Population Genomic Analysis of a Bacterial Plant Pathogen: Novel Insight into the Origin of Pierce's Disease of Grapevine in the U.S.

Abstract

Invasive diseases present an increasing problem worldwide; however, genomic techniques are now available to investigate the timing and geographical origin of such introductions. We employed genomic techniques to demonstrate that the bacterial pathogen causing Pierce's disease of grapevine (PD) is not native to the US as previously assumed, but descended from a single genotype introduced from Central America. PD has posed a serious threat to the US wine industry ever since its first outbreak in Anaheim, California in the 1880s and continues to inhibit grape cultivation in a large area of the country. It is caused by infection of xylem vessels by the bacterium Xylella fastidiosa subsp. fastidiosa, a genetically distinct subspecies at least 15,000 years old. We present five independent kinds of evidence that strongly support our invasion hypothesis: 1) a genome-wide lack of genetic variability in X. fastidiosa subsp. fastidiosa found in the US, consistent with a recent common ancestor; 2) evidence for historical allopatry of the North American subspecies X. fastidiosa subsp. multiplex and X. fastidiosa subsp. fastidiosa; 3) evidence that X. fastidiosa subsp. fastidiosa evolved in a more tropical climate than X. fastidiosa subsp. multiplex; 4) much greater genetic variability in the proposed source population in Central America, variation within which the US genotypes are phylogenetically nested; and 5) the circumstantial evidence of importation of known hosts (coffee plants) from Central America directly into southern California just prior to the first known outbreak of the disease. The lack of genetic variation in X. fastidiosa subsp. fastidiosa in the US suggests that preventing additional introductions is important since new genetic variation may undermine PD control measures, or may lead to infection of other crop plants through the creation of novel genotypes via inter-subspecific recombination. In general, geographically mixing of previously isolated subspecies should be avoided.

Genomic Insights into Xylella fastidiosa Interactions with Plant and Insect Hosts

“…However, as discussed later, the distribution of individual subspecies is more limited, suggesting that geographical isolation has been important in the evolution of this bacterium. Furthermore, as with grapevine isolates in Taiwan, evidence indicates that at least some isolates causing disease in plum in Brazil originated from North America (Nunes et al 2003) and that grapevine isolates in the United States originated from Central America (Nunney et al 2010). Therefore, X. fastidiosa populations appeared to have remained largely isolated due to geographical barriers, but recent human activity has resulted in dispersal over continental distances.…”

“…X. fastidiosa is currently subdivided into four subspecies, largely based on DNA-DNA hybridization and multi-locus sequence typing data (Scally et al 2005;Schaad et al 2004). Although these groupings are phylogenetically robust, they can be further subdivided into groups with well-supported genetic and biological distinctions (i.e., different host ranges) (e.g., Almeida and Purcell 2003b;Almeida et al 2008;Nunney et al 2010Nunney et al , 2013. The taxonomy of X. fastidiosa is discussed in detail later within an evolutionary context.…”

“…fastidiosa isolates from Costa Rica colonizing various plant species have more allelic diversity than those causing disease in grapevines in the United States (Nunney et al 2010). These results suggest that Pierce's disease in the United States was introduced from Central America.…”

“…Both the coffee and citrus isolates of subspecies pauca appear to have acquired alleles from subspecies multiplex (Nunney et al 2012). Likewise, subspecies multiplex has participated in recombination with subspecies fastidiosa (Nunney et al 2010;Kung et al 2013). This process of allele conversion has even gone as far as to produce new lineages with roughly equal contributions from subsp.…”

Natural Competence Rates Are Variable Among Xylella fastidiosa Strains and Homologous Recombination Occurs In Vitro Between Subspecies fastidiosa and multiplex

“…However, host plant specificity has been described between and within subspecies Almeida et al 2008;Harris and Balci 2015;Oliver et al 2014Oliver et al , 2015. Subspecies were believed to be geographically separated, but dissemination of plant materials and insect vectors has led to coexistence of two or more subspecies in the same geographic location (Chen et al 2005;Nunney et al 2010Nunney et al , 2014bParker et al 2012).…”