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. 2000 Jul 3;19(13):3204-14.
doi: 10.1093/emboj/19.13.3204.

Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease

G Tsiamis  1 , J W Mansfield, R Hockenhull, R W Jackson, A Sesma, E Athanassopoulos, M A Bennett, C Stevens, A Vivian, J D Taylor, J Murillo
Affiliations

Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease

G Tsiamis et al. EMBO J. .

Erratum in

  • EMBO J 2000 Nov 1;19(21):5941

Abstract

The avrPphF gene was cloned from Pseudomonas syringae pathovar phaseolicola (PPH:) races 5 and 7, based on its ability to confer avirulence towards bean cultivars carrying the R1 gene for halo-blight resistance, such as Red Mexican. avrPphF comprised two open reading frames, which were both required for function, and was located on a 154 kb plasmid (pAV511) in PPH: Strain RW60 of PPH:, lacking pAV511, displayed a loss in virulence to a range of previously susceptible cultivars such as Tendergreen and Canadian Wonder. In Tendergreen virulence was restored to RW60 by avrPphF alone, whereas subcloned avrPphF in the absence of pAV511 greatly accelerated the hypersensitive resistance reaction caused by RW60 in Canadian Wonder. A second gene from pAV511, avrPphC, which controls avirulence to soybean, was found to block the activity of avrPphF in Canadian Wonder, but not in Red Mexican. avrPphF also conferred virulence in soybean. The multiple functions of avrPphF illustrate how effector proteins from plant pathogens have evolved to be recognized by R gene products and, therefore, be classified as encoded by avirulence genes.

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Figures

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Fig. 1. Location of avrPphF within pPPY503 and the 1.8 kb of DNA sequenced. The direction of transcription is indicated by the horizontal arrowheads. Sites of insertion of Tn3gus in pPPY503 are indicated by vertical arrowheads; only those marked black in the expanded fragment abolished the avirulence activity of avrPphF. All transposon insertions were mapped from restriction digests, except A33, which was located by sequencing. The region found to have similarity to IS100 is indicated. Restriction sites for BamHI (B), BglII (Bg), EcoRI (E) and PstI (P) are marked; an asterisk indicates site in the vector pLAFR3. The reactions caused in bean cv. Red Mexican by transconjugants of race 6 harbouring subclones are noted. HR, hypersensitive reaction; S, susceptible response.
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Fig. 2. Southern hybridization (high stringency) of BamHI-digested total DNA from different strains of P.syringae using (A) ORF1 and (B) ORF2 of avrPphF and (C) the 0.5 kb EcoRI–BamHI fragment with similarity to IS100 as probes. Digests from races 1, 2, 3, 4, 5 (a, strain 52A; b, strain 1375A), 6, 7, 8 and 9 of P.s. pv. phaseolicola, and P.s. pv. pisi (pi) are shown.
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Fig. 3. Location of avrPphF in relation to avrD, virPphA, avrPphC and ORF4 in the 154 kb plasmid identified in race 7 strain 1449B (Jackson et al., 1999). The insert cloned in pAV520 (vector pLAFR3) is shown; the region present in pAV521 is underlined. Restriction sites for BamHI (B), EcoRI (E) and HindIII (H) are marked.
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Fig. 4. (A) Reaction phenotypes in a pod of cv. Tendergreen 2 days after inoculation with (from left to right) race 7, RW60, RW60 (pAV520) containing the PAI and RW60(pPPY511) expressing avrPphF alone. (B) Reaction phenotypes in a pod of cv. Canadian Wonder 2 days after inoculation with (from left to right) race 7, RW60, RW60(pPPY511) expressing avrPphF, and RW60(pPPY511, pDAHR15) expressing both avrPphF and avrPphC. Note that the lesions caused by RW60 and RW60(pPPY511, pDAHR15) are sunken at this stage compared with the water-soaked susceptible response to race 7, whereas RW60(pPPY511) has already caused a brown lesion characteristic of the rapid HR induced. (C) Reactions at infiltration sites in soybean leaves (cv. Osumi) 3 days after inoculation with (left to right) RW60, which causes a null reaction, and the transconjugant RW60(pPPY511) expressing avrPphF, which causes a susceptible response recognized by yellowing as shown and later some water- soaking.
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Fig. 5. Bacterial multiplication in leaves of bean cv. Tendergreen inoculated with suspensions of 2 × 108 cells/ml of race 7 (open), RW60 (striped), RW60 (pPPY511) (light grey), RW60 (pAV521) (dark grey) and the avrPphF marker exchange mutant race 7::avrPphF Tn3gusA33 (black); bars, ± SEM.
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Fig. 6. Bacterial multiplication in leaves of bean cv. Canadian Wonder inoculated with bacterial suspensions of 2 × 108 cells/ml of race 7 (open), RW60 (stippled), RW60 (pPPY511) (grey) and RW60(pPPY511, pDAHR15) (black); bars, ± SEM.
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Fig. 7. Bacterial growth in leaves of soybean cv. Osumi inoculated with bacterial suspensions of 108 cells/ml of P.s. pv. glycinea (open), RW60 (stippled) and RW60 (pPPY511) (grey); bars, ± SEM.
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