Xanthomonas adaptation to common bean is associated with horizontal transfers of genes encoding TAL effectors

Abstract

Background: Common bacterial blight is a devastating bacterial disease of common bean (Phaseolus vulgaris) caused by Xanthomonas citri pv. fuscans and Xanthomonas phaseoli pv. phaseoli. These phylogenetically distant strains are able to cause similar symptoms on common bean, suggesting that they have acquired common genetic determinants of adaptation to common bean. Transcription Activator-Like (TAL) effectors are bacterial type III effectors that are able to induce the expression of host genes to promote infection or resistance. Their capacity to bind to a specific host DNA sequence suggests that they are potential candidates for host adaption.

Results: To study the diversity of tal genes from Xanthomonas strains responsible for common bacterial blight of bean, whole genome sequences of 17 strains representing the diversity of X. citri pv. fuscans and X. phaseoli pv. phaseoli were obtained by single molecule real time sequencing. Analysis of these genomes revealed the existence of four tal genes named tal23A, tal20F, tal18G and tal18H, respectively. While tal20F and tal18G were chromosomic, tal23A and tal18H were carried on plasmids and shared between phylogenetically distant strains, therefore suggesting recent horizontal transfers of these genes between X. citri pv. fuscans and X. phaseoli pv. phaseoli strains. Strikingly, tal23A was present in all strains studied, suggesting that it played an important role in adaptation to common bean. In silico predictions of TAL effectors targets in the common bean genome suggested that TAL effectors shared by X. citri pv. fuscans and X. phaseoli pv. phaseoli strains target the promoters of genes of similar functions. This could be a trace of convergent evolution among TAL effectors from different phylogenetic groups, and comforts the hypothesis that TAL effectors have been implied in the adaptation to common bean.

Conclusions: Altogether, our results favour a model where plasmidic TAL effectors are able to contribute to host adaptation by being horizontally transferred between distant lineages.

Keywords: Common bean; Horizontal gene transfer; Host adaptation; TAL effectors; Xanthomonas.

Fig. 1

Localisation of tal genes within the genomes of 17 strains responsible for CBB. Presence of the corresponding molecule is represented by shades of grey depending on the presence of the different tal genes (see legend). Chr.: Chromosome

Fig. 2

Alignment of the nine unique RVD sequences retrieved in TAL effectors from 17 strains responsible for CBB. TAL effectors that could be aligned are grouped together, indels are represented by black rectangles and putative substitutions are marked with grey colour

Fig. 3

Phylogeny of Xanthomonas strains and tal genes. Strains or tal genes from the X. citri pv. fuscans genetic lineages fuscans, NF2 and NF3 are indicated in red, X. phaseoli pv. phaseoli NF1 lineage in blue, X. citri pv. aurantifolii in pink and X. phaseoli pv. manihotis in purple. Ks values corresponding to the divergence of tal genes are indicated in the different trees using the same colours. a Phylogenetic tree representing the evolution of Xanthomonas strains constructed using CVtree on the whole proteome of strains. Numbers at node correspond to mean Ks values calculated on seven housekeeping genes. Vertical dotted lines represent time of tal gene divergence estimated by Ks values written above. The most parsimonious course of events for the evolution of tal genes is highlighted according to the legend. NA: Not applicable. b ML tree constructed on the nucleotide sequences of N-ter-encoding region of tal genes. c ML tree constructed on the nucleotide sequences of C-ter-encoding region of tal genes. For (b) and (c), bootstrap values greater than 50% are shown for 1000 replicates and horizontal scale bars represent number of nucleotide substitutions per site

Fig. 4

Distance trees of repeat regions or RVD sequences of TAL effectors. TAL effectors from the X. citri pv. fuscans genetic lineages fuscans, NF2 and NF3 are indicated in red, X. phaseoli pv. phaseoli NF1 lineage in blue, X. citri pv. aurantifolii in pink and X. phaseoli pv. manihotis in purple. a Phylogenetic classification of the repeat regions of TAL effectors constructed with the DisTAL program (Pérez-Quintero et al., 2015). Analysis was performed on amino acid sequences of the repeat region (excluding RVD) of TAL effectors from X. citri pv. fuscans, X. citri pv. aurantifolii, X. phaseoli pv. phaseoli and X. phaseoli pv. manihotis, using eight TAL effectors from X. translucens pv. undulosa XT4699 as outgroups. b Neighbour Joining tree representing the distance between RVD sequences, constructed using the FuncTAL program. Analysis was performed on the RVD sequences of TAL effectors from X. citri pv. fuscans, X. citri pv. aurantifolii, X. phaseoli pv. phaseoli and X. phaseoli pv. manihotis