Title Homologous recombination and xylella fastidiosa host-pathogen associations in South America Permalink

Homologous recombination affects the evolution of bacteria such as Xylella fastidiosa, a naturally competent plant pathogen that requires insect vectors for dispersal. This bacterial species is taxonomically divided into subspecies, with phylogenetic clusters within subspecies that are host specific. One subspecies, pauca, is primarily limited to South America, with the exception of recently reported strains in Europe and Costa Rica. Despite the economic importance of X. fastidiosa subsp. pauca in South America, little is known about its genetic diversity. Multilocus sequence typing (MLST) has previously identified six sequence types (ST) among plant samples collected in Brazil (both subsp. pauca and multiplex). Here, we report on a survey of X. fastidiosa genetic diversity (MLST based) performed in six regions in Brazil and two in Argentina, by sampling five different plant species. In addition to the six previously reported ST, seven new subsp. pauca and two new subsp. multiplex ST were identified. The presence of subsp. multiplex in South America is considered to be the consequence of a single introduction from its native range in North America more than 80 years ago. Different phylogenetic approaches clustered the South American ST into four groups, with strains infecting citrus (subsp. pauca); coffee and olive (subsp. pauca); coffee, hibiscus, and plum (subsp. pauca); and plum (subsp. multiplex). In areas where these different genetic clusters occurred sympatrically, we found evidence of homologous recombination in the form of bidirectional allelic exchange between subspp. pauca and multiplex. In fact, the only strain of subsp. pauca isolated from a plum host had an allele that originated from subsp. multiplex. These signatures of bidirectional homologous recombination between endemic and introduced ST indicate that gene flow occurs in short evolutionary time frames in X. fastidiosa, despite the ecological isolation (i.e., host plant species) of genotypes. Understanding the drivers associated with emerging diseases is of paramount importance in the development of risk reduction strategies. Long-distance dispersal mediated by anthropogenic activities, land use changes, abiotic or biotic modifications affecting host biology or ecology, pathogen evolution, as well as other factors such as climate alterations all have been shown to drive emergence of animal, plant, and human diseases (Daszak et al. 2000; Hacker and Carniel 2001;Hufbauer et al. 2012;Murray andDaszak2013). Within this context, however, the emergence of diseases caused by related pathogens is usually associated with a limited number of drivers. For example, flu pandemics are linked to virus reassortments (Garten et al. 2009) and birdmigrations (Verhagen et al. 2015), while land use and climate change affect the occurrence of Lyme disease in North America (Simon et al. 2014). Therefore, broadly observed patterns serve as starting points when evaluating factors associated with emerging diseases caused by related pathogens. Quantitative analyses of databases and published literature have provided important insights on factors, as well as pathogen groups and potential geographical hotspots, associated with emerging animal and human diseases (Murray et al. 2015). Avery limited number of similar studies are available for plants (Anderson et al. 2004) but plant diseases emerge due to a variety of factors, from breakdown of host plant resistance via pathogen adaptation (Croll and McDonald 2012) to the introduction of new insect vectors (Almeida and Nunney 2015). The bacterium Xylella fastidiosa is the etiological agent of some of the most important plant diseases that have emerged during the last few decades. Epidemics of X. fastidiosa have been associated with long-distance introductions, geographical expansion of an invasive vector, as well as host adaptation possibly, via homologous recombination (Almeida and Nunney 2015). Significant advances in the understanding of ecological and evolutionary processes associatedwithX. fastidiosa epidemics have been recently obtained after the advent of a public multilocus sequence typing (MLST) database, a repository of sequence data for most of the known X. fastidiosa diversity (Scally et al. 2005; Schuenzel et al. 2005; Yuan et al. 2010). Currently, there are five X. fastidiosa subspecies, largely based on DNA-DNA hybridization and MLST data (Almeida and Nunney 2015). Recent data based on field surveys and experimental research have shown that, within subspecies, there is host–pathogen specificity, especially when symptoms are concerned (Almeida et al. 2008; Harris and Balci 2015; Nunney et al. 2013). Within X. fastidiosa subsp. pauca, specifically, cross inoculation of citrusand coffee-infecting isolates, which are genetically distinct, does not lead to disease even under greenhouse conditions (Almeida et al. 2008). X. fastidiosa is naturally competent, with high homologous recombination rates being achieved under laboratory conditions (Kung and Almeida 2011) as well as in the field (Nunney et al. 2013). Because recombination affects phylogenetic analyses, a general understanding ofX. fastidiosa genetic diversity has not been available until recently. The case of the apparently recombinogenic origin of a genotype infectingmulberry (X. fastidiosa subsp.morus) (Nunney et al. 2014b), and similar but less dramatic gene flow Corresponding author: H. D. Coletta-Filho; E-mail address: helvecio@centrodecitricultura.br *The e-Xtra logo stands for “electronic extra” and indicates that four supplementary tables are published online. © 2017 The American Phytopathological Society Vol. 107, No. 3, 2017 305 Phytopathology • 2017 • 107:305-312 • http://dx.doi. org/10.1094/PHYTO-09-16-0321-R