Plant disease resistance genes: unravelling how they work

1995 ◽  
Vol 73 (S1) ◽  
pp. 495-505 ◽  
Author(s):  
Kim E. Hammond-Kosack ◽  
Jonathan D. G. Jones

Resistance (R) genes confer on a plant the ability to defend itself following microbial attack. Each R gene exhibits an extreme specificity of action and is only effective against a microbe that has the corresponding functional avirulence (Avr) gene. This article reviews the strategies and experimental approaches deployed to understand the molecular events underlying the specificity of action of various tomato Cf resistance genes that results in incompatibility to the fungal pathogen Cladosporium fulvum. Topics covered include the clustering of Cf genes, the biology of Cf-dependent incompatibility, the map-based and transposon tagging approaches used to clone the Cf-2 and Cf-9 genes, respectively, identification by mutagenesis of other plant loci required for full Cf-9 mediated resistance, the expression of a functional Avr9 gene in planta and its lethal consequences to Cf-9 containing plants, the physiological and molecular host responses to C. fulvum and AVR elicitor challenges and some genetic approaches to ascertain the crucial components of the defense response. Key words: Cladosporium fulvum, Lycopersicon esculentum, tomato leaf mold, Cf resistance genes, fungal avirulence genes, plant defense responses.

1995 ◽  
Vol 73 (S1) ◽  
pp. 490-494 ◽  
Author(s):  
Pierre J. G. M. de Wit ◽  
Matthieu H. A. J. Joosten ◽  
Guy Honée ◽  
Paul J. M. J. Vossen ◽  
Ton J. Cozijnsen ◽  
...  

Host genotype specificity in interactions between biotrophic fungal pathogens and plants in most cases complies with the gene-for-gene model. Success or failure of infection is determined by the absence or presence of complementary genes, avirulence and resistance genes, in the pathogen and the host plant, respectively. Resistance, expressed by the induction of a hypersensitive response followed by other defence responses in the host, is envisaged to be based on recognition of the pathogen, mediated through direct interaction between products of avirulence genes of the pathogen (the so-called race-specific elicitors) and receptors in the host plant, the putative products of resistance genes. The interaction between the biotrophic fungus Cladosporium fulvum and its only host, tomato, is a model system to study fungus–plant gene-for-gene relationships. Here we review research on isolation, characterization, and biological function of two race-specific elicitors AVR4 and AVR9 of C. fulvum and cloning and regulation of their encoding genes. Key words: avirulence genes, race-specific elicitors, resistance genes, hypersensitive response, host defense responses.


PLoS ONE ◽  
2015 ◽  
Vol 10 (4) ◽  
pp. e0123271 ◽  
Author(s):  
Yuichiro Iida ◽  
Pieter van ‘t Hof ◽  
Henriek Beenen ◽  
Carl Mesarich ◽  
Masaharu Kubota ◽  
...  

2001 ◽  
Vol 14 (2) ◽  
pp. 181-188 ◽  
Author(s):  
Michael J. Axtell ◽  
Timothy W. McNellis ◽  
Mary Beth Mudgett ◽  
Caroline S. Hsu ◽  
Brian J. Staskawicz

Plants have evolved a large number of disease resistance genes that encode proteins containing conserved structural motifs that function to recognize pathogen signals and to initiate defense responses. The Arabidopsis RPS2 gene encodes a protein representative of the nucleotide-binding site-leucine-rich repeat (NBS-LRR) class of plant resistance proteins. RPS2 specifically recognizes Pseudomonas syringae pv. tomato strains expressing the avrRpt2 gene and initiates defense responses to bacteria carrying avrRpt2, including a hypersensitive cell death response (HR). We present an in planta mutagenesis experiment that resulted in the isolation of a series of rps2 and avrRpt2 alleles that disrupt the RPS2-avrRpt2 gene-for-gene interaction. Seven novel avrRpt2 alleles incapable of eliciting an RPS2-dependent HR all encode proteins with lesions in the C-terminal portion of AvrRpt2 previously shown to be sufficient for RPS2 recognition. Ten novel rps2 alleles were characterized with mutations in the NBS and the LRR. Several of these alleles code for point mutations in motifs that are conserved among NBS-LRR resistance genes, including the third LRR, which suggests the importance of these motifs for resistance gene function.


2004 ◽  
Vol 17 (2) ◽  
pp. 224-232 ◽  
Author(s):  
Donna Frost ◽  
Heather Way ◽  
Paul Howles ◽  
Joanne Luck ◽  
John Manners ◽  
...  

Tobacco was transformed with three different alleles (L2, L6, and L10) of the flax rust resistance gene L, a member of the toll interleukin-1 receptor, nucleotide-binding site, leucine-rich repeat (TIR-NBS-LRR) class of plant disease resistance genes. L6 transgenics had a stunted phenotype, expressed several defense response genes constitutively, and had increased resistance to the fungus Cercospora nicotianae and the oomycete Phytophthora parasitica pv. nicotianae. L2 and L10 transgenics, with one exception for L10, did not express these phenotypes, indicating that the activation of tobacco defense responses is L6 allele-specific. The phenotype of the exceptional L10 transgenic plant was associated with the presence of a truncated L10 gene resulting from an aberrant T-DNA integration. The truncated gene consisted of the promoter, the complete TIR region, and 39 codons of the NBS domain fused in-frame to a tobacco retrotransposon-like sequence. A similar truncated L10 gene, constructed in vitro, was transiently expressed in tobacco leaves and gave rise to a strong localized necrotic reaction. Together, these results suggest that defense signaling properties of resistance genes can be expressed in an allele-specific and pathogen-independent manner when transferred between plant genera.


1997 ◽  
Vol 10 (6) ◽  
pp. 725-734 ◽  
Author(s):  
Richard Laugé ◽  
Matthieu H. A. J. Joosten ◽  
Guido F. J. M. Van den Ackerveken ◽  
Henk W. J. Van den Broek ◽  
Pierre J. G. M. De Wit

The two extracellular proteins ECP1 and ECP2 are abundantly secreted by the plant-pathogenic fungus Cladosporium fulvum during colonization of the intercellular space of tomato leaves. We examined the involvement of both proteins in pathogenicity and virulence of this fungus. ECP1-deficient, ECP2-deficient, and ECP1/ECP2- deficient isogenic C. fulvum strains were created by targeted gene replacement. Upon inoculation onto susceptible 6-week-old tomato plants, all three mutants showed reduced virulence. Deficiency in ECP2 resulted in a strain that poorly colonized the leaf tissue and secreted lower amounts of the in planta-produced ECP3, AVR4, and AVR9 proteins than the wild-type strain. The ECP2-deficient strain produced little emerging mycelium and few conidia. Deficiency in ECP1 did not significantly modify colonization of the leaf tissue, but reduced secretion of in planta-produced proteins. The ECP1-deficient strain emerged from stomata of the lower epidermis, but failed to sporulate as abundantly as the wild-type strain. A strain deficient in both ECP1 and ECP2 proteins had a phenotype similar to that of the ECP2-deficient strain. Accumulation of pathogenesis-related proteins and induction of late responses, such as leaf desiccation and abscission, occurred more quickly and more severely in tomato after inoculation with the ECP1-, ECP2-, and ECP1/ECP2-deficient strains than after inoculation with the wild-type strain. Moreover, partial collapse of stomatal guard cells occurred at emergence of the ECP2-deficient strain. These results indicate that the ECP1 and ECP2 proteins play a role in virulence of C. fulvum on tomato and suggest that both are involved in suppression of host defense responses.


2003 ◽  
Vol 16 (4) ◽  
pp. 289-294 ◽  
Author(s):  
Shunyuan Xiao ◽  
Piyavadee Charoenwattana ◽  
Lucy Holcombe ◽  
John G. Turner

Plant disease resistance (R) gene products recognize pathogen avirulence (Avr) gene products and induce defense responses. It is not known if an R gene can function in different plant families, however. The Arabidopsis thaliana R genes RPW8.1 and RPW8.2 confer resistance to the powdery mildew pathogens Erysiphe orontii, E. cichoracearum, and Oidium lycopersici, which also infect plants from other families. We produced transgenic Nicotiana tabacum, N. benthamiana, and Lycopersicon esculentum plants containing RPW8.1 and RPW8.2. Transgenic N. tabacum plants had increased resistance to E. orontii and O. lycopersici, transgenic N. benthamiana plants had increased resistance to E. cichoracearum, but transgenic L. esculentum plants remained susceptible to these pathogens. The defense responses induced in transgenic N. tabacum and N. benthamiana were similar to those mediated by RPW8.1 and RPW8.2 in Arabidopsis. Apparently, RPW8.1 and RPW8.2 could be used to control powdery mildew diseases of plants from other families.


2000 ◽  
Vol 13 (4) ◽  
pp. 439-446 ◽  
Author(s):  
Renier A. L. Van der Hoorn ◽  
Franck Laurent ◽  
Ronelle Roth ◽  
Pierre J. G. M. De Wit

The avirulence genes Avr9 and Avr4 from the fungal tomato pathogen Cladosporium fulvum encode extracellular proteins that elicit a hypersensitive response when injected into leaves of tomato plants carrying the matching resistance genes, Cf-9 and Cf-4, respectively. We successfully expressed both Avr9 and Avr4 genes in tobacco with the Agrobacterium tumefaciens transient transformation assay (agroinfiltration). In addition, we expressed the matching resistance genes, Cf-9 and Cf-4, through agroinfiltration. By combining transient Cf gene expression with either transgenic plants expressing one of the gene partners, Potato virus X (PVX)-mediated Avr gene expression, or elicitor injections, we demonstrated that agroinfiltration is a reliable and versatile tool to study Avr/Cf-mediated recognition. Significantly, agroinfiltration can be used to quantify and compare Avr/Cf-induced responses. Comparison of different Avr/Cf-interactions within one tobacco leaf showed that Avr9/Cf-9-induced necrosis developed slower than necrosis induced by Avr4/Cf-4. Quantitative analysis demonstrated that this temporal difference was due to a difference in Avr gene activities. Transient expression of matching Avr/Cf gene pairs in a number of plant families indicated that the signal transduction pathway required for Avr/Cf-induced responses is conserved within solana-ceous species. Most non-solanaceous species did not develop specific Avr/Cf-induced responses. However, co-expression of the Avr4/Cf-4 gene pair in lettuce resulted in necrosis, providing the first proof that a resistance (R) gene can function in a different plant family.


2021 ◽  
Author(s):  
Nathalie D Lackus ◽  
Axel Schmidt ◽  
Jonathan Gershenzon ◽  
Tobias G Köllner

AbstractBenzenoids (C6–C1 aromatic compounds) play important roles in plant defense and are often produced upon herbivory. Black cottonwood (Populus trichocarpa) produces a variety of volatile and nonvolatile benzenoids involved in various defense responses. However, their biosynthesis in poplar is mainly unresolved. We showed feeding of the poplar leaf beetle (Chrysomela populi) on P. trichocarpa leaves led to increased emission of the benzenoid volatiles benzaldehyde, benzylalcohol, and benzyl benzoate. The accumulation of salicinoids, a group of nonvolatile phenolic defense glycosides composed in part of benzenoid units, was hardly affected by beetle herbivory. In planta labeling experiments revealed that volatile and nonvolatile poplar benzenoids are produced from cinnamic acid (C6–C3). The biosynthesis of C6–C1 aromatic compounds from cinnamic acid has been described in petunia (Petunia hybrida) flowers where the pathway includes a peroxisomal-localized chain shortening sequence, involving cinnamate-CoA ligase (CNL), cinnamoyl-CoA hydratase/dehydrogenase (CHD), and 3-ketoacyl-CoA thiolase (KAT). Sequence and phylogenetic analysis enabled the identification of small CNL, CHD, and KAT gene families in P. trichocarpa. Heterologous expression of the candidate genes in Escherichia coli and characterization of purified proteins in vitro revealed enzymatic activities similar to those described in petunia flowers. RNA interference-mediated knockdown of the CNL subfamily in gray poplar (Populus x canescens) resulted in decreased emission of C6–C1 aromatic volatiles upon herbivory, while constitutively accumulating salicinoids were not affected. This indicates the peroxisomal β-oxidative pathway participates in the formation of volatile benzenoids. The chain shortening steps for salicinoids, however, likely employ an alternative pathway.


Genetics ◽  
2001 ◽  
Vol 158 (1) ◽  
pp. 439-450 ◽  
Author(s):  
Diya Banerjee ◽  
Xiaochun Zhang ◽  
Andrew F Bent

Abstract Like many other plant disease resistance genes, Arabidopsis thaliana RPS2 encodes a product with nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domains. This study explored the hypothesized interaction of RPS2 with other host factors that may be required for perception of Pseudomonas syringae pathogens that express avrRpt2 and/or for the subsequent induction of plant defense responses. Crosses between Arabidopsis ecotypes Col-0 (resistant) and Po-1 (susceptible) revealed segregation of more than one gene that controls resistance to P. syringae that express avrRpt2. Many F2 and F3 progeny exhibited intermediate resistance phenotypes. In addition to RPS2, at least one additional genetic interval associated with this defense response was identified and mapped using quantitative genetic methods. Further genetic and molecular genetic complementation experiments with cloned RPS2 alleles revealed that the Po-1 allele of RPS2 can function in a Col-0 genetic background, but not in a Po-1 background. The other resistance-determining genes of Po-1 can function, however, as they successfully conferred resistance in combination with the Col-0 allele of RPS2. Domain-swap experiments revealed that in RPS2, a polymorphism at six amino acids in the LRR region is responsible for this allele-specific ability to function with other host factors.


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