The effector protein Avr2 of the xylem‐colonizing fungus <i>Fusarium oxysporum</i> activates the tomato resistance protein I‐2 intracellularly

Houterman, Petra M.; Ma, Lisong; Ooijen, Gerben van; Vroomen, Marianne J. de; Cornelissen, Ben J. C.; Takken, Frank L. W.; Rep, Martijn

doi:10.1111/j.1365-313x.2009.03838.x

Cited by 243 publications

(329 citation statements)

References 45 publications

Supporting

Mentioning

317

Contrasting

Unclassified

Order By: Relevance

“…A number of fungal Avr proteins are also inferred to be delivered into host cells, based on their intracellular recognition by R proteins (Jia et al, 2000;Dodds et al, 2004;Catanzariti et al, 2006;Ridout et al, 2006;Houterman et al, 2009;Li et al, 2009). For instance, flax rust Avr proteins have been shown to trigger HR when transiently expressed as intracellular proteins in flax leaves expressing corresponding R genes (Dodds et al, 2004;Catanzariti et al, 2006), and recognition of both AvrM and AvrL567 is determined by direct interaction with cytoplasmic resistance proteins Catanzariti et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Khang et al (2010) showed that the biotrophic interfacial complex-localized proteins are subsequently delivered into host cells, suggesting that this structure serves as an assembly area for secreted effectors prior to their transport into host cells. Likewise, the Avr2 protein of Fusarium oxysporum f. sp lycopersicon is recognized by the tomato I-2 resistance protein intracellularly (Houterman et al, 2009). Several genes for secreted proteins in the maize smut fungus, Ustilago maydis, have homology to proteins with intracellular regulatory functions, suggesting that they may act inside plant cells (Mueller et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Internalization of Flax Rust Avirulence Proteins into Flax and Tobacco Cells Can Occur in the Absence of the Pathogen

et al. 2010

View full text Add to dashboard Cite

Translocation of pathogen effector proteins into the host cell cytoplasm is a key determinant for the pathogenicity of many bacterial and oomycete plant pathogens. A number of secreted fungal avirulence (Avr) proteins are also inferred to be delivered into host cells, based on their intracellular recognition by host resistance proteins, including those of flax rust (Melampsora lini). Here, we show by immunolocalization that the flax rust AvrM protein is secreted from haustoria during infection and accumulates in the haustorial wall. Five days after inoculation, the AvrM protein was also detected within the cytoplasm of a proportion of plant cells containing haustoria, confirming its delivery into host cells during infection. Transient expression of secreted AvrL567 and AvrM proteins fused to cerulean fluorescent protein in tobacco (Nicotiana tabacum) and flax cells resulted in intracellular accumulation of the fusion proteins. The rust Avr protein signal peptides were functional in plants and efficiently directed fused cerulean into the secretory pathway. Thus, these secreted effectors are internalized into the plant cell cytosol in the absence of the pathogen, suggesting that they do not require a pathogenencoded transport mechanism. Uptake of these proteins is dependent on signals in their N-terminal regions, but the primary sequence features of these uptake regions are not conserved between different rust effectors.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Internalization of Flax Rust Avirulence Proteins into Flax and Tobacco Cells Can Occur in the Absence of the Pathogen

et al. 2010

View full text Add to dashboard Cite

show abstract

“…The three I genes confer resistance against FOL races containing the three matching avirulence genes AVR1, AVR2, and AVR3, respectively (18)(19)(20). AVR1 is present in all FOL race 1 isolates but is absent in race 2 and 3 isolates (21), with two exceptions: a race 2 isolate and a race 3 isolate from Japan in which the AVR1 gene was independently interrupted by a transposon (22,23).…”

mentioning

confidence: 99%

Multiple Evolutionary Trajectories Have Led to the Emergence of Races in Fusarium oxysporum f. sp. lycopersici

Biju

Fokkens

Houterman

et al. 2017

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

Race 1 isolates of Fusarium oxysporum f. sp. lycopersici (FOL) are characterized by the presence of AVR1 in their genomes. The product of this gene, Avr1, triggers resistance in tomato cultivars carrying resistance gene I. In FOL race 2 and race 3 isolates, AVR1 is absent, and hence they are virulent on tomato cultivars carrying I. In this study, we analyzed an approximately 100-kb genomic fragment containing the AVR1 locus of FOL race 1 isolate 004 (FOL004) and compared it to the sequenced genome of FOL race 2 isolate 4287 (FOL4287). A genomic fragment of 31 kb containing AVR1 was found to be missing in FOL4287. Further analysis suggests that race 2 evolved from race 1 by deletion of this 31-kb fragment due to a recombination event between two transposable elements bordering the fragment. A worldwide collection of 71 FOL isolates representing races 1, 2, and 3, all known vegetative compatibility groups (VCGs), and five continents was subjected to PCR analysis of the AVR1 locus, including the two bordering transposable elements. Based on phylogenetic analysis using the EF1-␣ gene, five evolutionary lineages for FOL that correlate well with VCGs were identified. More importantly, we show that FOL races evolved in a stepwise manner within each VCG by the loss of function of avirulence genes in a number of alternative ways.IMPORTANCE Plant-pathogenic microorganisms frequently mutate to overcome disease resistance genes that have been introduced in crops. For the fungus Fusarium oxysporum f. sp. lycopersici, the causal agent of Fusarium wilt in tomato, we have identified the nature of the mutations that have led to the overcoming of the I and I-2 resistance genes in all five known clonal lineages, which include a newly discovered lineage. Five different deletion events, at least several of which are caused by recombination between transposable elements, have led to loss of AVR1 and overcoming of I. Two new events affecting AVR2 that led to overcoming of I-2 have been identified. We propose a reconstruction of the evolution of races in FOL, in which the same mutations in AVR2 and AVR3 have occurred in different lineages and the FOL pathogenicity chromosome has been transferred to new lineages several times.

show abstract

“…Plants can recognize pathogen effectors through R proteins and the immunity they activate is known as effector triggered immunity or ETI (Chisholm et al, 2006). Although this resistance is most of the time total, it is race specific and can be easily overcome by point mutation in effectors that escape plant recognition (Houterman et al, 2009). ETI is the molecular explanation of the gene-by-gene model proposed by Flor.…”

Section: The Abc Of Plant Immunitymentioning

confidence: 99%

Unraveling the molecules hidden in the gray shadows of quantitative disease resistance to pathogens

2018

View full text Add to dashboard Cite

One of the most challenging questions in plant breeding and molecular plant pathology research is what are the genetic and molecular bases of quantitative disease resistance (QDR)?. The scarce knowledge of how this type of resistance works has hindered plant breeders to fully take advantage of it. To overcome these obstacles new methodologies for the study of quantitative traits have been developed. Approaches such as genetic mapping, identification of quantitative trait loci (QTL) and association mapping, including candidate gene approach and genome wide association studies, have been historically undertaken to dissect quantitative traits and therefore to study QDR. Additionally, great advances in quantitative phenotypic data collection have been provided to improve these analyses. Recently, genes associated to QDR have been cloned, leading to new hypothesis concerning the molecular bases of this type of resistance. In this review we present the more recent advances about QDR and corresponding application, which have allowed postulating new ideas that can help to construct new QDR models. Some of the hypotheses presented here as possible explanations for QDR are related to the expression level and alternative splicing of some defense-related genes expression, the action of "weak alleles" of R genes, the presence of allelic variants in genes involved in the defense response and a central role of kinases or pseudokinases. With the information recapitulated in this review it is possible to conclude that the conceptual distinction between qualitative and quantitative resistance may be questioned since both share important components. Keywords: breeding, complex traits, genome, gene expression, plant immunity, quantitative disease resistance (QDR), quantitative trait loci (QTL). RESUMENUna de las preguntas más desafiantes del fitomejoramiento y de la fitopatología molecular es ¿cuáles son las bases genéticas y moleculares de la resistencia cuantitativa a enfermedades?. El escaso conocimiento de cómo este tipo de resistencia funciona ha obstaculizado que los fitomejoradores la aprovecharlo plenamente. Para superar estos obstáculos se han desarrollado nuevas metodologías para el estudio de rasgos cuantitativos. Los enfoques como el mapeo genético, la identificación de loci de rasgos cuantitativos (QTL) y el mapeo por asociaciones, incluyendo el enfoque de genes candidatos y los estudios de asociación amplia del genoma, se han llevado a cabo históricamente para describir rasgos cuantitativos y por lo tanto para estudiar QDR. Además, se han proporcionado grandes avances en la obtención de datos fenotípicos cuantitativos para mejorar estos análisis. Recientemente, algunos genes asociados a QDR han sido clonados, lo que conduce a nuevas hipótesis sobre las bases moleculares de este tipo de resistencia. En esta revisión presentamos los avances más recientes sobre QDR y la correspondiente aplicación, que han permitido postular nuevas ideas que pueden ayudar a construir nuevos modelos. Algunas de las hipótesis presen...

show abstract

The effector protein Avr2 of the xylem‐colonizing fungus Fusarium oxysporum activates the tomato resistance protein I‐2 intracellularly

Cited by 243 publications

References 45 publications

Internalization of Flax Rust Avirulence Proteins into Flax and Tobacco Cells Can Occur in the Absence of the Pathogen

Internalization of Flax Rust Avirulence Proteins into Flax and Tobacco Cells Can Occur in the Absence of the Pathogen

Multiple Evolutionary Trajectories Have Led to the Emergence of Races in Fusarium oxysporum f. sp. lycopersici

Unraveling the molecules hidden in the gray shadows of quantitative disease resistance to pathogens

Contact Info

Product

Resources

About