Pto update: recent progress on an ancient plant defence response signalling pathway

The Pto gene in tomato confers gene-for-gene resistance to Pseudomonas syringae pv. tomato, the causative agent of bacterial speck disease. Pto was first introgressed from a wild species of tomato into cultivated tomato varieties over 60 years ago and is now widely used to control speck disease. Cloning of the Pto gene revealed that it encodes a cytoplasmically localized serine-threonine protein kinase. The molecular basis of gene-for-gene recognition in this pathosystem is the direct physical interaction of the Pto kinase with either of two Pseudomonas effector proteins, AvrPto and AvrPtoB. Upon recognition of AvrPto or AvrPtoB, the Pto kinase acts in concert with Prf, a leucine-rich repeat-containing protein, to activate multiple signal transduction pathways. There has been much progress in understanding the evolutionary origin of the Pto gene, structural details about how the Pto kinase interacts with AvrPto and AvrPtoB, signaling steps downstream of Pto, and defense responses activated by the Pto pathway. Future work on this model system will focus on how the interaction of the Pto kinase with bacterial effector proteins activates signal transduction, defining the specific role of signaling components, and ultimately, determining which host defense responses are most responsible for inhibiting growth of the pathogen and suppressing symptoms of bacterial speck disease.

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“…[see (6)]. We begin with a brief history of the discovery of the Pto locus-work that laid the foundation for the cloning of the Pto gene.…”

mentioning

confidence: 99%

MOLECULAR BASIS OF PTO-MEDIATED RESISTANCE TO BACTERIAL SPECK DISEASE IN TOMATO

Pedley

Martin²

2003

Annu. Rev. Phytopathol.

283

248

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“…tomato (Pst), provides an excellent opportunity for evolutionary studies because both the pathogen ligand and resistance protein have been extensively characterized at the molecular level (reviewed in Bogdanove 2002;Wu et al 2004). Since the physical interaction of these molecules elicits the resistance response (Scofield et al 1996;Tang et al 1996), they provide the possibility to study the origin and recognition specificity of these molecules and the functional consequences of amino acid variation on an important aspect of plant fitness.…”

mentioning

confidence: 99%

“…The current model for Pto activation involves Pto binding to AvrPto within the plant cell and then becoming activated, possibly by a change in protein conformation induced through ligand binding. The activated Pto protein then transduces the AvrPto signal and is dependent upon Prf to elicit the resistance response (Rathjen et al 1999;Bogdanove 2002). …”

mentioning

confidence: 99%

Natural Variation in the Pto Pathogen Resistance Gene Within Species of Wild Tomato (Lycopersicon). I. Functional Analysis of Pto Alleles

Rose

Langley

Bernal³

et al. 2005

Genetics

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Disease resistance to the bacterial pathogen Pseudomonas syringae pv. tomato (Pst) in the cultivated tomato, Lycopersicon esculentum, and the closely related L. pimpinellifolium is triggered by the physical interaction between plant disease resistance protein, Pto, and the pathogen avirulence protein, AvrPto. To investigate the extent to which variation in the Pto gene is responsible for naturally occurring variation in resistance to Pst, we determined the resistance phenotype of 51 accessions from seven species of Lycopersicon to isogenic strains of Pst differing in the presence of avrPto. One-third of the plants displayed resistance specifically when the pathogen expressed AvrPto, consistent with a gene-for-gene interaction. To test whether this resistance in these species was conferred specifically by the Pto gene, alleles of Pto were amplified and sequenced from 49 individuals and a subset (16) of these alleles was tested in planta using Agrobacterium-mediated transient assays. Eleven alleles conferred a hypersensitive resistance response (HR) in the presence of AvrPto, while 5 did not. Ten amino acid substitutions associated with the absence of AvrPto recognition and HR were identified, none of which had been identified in previous structure-function studies. Additionally, 3 alleles encoding putative pseudogenes of Pto were isolated from two species of Lycopersicon. Therefore, a large proportion, but not all, of the natural variation in the reaction to strains of Pst expressing AvrPto can be attributed to sequence variation in the Pto gene.

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“…The interaction between Pto and either one of the pathogen effectors (37) Percent similarity of coiled-coil (CC) region only is shown in parentheses activates the NBS-LRR subclass R guard protein, Prf, thereby inducing an HR [64]. Prf is also required for the activity of fen, a Pto-like gene that mediates a hypersensitive-like response to the insecticide fenthion [15].…”

Section: Sequence Variation In Rgc-cc_1 In Sugar Pinementioning

confidence: 99%

Isolation of a full-length CC–NBS–LRR resistance gene analog candidate from sugar pine showing low nucleotide diversity

Jermstad

Sheppard

Kinloch

et al. 2006

Tree Genetics & Genomes

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The nucleotide-binding-site and leucine-richrepeat (NBS-LRR) class of R proteins is abundant and widely distributed in plants. By using degenerate primers designed on the NBS domain in lettuce, we amplified sequences in sugar pine that shared sequence identity with many of the NBS-LRR class resistance genes catalogued in GenBank. The polymerase chain reaction products were used to probe a cDNA library constructed from needle tissue of sugar pine seedlings. A full-length cDNA was obtained that demonstrated high predicted amino acid sequence similarity to the coiled coil (CC)-NBS-LRR subclass of NBS-LRR resistance proteins in GenBank. Sequence analyses of this gene in megagametophytes from two sugar pine trees segregating for the hypersensitive response to white pine blister rust revealed zero nucleotide variation. Moreover, there was no variation found in 24 unrelated sugar pine trees except for three single-nucleotide polymorphisms located in the 3′ untranslated region. Compared to other genes sequenced in Pinaceae, such a low level of sequence variation in unrelated individuals is unusual. Although, numerous studies have reported that plant R genes are under diversifying selection for specificity to evolving pathogens, the resistance gene analog discussed here appears to be under intense purifying selection.

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Pto update: recent progress on an ancient plant defence response signalling pathway

Cited by 12 publications

References 47 publications

MOLECULAR BASIS OF PTO-MEDIATED RESISTANCE TO BACTERIAL SPECK DISEASE IN TOMATO

MOLECULAR BASIS OF PTO-MEDIATED RESISTANCE TO BACTERIAL SPECK DISEASE IN TOMATO

Natural Variation in the Pto Pathogen Resistance Gene Within Species of Wild Tomato (Lycopersicon). I. Functional Analysis of Pto Alleles

Isolation of a full-length CC–NBS–LRR resistance gene analog candidate from sugar pine showing low nucleotide diversity

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