<i>Cladosporium fulvum</i> overcomes <i>Cf‐2</i>‐mediated resistance by producing truncated AVR2 elicitor proteins

Luderer, R.; Takken, Frank L. W.; Wit, P.J.G.M. de; Joosten, M.H.A.J.

doi:10.1046/j.1365-2958.2002.03060.x

Cited by 159 publications

(133 citation statements)

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“…Furthermore, Kapitonov and Jurka (38) have identified an unique class of SINEs that are derived from the fusion of a 5S rRNA gene and a LINE, showing that 5S rRNA genes and retroelements can indeed interact with one another. A number of retroelements, including SINEs, LINEs, and related retrotransposons, have been identified in A. nidulans (39), F. graminearum (40), M. grisea (41,42), N. crassa (43), and a number of other related fungal species (44)(45)(46)(47)(48)(49). Interestingly, Esnault et al (50) have shown that LINEs are capable of amplifying and integrating non-LINE mRNA transcripts by turning them into processed pseudogenes and then integrating them into other parts of the genome.…”

Section: Discussionmentioning

confidence: 99%

Evolution of a large ribosomal RNA multigene family in filamentous fungi: Birth and death of a concerted evolution paradigm

Rooney

Ward

2005

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

168

153

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In eukaryotes, the primary components of the ribosome are encoded by multicopy nuclear ribosomal RNA (rRNA) genes: 28͞26S, 18S, 5.8S, and 5S. Copies of these genes are typically localized within tandem arrays and homogenized within a genome. As a result, nuclear rRNA gene families have become a paradigm of concerted evolution. In filamentous fungi of the subphylum Pezizomycotina, 5S rRNA genes exist as a large and dispersed multigene family, with between 50 and 100 copies per genome. To determine whether these genes defy the concerted evolution paradigm, we examined the patterns of evolution of these genes by using sequences from the complete genomes of four species. Analyses of these sequences revealed (i) multiple 5S gene types within a genome, (ii) interspecies clustering of gene types, (iii) multiple identical gene types shared among species, (iv) multiple pseudogenes within a genome, and (v) presence͞absence variation of individual 5S copies in comparisons of closely related species. These results demonstrate that the 5S family in these species is characterized by birth-and-death evolution under strong purifying selection. Furthermore, our results suggest that birth-and-death evolution occurs at different rates in the genera examined, and that the multiplication and movement of 5S genes across the genome are highly dynamic. As such, we hypothesize that a mechanism resembling retroposition controls 5S rRNA gene amplification, dispersal, and integration in the genomes of filamentous fungi.5S rRNA ͉ retroposition

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Section: Discussionmentioning

confidence: 99%

Evolution of a large ribosomal RNA multigene family in filamentous fungi: Birth and death of a concerted evolution paradigm

Rooney

Ward

2005

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

168

153

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“…Although Avr products identified in other plant pathogenic fungi also are secreted proteins (Lauge and de Wit, 1998), the Avr2, Avr4, and Avr9 products of Cladosporium fulvum (Parniske et al, 1997;Luderer et al, 2002) and the Rhyncosporium secalis NIP1 protein (Knogge, 1996) are recognized extracellularly and probably do not enter plant cells. Delivery of the Avr1b protein from the oomycete pathogen Phytophthora sojae to the extracellular space of Glycine max (soybean) leaves induced R genedependent cell death (Tyler 2002), suggesting that it also may be recognized extracellularly.…”

Section: Avrl567 Proteins Are Secreted From Rust Haustoria and Recognmentioning

confidence: 99%

The Melampsora lini AvrL567 Avirulence Genes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells

et al. 2004

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The Linum usitatissimum (flax) L gene alleles, which encode nucleotide binding site-Leu rich repeat class intracellular receptor proteins, confer resistance against the Melampsora lini (flax rust) fungus. At least 11 different L resistance specificities are known, and the corresponding avirulence genes in M. lini map to eight independent loci, some of which are complex and encode multiple specificities. We identified an M. lini cDNA marker that cosegregates in an F2 rust family with a complex locus determining avirulence on the L5, L6, and L7 resistance genes. Two related avirulence gene candidates, designated AvrL567-A and AvrL567-B, were identified in a genomic DNA contig from the avirulence allele, whereas the corresponding virulence allele contained a single copy of a related gene, AvrL567-C. Agrobacterium tumefaciens-mediated transient expression of the mature AvrL567-A or AvrL567-B (but not AvrL567-C) proteins as intracellular products in L. usitatissimum and Nicotiana tabacum (tobacco) induced a hypersensitive response-like necrosis that was dependent on coexpression of the L5, L6, or L7 resistance gene. An F1 seedling lethal or stunted growth phenotype also was observed when transgenic L. usitatissimum plants expressing AvrL567-A or AvrL567-B (but not AvrL567-C) were crossed to resistant lines containing L5, L6, or L7. The AvrL567 genes are expressed in rust haustoria and encode 127 amino acid secreted proteins. Intracellular recognition of these rust avirulence proteins implies that they are delivered into host cells across the plant membrane. Differences in the three AvrL567 protein sequences result from diversifying selection, which is consistent with a coevolutionary arms race.

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“…RCR3, however, is also required for the function of resistance gene Cf-2, which confers recognition of the fungal pathogen C. fulvum carrying the Avr2 avirulence gene [43]. The AVR2 protein is a small Cys-rich basic protein that is secreted during infection and is not homologous to any known protein [47]. Protease activity profiling of RCR3 in the presence and absence of AVR2 revealed that AVR2 is an inhibitor of RCR3 [42 ].…”

Section: Pathogen Inhibitors Targeting Plant Enzymesmentioning

confidence: 99%

Enzyme–inhibitor interactions at the plant–pathogen interface

Misas-Villamil

Hoorn

2008

Current Opinion in Plant Biology

120

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The plant apoplast during plant-pathogen interactions is an ancient battleground that holds an intriguing range of attacking enzymes and counteracting inhibitors. Examples are pathogen xylanases and polygalacturonases that are inhibited by plant proteins like TAXI, XIP, and PGIP; and plant glucanases and proteases, which are targeted by pathogen proteins such as GIP1, EPI1, EPIC2B, and AVR2. These seven well-characterized inhibitors have different modes of action and many probably evolved from inactive enzymes themselves. Detailed studies of the structures, sequence variation, and mutated proteins uncovered molecular struggles between these enzymes and their inhibitors, resulting in positive selection for variant residues at the contact surface, where single residues determine the outcome of the interaction. Introduction Extracellular plant-pathogen interactions probably existed long before the evolution of pathogen effector translocation systems and plant resistance (R) genes. The molecular basis of these interactions is mostly undiscovered but some have been investigated in detail and reveal intriguing mechanisms. Here we will highlight major recent findings of extracellular enzyme-inhibitor interactions at the plant-pathogen interface.Although extracellular plant-pathogen interactions are complex, they can be simplified by assuming that they evolved in several stages (Figure 1). First, micro-organisms became pathogens by attacking plants using cell-wall-degrading enzymes and other hydrolases ( Figure 1A). In response to this attack, plants secrete inhibitors that suppress these hydrolases ( Figure 1B). Initially, these inhibitors were probably constitutively produced, but upon evolution of pathogen recognition systems the production and secretion of these proteins became inducible, becoming part of the arsenal of pathogenesis-related (PR) proteins. Besides suppression of pathogen attack, counter attack mechanisms also evolved in plants through the induced secretion of hydrolytic enzymes ( Figure 1C). Examples are the well-studied PR proteins including endo-b-1,3-glucanases (PR-2), chitinases (PR-3), and proteases (PR-7) [1 ]. Pathogens, in turn, responded to this counter attack by producing inhibitors that suppress these enzymes ( Figure 1D). The fifth and latest step was a sophisticated refinement of the pathogen recognition system by the evolution of R genes that recognize the manipulation of plant targets by pathogens, inducing a severe defense response that includes cell death ( Figure 1E). Aspects of this simplified model are consistent with the 'zigzag' model for the plant immune system, which explains the suppression of basal defense responses by pathogen effector proteins, followed by the evolution of efficient effector recognition by R proteins [2].Antagonistic interactions between organisms at the molecular level result in enzymes that evade inhibition, and inhibitors that adapt to these new enzymes. These 'molecular struggles' result in positive selection for variation of residues at the interactio...

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Cladosporium fulvum overcomes Cf‐2‐mediated resistance by producing truncated AVR2 elicitor proteins

Cited by 159 publications

References 42 publications

Evolution of a large ribosomal RNA multigene family in filamentous fungi: Birth and death of a concerted evolution paradigm

Evolution of a large ribosomal RNA multigene family in filamentous fungi: Birth and death of a concerted evolution paradigm

The Melampsora lini AvrL567 Avirulence Genes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells

Enzyme–inhibitor interactions at the plant–pathogen interface

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