that X.f. pauca strains were widely spread through olive orchards and 75% of the diseased plants were infected by a single sequence type (ST16) that was firstly reported infecting coffee orchards. Based on the epidemiological characteristics of X.f. pauca and its ancient infections in coffee plants in Brazil, we then hypothesized that coffee populations are the source of inoculum of X.f. pauca for olive trees under natural conditions. To test this hypothesis, we analyzed the genetic diversity and population dynamics of all 584 isolates (n=82 from olive, n=170 from coffee, and n=237 from citrus) of X.f. pauca using 12 microsatellites (SSR) loci. We observed that the coffee-infecting population had the highest genetic diversity and lowest clonal fraction among the three hosts. Based on a discriminant analysis of principal components and Bayesian clustering analysis, we found evidence for two major genetic groups of isolates. The first group is formed by isolates from olive and coffee and the second and more distant by isolates from citrus. A minimum spanning network analysis provided further evidence for the proximity between olive and coffee populations, maintaining citrus haplotypes further isolated. Coffee and olive crops occur sympatrically in São Paulo and Minas Gerais states, which may favor the exchange of the genetic material between these two hosts. Our results corroborate the importance of monitoring the population structure of multi-host pathogens to elaborate strategies for pathogen control and reduction of pathogen transmission. 
Support: Horizon 2020 (XF Actors 727987), Fapesp (Proc. 2016/02176-7)