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. 2011 Dec;192(4):976-987.
doi: 10.1111/j.1469-8137.2011.03854.x. Epub 2011 Sep 8.

Functional diversification of the GALA type III effector family contributes to Ralstonia solanacearum adaptation on different plant hosts

Philippe Remigi  1   2 , Maria Anisimova  3   4 , Alice Guidot  1   2 , Stéphane Genin  1   2 , Nemo Peeters  1   2
Affiliations
Free PMC article

Functional diversification of the GALA type III effector family contributes to Ralstonia solanacearum adaptation on different plant hosts

Philippe Remigi et al. New Phytol. 2011 Dec.
Free PMC article

Abstract

Type III effectors from phytopathogenic bacteria exhibit a high degree of functional redundancy, hampering the evaluation of their precise contribution to pathogenicity. This is illustrated by the GALA type III effectors from Ralstonia solanacearum, which have been shown to be collectively, but not individually, required for disease on Arabidopsis thaliana and tomato. We investigated evolution, redundancy and diversification of this family in order to understand the individual contribution of the GALA effectors to pathogenicity. From sequences available, we reconstructed GALA phylogeny and performed selection studies. We then focused on the GALAs from the reference strain GMI1000 to examine their ability to suppress plant defense responses and contribution to pathogenicity on three different host plants: A. thaliana, tomato (Lycopersicum esculentum) and eggplant (Solanum melongena). The GALA family is well conserved within R. solanacearum species. Patterns of selection detected on some GALA family members, together with experimental results, show that GALAs underwent functional diversification. We conclude that functional divergence of the GALA family likely accounts for its remarkable conservation during R. solanacearum evolution and could contribute to R. solanacearum's adaptation on several host plants.

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Figures

Fig. 1
Fig. 1
GALA phylogeny. Unrooted maximum-likelihood phylogenetic reconstruction of GALAs from strains GMI1000, RS1000, CMR15, IPO1609, Molk2, CFBP2957 and PSI07. Branch support values (aBayes) are shown only for clades with strong support (> 0.9).
Fig. 2
Fig. 2
GALA4 but not GALA5 can interfere with callose deposition. Arabidopsis thaliana leaves were inoculated with Pseudomonas syringae strains and stained for callose 24 h after infection. A box plot diagram of papillae number from at least five independent fields of view is shown for each strain. The horizontal black bar is the median and the boxes indicate lower and upper quartiles. This experiment was repeated four times with similar results. *, median number of callose spots per field of view in the tested strain is statistically different from the strain Pst DC3000 ΔCEL (Mann–Whitney test, P < 0.05). WT, wild-type.
Fig. 3
Fig. 3
gala2, 3, 6, 7 mutant (strain GRS460, triangles) phenocopies the septuple gala mutant (strain GRS447, squares) on Arabidopsis thaliana and Lycopersicon esculentum (tomato) but not on Solanum melongena (eggplant). Kaplan–Meier survival analysis of A. thaliana (a), tomato (b) and eggplant (c) plants inoculated with Ralstonia solanacearum. GMI1000, wild-type, circles. Each strain was inoculated on 16 A. thaliana plants (a), 24 tomato plants (b) and 20 eggplant plants (c). Correspondence between strains and color code is conserved in the three graphs. P-values from Gehan–Breslow–Wilcoxon tests are associated with each graph. Yellow boxes indicate a P-value of <0.05. These experiments were performed at three times with similar results.
Fig. 4
Fig. 4
Pathogenicity assays of Ralstonia solanacearum triple gala mutants on Arabidopsis thaliana and Lycopersicon esculentum (tomato). Kaplan–Meier survival analysis of A. thaliana (a, b, c) and tomato (d, e) plants inoculated with R. solanacearum mutants. Genotypes of the tested strains are the following: GMI1000, wild-type; GRS536, gala2, 3, 7; GRS537, gala2, 3, 6; GRS538, gala3, 6, 7; GRS539, gala2, 6, 7; GRS460, gala2, 3, 6, 7. Each strain was inoculated on 16 A. thaliana plants (a, b, c) and 24 tomato plants (d, e). P-values from Gehan–Breslow–Wilcoxon tests are associated with each graph. Yellow boxes indicate a P-value of <0.05. These experiments were performed three times with similar results.
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