Intersubspecific Recombination in Xylella fastidiosa Strains Native to the United States: Infection of Novel Hosts Associated with an Unsuccessful Invasion

Abstract

The bacterial pathogen Xylella fastidiosa infects xylem and causes disease in many plant species in the Americas. Different subspecies of this bacterium and different genotypes within subspecies infect different plant hosts, but the genetics of host adaptation are unknown. Here we examined the hypothesis that the introduction of novel genetic variation via intersubspecific homologous recombination (IHR) facilitates host shifts. We investigated IHR in 33 X. fastidiosa subsp. multiplex isolates previously identified as recombinant based on 8 loci (7 multilocus sequence typing [MLST] loci plus 1 locus). We found significant evidence of introgression from X. fastidiosa subsp. fastidiosa in 4 of the loci and, using published data, evidence of IHR in 6 of 9 additional loci. Our data showed that IHR regions in 2 of the 4 loci were inconsistent (12 mismatches) with X. fastidiosa subsp. fastidiosa alleles found in the United States but consistent with alleles from Central America. The other two loci were consistent with alleles from both regions. We propose that the recombinant forms all originated via genomewide recombination of one X. fastidiosa subsp. multiplex ancestor with one X. fastidiosa subsp. fastidiosa donor from Central America that was introduced into the United States but subsequently disappeared. Using all of the available data, 5 plant hosts of the recombinant types were identified, 3 of which also supported non-IHR X. fastidiosa subsp. multiplex, but 2 were unique to recombinant types from blueberry (7 isolates from Georgia, 3 from Florida); and blackberry (1 each from Florida and North Carolina), strongly supporting the hypothesis that IHR facilitated a host shift to blueberry and possibly blackberry.

Scientific Opinion on the risks to plant health posed byXylella fastidiosain the EU territory, with the identification and evaluation of risk reduction options

“…In this specific case, however, the use of the strain of subspecies fastidiosa being tested in the USA in the EU would represent the introduction of novel X. fastidiosa genetic diversity into the risk assessment area. This could be an important problem because of the very high rates of X. fastidiosa recombination rates in the field (Nunney et al, , 2014 and laboratory (Kung andAlmeida 2011, 2014); in other words, recombination between the genotype present in Apulia, Italy, and any novel genotype could lead to recombination and eventually the emergence of new diseases. Furthermore, the strategy of using avirulent strains to fight X. fastidiosa infections may be counterproductive, as changes in virulence or reversions of avirulent strains may occur through lateral gene transfer, a phenomenon well known to occur in X. fastidiosa (e.g.…”

“…It has been shown that the strain present in Italy is very homogeneous, and identical to a variant infecting oleander in Costa Rica. This also represents the first report of subspecies pauca in Costa Rica (Nunney et al, 2014). It was assigned a new sequence type (ST) profile, ST 53, and named CoDiRO for "Complesso del Disseccamento Rapido dell' Olivo".…”

“…• Central America and Caribbean: X. fastidiosa has been reported in Costa Rica (Nunney et al, 2014) and Mexico (Legendre et al, 2014). In addition it has been intercepted in consignments imported into Europe from Honduras (EUROPHYT, online).…”

“…A recent paper (Nunney et al, 2014) states that recombinations between X. fastidiosa strains, even if they are attributed to different subspecies, may be possible and may result in new strains with unpredictable characteristics. This should be further studied as it may greatly impact the risks associated with X. fastidiosa in terms of host range, association with vectors and severity of the disease.…”

“…There are no other records of this genotype, or reports of its occurrence. More recently, another subspecies has been proposed, subspecies morus, associated with isolates in the USA colonising mulberry (Nunney et al 2014b). This subspecies, proposed based on multilocus sequence typing (MLST) data, is recombinogenic with alleles from subspecies fastidiosa and multiplex (Nunney et al, 2014a).…”