Adaptive Evolution among Plant Pathogenic Oomycte RXLR Effector Genes

Fungi and oomycetes include deep and diverse lineages of eukaryotic plant pathogens. The last 10 years have seen the sequencing of the genomes of a multitude of species of these so-called filamentous plant pathogens. Already, fundamental concepts have emerged. Filamentous plant pathogen genomes tend to harbor large repertoires of genes encoding virulence effectors that modulate host plant processes. Effector genes are not randomly distributed across the genomes but tend to be associated with compartments enriched in repetitive sequences and transposable elements. These findings have led to the “two-speed genome” model in which filamentous pathogen genomes have a bipartite architecture with gene sparse, repeat rich compartments serving as a cradle for adaptive evolution. Here, we review this concept and discuss how plant pathogens are great model systems to study evolutionary adaptations at multiple time scales. We will also introduce the next phase of research on this topic.

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Allelic Variation in the Effector Genes of the Tomato Pathogen Cladosporium fulvum Reveals Different Modes of Adaptive Evolution

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-20-10-1271 ◽

2007 ◽

Vol 20 (10) ◽

pp. 1271-1283 ◽

Cited By ~ 71

Author(s):

Ioannis Stergiopoulos ◽

Maarten J. D. De Kock ◽

Pim Lindhout ◽

Pierre J. G. M. De Wit

Keyword(s):

Adaptive Evolution ◽

Genetic Recombination ◽

Allelic Variation ◽

Point Mutations ◽

Haplotype Network ◽

Cladosporium Fulvum ◽

Effector Genes ◽

Mating Type Genes ◽

Tomato Pathogen ◽

Avr Genes

The allelic variation in four avirulence (Avr) and four extracellular protein (Ecp)–encoding genes of the tomato pathogen Cladosporium fulvum was analyzed for a worldwide collection of strains. The majority of polymorphisms observed in the Avr genes are deletions, point mutations, or insertions of transposon-like elements that are associated with transitions from avirulence to virulence, indicating adaptive evolution of the Avr genes to the cognate C. fulvum resistance genes that are deployed in commercial tomato lines. Large differences in types of polymorphisms between the Avr genes were observed, especially between Avr2 (indels) and Avr4 (amino-acid substitutions), indicating that selection pressure favors different types of adaptation. In contrast, only a limited number of polymorphisms were observed in the Ecp genes, which mostly involved synonymous modifications. A haplotype network based on the polymorphisms observed in the effector genes revealed a complex pattern of evolution marked by reticulations that suggests the occurrence of genetic recombination in this presumed asexual fungus. This, as well as the identification of strains with identical polymorphisms in Avr and Ecp genes but with opposite mating-type genes, suggests that development of complex races can be the combined result of positive selection and genetic recombination.

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Functional analysis of a Phytophthora host-translocated effector using the yeast model system

PeerJ ◽

10.7717/peerj.12576 ◽

2021 ◽

Vol 9 ◽

pp. e12576

Author(s):

Avery C. Wilson ◽

William R. Morgan

Keyword(s):

Amino Acid ◽

Plant Pathogens ◽

Bioinformatics Analysis ◽

Effector Proteins ◽

Yeast Cells ◽

Phosphate Homeostasis ◽

Rxlr Effectors ◽

Effector Genes ◽

Rxlr Effector ◽

Yeast Genes

Background Phytophthora plant pathogens secrete effector proteins that are translocated into host plant cells during infection and collectively contribute to pathogenicity. A subset of these host-translocated effectors can be identified by the amino acid motif RXLR (arginine, any amino acid, leucine, arginine). Bioinformatics analysis has identified hundreds of putative RXLR effector genes in Phytophthora genomes, but the specific molecular function of most remains unknown. Methods Here we describe initial studies to investigate the use of Saccharomyces cerevisiae as a eukaryotic model to explore the function of Phytophthora RXLR effector proteins. Results and Conclusions Expression of individual RXLR effectors in yeast inhibited growth, consistent with perturbation of a highly conserved cellular process. Transcriptome analysis of yeast cells expressing the poorly characterized P. sojae RXLR effector Avh110 identified nearly a dozen yeast genes whose expression levels were altered greater than two-fold compared to control cells. All five of the most down-regulated yeast genes are normally induced under low phosphate conditions via the PHO4 transcription factor, indicating that PsAvh110 perturbs the yeast regulatory network essential for phosphate homeostasis and suggesting likely PsAvh110 targets during P. sojae infection of its soybean host.

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Correction: Copy Number Variation and Transcriptional Polymorphisms of Phytophthora sojae RXLR Effector Genes Avr1a and Avr3a

PLoS ONE ◽

10.1371/annotation/2a2adcf8-afbc-4d46-92c6-d543d6b29182 ◽

2009 ◽

Vol 4 (6) ◽

Cited By ~ 3

Author(s):

Dinah Qutob ◽

Jennifer Tedman-Jones ◽

Suomeng Dong ◽

Kuflom Kuflu ◽

Hai Pham ◽

...

Keyword(s):

Copy Number Variation ◽

Copy Number ◽

Phytophthora Sojae ◽

Effector Genes ◽

Rxlr Effector ◽

Number Variation

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Up-regulated RxLR effector genes of Plasmopara viticola in synchronized host-free stages and infected leaves of hosts with different susceptibility

Fungal Biology ◽

10.1016/j.funbio.2018.07.006 ◽

2018 ◽

Vol 122 (12) ◽

pp. 1125-1133

Author(s):

Javier Gómez-Zeledón ◽

Otmar Spring

Keyword(s):

Plasmopara Viticola ◽

Effector Genes ◽

Rxlr Effector

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Two RxLR Avirulence Genes in Phytophthora sojae Determine Soybean Rps1k-Mediated Disease Resistance

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-12-12-0289-r ◽

2013 ◽

Vol 26 (7) ◽

pp. 711-720 ◽

Cited By ~ 37

Author(s):

Tianqiao Song ◽

Shiv D. Kale ◽

Felipe D. Arredondo ◽

Danyu Shen ◽

Liming Su ◽

...

Keyword(s):

Disease Resistance ◽

Defense Response ◽

Phytophthora Sojae ◽

Stem Rot ◽

Avirulence Genes ◽

The Past ◽

Effector Genes ◽

Rxlr Effector ◽

Soybean Plants ◽

Lines Of Evidence

Resistance to Phytophthora sojae (Rps) genes have been widely used in soybean against root and stem rot diseases caused by this oomycete. Among 15 known soybean Rps genes, Rps1k has been the most widely used in the past four decades. Here, we show that the products of two distinct but closely linked RxLR effector genes are detected by Rps1k-containing plants, resulting in disease resistance. One of the genes is Avr1b-1, that confers avirulence in the presence of Rps1b. Three lines of evidence, including overexpression and gene silencing of Avr1b-1 in stable P. sojae transformants, as well as transient expression of this gene in soybean, indicated that Avr1b could trigger an Rps1k-mediated defense response. Some isolates of P. sojae that do not express Avr1b are nevertheless unable to infect Rps1k plants. In those isolates, we identified a second RxLR effector gene (designated Avr1k), located 5 kb away from Avr1b-1. Silencing or overexpression of Avr1k in P. sojae stable transformants resulted in the loss or gain, respectively, of the avirulence phenotype in the presence of Rps1k. Only isolates of P. sojae with mutant alleles of both Avr1b-1 and Avr1k could evade perception by the soybean plants carrying Rps1k.

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