Effector Genes of<i>Xanthamonas axonopodis</i>pv.<i>vesicatoria</i>Promote Transmission and Enhance Other Fitness Traits in the Field

Wichmann, Gale; Bergelson, Joy

doi:10.1534/genetics.166.2.693

Cited by 85 publications

(76 citation statements)

References 63 publications

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“…Although modification of the 14-3-3 binding motif did not attenuate virulence dramatically under growth chamber conditions, it may result in a significant reduction of pathogen fitness in the field (Wichmann and Bergelson, 2004). Crude protein extracts (20 mg of proteins per lane) were isolated from leaves 48 h after agroinfiltration.…”

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confidence: 99%

Phosphorylation of HopQ1, a Type III Effector from Pseudomonas syringae, Creates a Binding Site for Host 14-3-3 Proteins

et al. 2013

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HopQ1 (for Hrp outer protein Q), a type III effector secreted by Pseudomonas syringae pv phaseolicola, is widely conserved among diverse genera of plant bacteria. It promotes the development of halo blight in common bean (Phaseolus vulgaris). However, when this same effector is injected into Nicotiana benthamiana cells, it is recognized by the immune system and prevents infection. Although the ability to synthesize HopQ1 determines host specificity, the role it plays inside plant cells remains unexplored. Following transient expression in planta, HopQ1 was shown to copurify with host 14-3-3 proteins. The physical interaction between HopQ1 and 14-3-3a was confirmed in planta using the fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy technique. Moreover, mass spectrometric analyses detected specific phosphorylation of the canonical 14-3-3 binding site (RSXpSXP, where pS denotes phosphoserine) located in the amino-terminal region of HopQ1. Amino acid substitution within this motif abrogated the association and led to altered subcellular localization of HopQ1. In addition, the mutated HopQ1 protein showed reduced stability in planta. These data suggest that the association between host 14-3-3 proteins and HopQ1 is important for modulating the properties of this bacterial effector.

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confidence: 99%

Phosphorylation of HopQ1, a Type III Effector from Pseudomonas syringae, Creates a Binding Site for Host 14-3-3 Proteins

et al. 2013

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“…AvrBs3 activates the expression of pepper UPA20, which encodes a basic helix-loop-helix (bHLH) transcription factor that induces cell hypertrophy (22). Loss of AvrBs3 has been demonstrated to incur a bacterial fitness cost in the field (23).…”

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confidence: 99%

TALE-induced bHLH transcription factors that activate a pectate lyase contribute to water soaking in bacterial spot of tomato

Schwartz

Morbitzer

Lahaye

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

107

129

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AvrHah1 [avirulence (avr) gene homologous to avrBs3 and hax2, no. 1] is a transcription activator-like (TAL) effector (TALE) in Xanthomonas gardneri that induces water-soaked disease lesions on fruits and leaves during bacterial spot of tomato. We observe that water from outside the leaf is drawn into the apoplast in X. gardneriinfected, but not X. gardneriΔavrHah1 (XgΔavrHah1)-infected, plants, conferring a dark, water-soaked appearance. The pull of water can facilitate entry of additional bacterial cells into the apoplast. Comparing the transcriptomes of tomato infected with X. gardneri vs. XgΔavrHah1 revealed the differential up-regulation of two basic helix-loop-helix (bHLH) transcription factors with predicted effector binding elements (EBEs) for AvrHah1. We mined our RNA-sequencing data for differentially up-regulated genes that could be direct targets of the bHLH transcription factors and therefore indirect targets of AvrHah1. We show that two pectin modification genes, a pectate lyase and pectinesterase, are targets of both bHLH transcription factors. Designer TALEs (dTALEs) for the bHLH transcription factors and the pectate lyase, but not for the pectinesterase, complement water soaking when delivered by XgΔavrHah1. By perturbing transcriptional networks and/or modifying the plant cell wall, AvrHah1 may promote water uptake to enhance tissue damage and eventual bacterial egression from the apoplast to the leaf surface. Understanding how disease symptoms develop may be a useful tool for improving the tolerance of crops from damaging disease lesions.

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“…Yet, some effectors of the bacterial genus Xanthomonas harbor nuclear localization signals and a transcriptional activation domain (Van den Ackerveken et al, 1996;Yang et al, 2000;Szurek et al, 2001) and have been termed transcription activator-like effector proteins (TALes; Kay and Bonas, 2009). The prototype TALe, AvrBs3, was identified from Xanthomonas campestris pv vesicatoria (Xcv) based on its avirulence activity in pepper (Capsicum annuum; Bonas et al, 1989) and was later shown to contribute to bacterial virulence in susceptible pepper genotypes (Wichmann and Bergelson, 2004). The most characteristic structural feature of TALes is a variable number of tandemly arranged, nearly perfect copies of a 34-amino acid motif that mediates binding of the TALe AvrBs3 to host target promoters (Kay et al, 2007).…”

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Recognition of AvrBs3-Like Proteins Is Mediated by Specific Binding to Promoters of Matching Pepper Bs3 Alleles

et al. 2009

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The pepper (Capsicum annuum) bacterial spot (Bs) resistance gene Bs3 and its allelic variant Bs3-E mediate recognition of the Xanthomonas campestris pv vesicatoria type III effector protein AvrBs3 and its deletion derivative AvrBs3Drep16. Recognition specificity resides in the Bs3 and Bs3-E promoters and is determined by a defined promoter region, the UPA (for up-regulated by AvrBs3) box. Using site-directed mutagenesis, we defined the exact boundaries of the UPA AvrBs3 box of the Bs3 promoter and the UPA AvrBs3Drep16 box of the Bs3-E promoter and show that both boxes overlap by at least 11 nucleotides. Despite partial sequence identity, the UPA AvrBs3 box and the UPA AvrBs3Drep16 box were bound specifically by the corresponding AvrBs3 and AvrBs3Drep16 proteins, respectively, suggesting that selective promoter binding of AvrBs3-like proteins is the basis for promoter activation specificity. We also demonstrate that the UPA AvrBs3 box retains its functionality at different positions within the pepper Bs3 promoter and confers AvrBs3 inducibility in a novel promoter context. Notably, the transfer of the UPA AvrBs3 box to different promoter locations is always correlated with a new transcriptional start site. The analysis of naturally occurring Bs3 alleles revealed many pepper accessions that encode a nonfunctional Bs3 variant. These accessions showed no apparent abnormalities, supporting the supposition that Bs3 functions only in disease resistance and not in other developmental or physiological processes.

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Effector Genes ofXanthamonas axonopodispv.vesicatoriaPromote Transmission and Enhance Other Fitness Traits in the Field

Cited by 85 publications

References 63 publications

Phosphorylation of HopQ1, a Type III Effector from Pseudomonas syringae, Creates a Binding Site for Host 14-3-3 Proteins

Phosphorylation of HopQ1, a Type III Effector from Pseudomonas syringae, Creates a Binding Site for Host 14-3-3 Proteins

TALE-induced bHLH transcription factors that activate a pectate lyase contribute to water soaking in bacterial spot of tomato

Recognition of AvrBs3-Like Proteins Is Mediated by Specific Binding to Promoters of Matching Pepper Bs3 Alleles

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