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Determinants of Xylella fastidiosa host specificity

The plant pathogen Xylella fastidiosa has a large host range with 563 plant species reported (3). Only few plant species tested have proved to be inadequate as hosts both under experimental conditions and in the field (9). However, for most host plant species, X. fastidiosa does not cause disease (9). Thus, colonization does not necessarily equal disease. Importantly, the minimal genomic diversity of X. fastidiosa availablesuggests that different phylogenetic groups have similar pathogenicity mechanisms. Despite its importance as a plant pathogen, there are no hypotheses on the determinants of X. fastidiosa host specificity. This project aims to address this very important knowledge gap.

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Xylella fastidiosa​ infected olive trees in Apulia

Context of the project

The phytobacterium Xylella fastidiosa poses a serious threat to agriculture in Europe and especially across the Mediterranean basin. Since it was first reported in 2013 in Apulia, Italy (11) where it is devastating olive orchards, several other cases have also been reported in France, Germany and Spain (1, 2, 6, 8, 10). Although X. fastidiosa infected plant species have been eradicated in Germany, this is far from being the case in some regions from the three other countries which have officially been declared as being areas under containment (Corsica, France; Balearic Islands, Spain; Southern Apulia, Italy) (3). While strains from two and three different subspecies have been found infecting 36 and 18 plant species respectively in France (Corsica and PACA) and in Spain (Balearic Islands and mainland Spain) pointing towards several introductions into these two countries, only one genotype belonging to X. fastidiosa subsp. pauca has been found in Italy. This strain has been shown to infect 31 plant species from different plant orders (3). Olive trees are the main crop affected in this olive-growing region raising major economic, social and political concerns.

The host range of a given X. fastidiosa strain remains completely unpredictable (12) making the monitoring of plant species at risk quite difficult in the affected areas. This project thus aims at determining the genetic basis of X. fastidiosa host specificity by studying the recent adaptation of this bacterium to olive trees in Italy.

Ongoing Work

Since the outbreak and up to 2017, 74 isolates from olive trees have been sampled across the infected area and their whole genome has been sequenced. We have found less than 320 single nucleotide polymorphisms (SNPs) when comparing the whole genome sequence of these isolates to the reference Apulian strain De Donno (4); further confirming that a single introduction is at the origin of this outbreak in Italy. Furthermore, when reconstructing a phylogenetic tree of X. fastidiosa subsp. pauca strains, we have found that three isolates from Costa Rica, COF0407, OLS0479 and OLS0478 were genetically closely related to the Apulian strains – as already described using MLST data in (5, 7).

This result has led us to further compare all of the Apulian isolates to the Costa Rican strain isolated from Coffea sp. Two different approaches are being used for this purpose and have thus far enabled us to identify a few genes of interest. In parallel, we are looking at the genes under positive selection pressure in this data set. By using these different approaches, we are hoping to determine a small list of genes that could be involved in the adaptation of this bacterium to olive trees.

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Geographic and genetic distribution of Xylella fastidiosa isolates collected between 2014 in 2017 from infected olive trees in Apulia, Italy

Future directions

These genes are going to be further studied to determine whether they are indeed involved in X. fastidiosa adaptation to olive trees. 

In parallel, we are testing the presence of temporal signal in the data set to date the introduction of X. fastidiosa in Italy.

This work should thus help us better understand the epidemics of this phytopathogen in Italy.  This is the first comprehensive study which aims at tackling the long-lasting question of the determinants of X. fastidiosa host specificity.

References

1. Auricoste J, Claquin P, Denancé N, Jacques M-A, de Jerphanion P, et al. 2017. Xylella fastidiosa en Francia en ornamentales y otras especies. In Enfermedades causadas por la bacteria Xylella fastidiosa, pp. 211–29. Cajamar Caja Rural ed.

2. Denancé N, Legendre B, Briand M, Olivier V, de Boisseson C, et al. 2017. Several subspecies and sequence types are associated with the emergence of Xylella fastidiosa in natural settings in France. Plant Pathology. 66(7):1054–64

3. EFSA Panel on Plant Health (EFSA PLH Panel), Jeger M, Caffier D, Candresse T, Chatzivassiliou E, et al. 2018. Updated pest categorisation of Xylella fastidiosa. EFSA Journal. 16(7)

4. Giampetruzzi A, Saponari M, Almeida RP, Essakhi S, Boscia D, et al. 2017. Complete genome sequence of the olive-infecting strain Xylella fastidiosa subsp. pauca De Donno. Genome announcements. 5(27):e00569–17

5. Giampetruzzi A, Saponari M, Loconsole G, Boscia D, Savino VN, et al. 2017. Genome-wide analysis provides evidence on the genetic relatedness of the emergent Xylella fastidiosa genotype in Italy to isolates from Central America. Phytopathology. 107(7):816–27

6. https://gd.eppo.int/taxon/XYLEFA/distribution

7. Marcelletti S, Scortichini M. 2016. Xylella fastidiosa CoDiRO strain associated with the olive quick decline syndrome in southern Italy belongs to a clonal complex of the subspecies pauca that evolved in Central America. Microbiology. 162(12):2087–98

8. Olmo D, Nieto A, Borràs D, Montesinos M, Adrover F, et al. 2017. X. fastidiosa en las Islas Baleares. In Enfermedades causadas por la bacteria Xylella fastidiosa, pp. 231–61. Cajamar Caja Rural ed.

9. Purcell AH, Saunders SR. 1999. Fate of Pierce’s Disease Strains of Xylella fastidiosa in Common Riparian Plants in California. Plant Disease. 83(9):825–30

10. Roselló M, Ferrer A, Peris-Peris C, Llopis, JM, Rallo, E, et al. 2017. Xylella fastidiosa en la Comunidad Valenciana. In Enfermedades causadas por la bacteria Xylella fastidiosa, pp. 263–76. Cajamar Caja Rural ed.

11. Saponari M, Boscia D, Nigro F, Martelli GP. 2013. Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (southern Italy). Journal of Plant Pathology. 95:668

12. Sicard A, Zeilinger AR, Vanhove M, Schartel TE, Beal DJ, et al. 2018. Xylella fastidiosa : Insights into an Emerging Plant Pathogen. Annual Review of Phytopathology. 56(1)
   
Acknowledgment
This project is funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 707013.