scholarly journals Effectors with Different Gears: Divergence of Ustilago maydis Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection

2020 ◽  
Vol 7 (1) ◽  
pp. 16
Author(s):  
Jasper R. L. Depotter ◽  
Weiliang Zuo ◽  
Maike Hansen ◽  
Boqi Zhang ◽  
Mingliang Xu ◽  
...  
Keyword(s):  
Amino Acid ◽  
Plant Pathogens ◽  
Ustilago Maydis ◽  
Effector Proteins ◽  
Intraspecific Diversity ◽  
Close Relative ◽  
Host Immune System ◽  
Gene Repertoire ◽  
Effector Genes ◽  
Amino Acid Divergence

Plant pathogens secrete a variety of effector proteins that enable host colonization but are also typical pathogen detection targets for the host immune system. Consequently, effector genes encounter high selection pressures, which typically makes them fast evolving. The corn smut pathogen Ustilago maydis has an effector gene repertoire with a dynamic expression across the different disease stages. We determined the amino acid divergence of U. maydis effector candidates with Sporisorium reilianum orthologs, a close relative of U. maydis. Intriguingly, there are two distinct groups of effector candidates, ones with a respective conserved and diverged protein evolution. Conservatively evolving effector genes especially have their peak expression during the (pre-)penetration stages of the disease cycle. In contrast, expression of divergently evolving effector genes generally peaks during fungal proliferation within the host. To test if this interspecific effector diversity corresponds to intraspecific diversity, we sampled and sequenced a diverse collection of U. maydis strains from the most important maize breeding and production regions in China. Effector candidates with a diverged interspecific evolution had more intraspecific amino acid variation than candidates with a conserved evolution. In conclusion, we highlight diversity in evolution within the U. maydis effector repertoire with dynamically and conservatively evolving members.

scholarly journals Effectors with different gears: divergence of Ustilago maydis effector genes is associated with their temporal expression pattern during plant infection

2020 ◽  
Author(s):  
Jasper R.L. Depotter ◽  
Weiliang Zuo ◽  
Maike Hansen ◽  
Boqi Zhang ◽  
Mingliang Xu ◽  
...  
Keyword(s):  
Amino Acid ◽  
Plant Pathogens ◽  
Ustilago Maydis ◽  
Effector Proteins ◽  
Intraspecific Diversity ◽  
Close Relative ◽  
Host Immune System ◽  
Gene Repertoire ◽  
Effector Genes ◽  
Amino Acid Divergence

AbstractPlant pathogens secrete a variety of effector proteins that enable host colonization but are also typical pathogen detection targets for the host immune system. Consequently, effector genes encounter high selection pressures, which typically makes them fast evolving. The corn smut pathogen Ustilago maydis has an effector gene repertoire with a dynamic expression across the different disease stages. We determined the amino acid divergence of U. maydis effector candidates with Sporisorium reilianum orthologs, a close relative of U. maydis. Intriguingly, there are two distinct groups of effector candidates, ones with a respective conserved and diverged protein evolution. Conservatively evolving effector genes especially have their peak expression during the (pre-)penetration stages of the disease cycle. In contrast, expression of divergently evolving effector genes generally peaks during fungal proliferation within the host. To test if this interspecific effector diversity corresponds to intraspecific diversity, we sampled and sequenced a diverse collection of U. maydis strains from the most important maize breeding and production regions in China. Effector candidates with a diverged interspecific evolution had more intraspecific amino acid variation than candidates with a conserved evolution. In conclusion, we highlight diversity in evolution within the U. maydis effector repertoire with dynamically and conservatively evolving members.

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

PeerJ ◽  
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.

scholarly journals A Fungal Effector With Host Nuclear Localization and DNA-Binding Properties Is Required for Maize Anthracnose Development

2016 ◽  
Vol 29 (2) ◽  
pp. 83-95 ◽  
Author(s):  
Walter A. Vargas ◽  
José M. Sanz-Martín ◽  
Gabriel E. Rech ◽  
Vinicio D. Armijos-Jaramillo ◽  
Lina P. Rivera ◽  
...  
Keyword(s):  
Dna Binding ◽  
Nuclear Localization ◽  
Plant Pathogens ◽  
Effector Proteins ◽  
Host Immune System ◽  
Disease Development ◽  
Colletotrichum Graminicola ◽  
Double Stranded Dna ◽  
Colletotrichum Spp ◽  
Host Nucleus

Plant pathogens have the capacity to manipulate the host immune system through the secretion of effectors. We identified 27 putative effector proteins encoded in the genome of the maize anthracnose pathogen Colletotrichum graminicola that are likely to target the host’s nucleus, as they simultaneously contain sequence signatures for secretion and nuclear localization. We functionally characterized one protein, identified as CgEP1. This protein is synthesized during the early stages of disease development and is necessary for anthracnose development in maize leaves, stems, and roots. Genetic, molecular, and biochemical studies confirmed that this effector targets the host’s nucleus and defines a novel class of double-stranded DNA-binding protein. We show that CgEP1 arose from a gene duplication in an ancestor of a lineage of monocot-infecting Colletotrichum spp. and has undergone an intense evolution process, with evidence for episodes of positive selection. We detected CgEP1 homologs in several species of a grass-infecting lineage of Colletotrichum spp., suggesting that its function may be conserved across a large number of anthracnose pathogens. Our results demonstrate that effectors targeted to the host nucleus may be key elements for disease development and aid in the understanding of the genetic basis of anthracnose development in maize plants.

scholarly journals Positively selected effector genes and their contribution to virulence in the smut fungus Sporisorium reilianum

2017 ◽  
Author(s):  
Gabriel Schweizer ◽  
Karin Münch ◽  
Gertrud Mannhaupt ◽  
Jan Schirawski ◽  
Regine Kahmann ◽  
...  
Keyword(s):  
Positive Selection ◽  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Large Fraction ◽  
Gene Families ◽  
Effector Proteins ◽  
Smut Fungi ◽  
Formae Speciales ◽  
Effector Genes ◽  
Sporisorium Reilianum

AbstractPlants and fungi display a broad range of interactions in natural and agricultural ecosystems ranging from symbiosis to parasitism. These ecological interactions result in coevolution between genes belonging to different partners. A well-understood example are secreted fungal effector proteins and their host targets, which play an important role in pathogenic interactions. Biotrophic smut fungi (Basidiomycota) are well-suited to investigate the evolution of plant pathogens, because several reference genomes and genetic tools are available for these species. Here, we used the genomes of Sporisorium reilianum f. sp. zeae and S. reilianum f. sp. reilianum, two closely related formae speciales infecting maize and sorghum, respectively, together with the genomes of Ustilago hordei, Ustilago maydis and Sporisorium scitamineum to identify and characterize genes displaying signatures of positive selection. We identified 154 gene families having undergone positive selection during species divergence in at least one lineage, among which 77% were identified in the two investigated formae speciales of S. reilianum. Remarkably, only 29% of positively selected genes encode predicted secreted proteins. We assessed the contribution to virulence of nine of these candidate effector genes in S. reilianum f. sp. zeae by deleting individual genes, including a homologue of the effector gene pit2 previously characterized in U. maydis. Only the pit2 deletion mutant was found to be strongly reduced in virulence. Additional experiments are required to understand the molecular mechanisms underlying the selection forces acting on the other candidate effector genes, as well as the large fraction of positively selected genes encoding predicted cytoplasmic proteins.

scholarly journals Population genomics of the maize pathogen Ustilago maydis: demographic history and role of virulence clusters in adaptation

2020 ◽  
Author(s):  
Gabriel Schweizer ◽  
Muhammad Bilal Haider ◽  
Gustavo V. Barroso ◽  
Nicole Rössel ◽  
Karin Münch ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Cell Biology ◽  
Plant Pathogens ◽  
Demographic History ◽  
Ustilago Maydis ◽  
Adaptive Mutations ◽  
Effector Genes ◽  
Genome Wide ◽  
History Of ◽  
Maize Domestication

AbstractThe tight interaction between pathogens and their hosts results in reciprocal selective forces that impact the genetic diversity of the interacting species. The footprints of this selection differ between pathosystems because of distinct life-history traits, demographic histories, or genome architectures. Here, we studied the genome-wide patterns of genetic diversity of 22 isolates of the causative agent of the corn smut disease, Ustilago maydis, originating from five locations in Mexico, the presumed center of origin of this species. In this species, many genes encoding secreted effector proteins reside in so-called virulence clusters in the genome, an arrangement that is so far not found in other filamentous plant pathogens. Using a combination of population genomic statistical analyses, we assessed the geographical, historical and genome-wide variation of genetic diversity in this fungal pathogen.We report evidence of two partially admixed subpopulations that are only loosely associated with geographic origin. Using the multiple sequentially Markov coalescent model, we inferred the demographic history of the two pathogen subpopulations over the last 0.5 million years. We show that both populations experienced a recent strong bottleneck starting around 10,000 years ago, coinciding with the assumed time of maize domestication. While the genome average genetic diversity is low compared to other fungal pathogens, we estimated that the rate of non-synonymous adaptive substitutions is three times higher in genes located within virulence clusters compared to non-clustered genes, including non-clustered effector genes. These results highlight the role that these singular genomic regions play in the evolution of this pathogen.Significance statementThe maize pathogen Ustilago maydis is a model species to study fungal cell biology and biotrophic host-pathogen interactions. Population genetic studies of this species, however, were so far restricted to using a few molecular markers, and genome-wide comparisons involved species that diverged more than 20 million years ago. Here, we sequenced the genomes of 22 Mexican U. maydis isolates to study the recent evolutionary history of this species. We identified two co-existing populations that went through a recent bottleneck and whose divergence date overlaps with the time of maize domestication. Contrasting the patterns of genetic diversity in different categories of genes, we further showed that effector genes in virulence clusters display a high rate of adaptive mutations, highlighting the importance of these effector arrangements for the adaptation of U. maydis to its host.

scholarly journals The Pleiades cluster of fungal effector genes inhibit host defenses

2019 ◽  
Author(s):  
Fernando Navarrete ◽  
Nenad Grujic ◽  
Alexandra Stirnberg ◽  
David Aleksza ◽  
Michelle Gallei ◽  
...  
Keyword(s):  
Plant Pathogens ◽  
Functional Characterization ◽  
Rapid Evolution ◽  
Effector Proteins ◽  
Host Defenses ◽  
E3 Ligases ◽  
Effector Genes ◽  
Ros Burst ◽  
Molecular Patterns

SummaryBiotrophic plant pathogens secrete effector proteins to manipulate the host physiology. Effectors suppress defenses and induce an environment favorable to disease development. Sequence-based prediction of effector function is difficulted by their rapid evolution rate. In the maize pathogen Ustilago maydis, effector-coding genes frequently organize in clusters. Here we describe the functional characterization of the pleiades, a cluster of ten symplastic effectors. Deletion of the pleiades leads to strongly impaired virulence and accumulation of reactive oxygen species (ROS) in infected tissue. Eight of the Pleiades suppress the production of ROS upon perception of pathogen associated molecular patterns (PAMPs). Although genetically redundant, the Pleiades target different host components. The paralogs Taygeta1 and Merope1 suppress ROS production in either the cytoplasm or nucleus, respectively. Merope1 targets and promotes the autoubiquitination activity of RFI2, a conserved family of E3 ligases that regulates the production of PAMP-triggered ROS burst and influences flowering time in plants.

scholarly journals Comparative genomics of Alexander Fleming’s original Penicillium isolate (IMI 15378) reveals sequence divergence of penicillin synthesis genes

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Ayush Pathak ◽  
Reuben W. Nowell ◽  
Christopher G. Wilson ◽  
Matthew J. Ryan ◽  
Timothy G. Barraclough
Keyword(s):  
Amino Acid ◽  
Draft Genome ◽  
Sequence Divergence ◽  
Regulatory Genes ◽  
Penicillin G ◽  
Antimicrobial Drugs ◽  
Effector Genes ◽  
Amino Acid Divergence ◽  
Industrial Strains ◽  
In The Wild

Abstract Antibiotics were derived originally from wild organisms and therefore understanding how these compounds evolve among different lineages might help with the design of new antimicrobial drugs. We report the draft genome sequence of Alexander Fleming’s original fungal isolate behind the discovery of penicillin, now classified as Penicillium rubens Biourge (1923) (IMI 15378). We compare the structure of the genome and genes involved in penicillin synthesis with those in two ‘high producing’ industrial strains of P. rubens and the closely related species P. nalgiovense. The main effector genes for producing penicillin G (pcbAB, pcbC and penDE) show amino acid divergence between the Fleming strain and both industrial strains, whereas a suite of regulatory genes are conserved. Homologs of penicillin N effector genes cefD1 and cefD2 were also found and the latter displayed amino acid divergence between the Fleming strain and industrial strains. The draft assemblies contain several partial duplications of penicillin-pathway genes in all three P. rubens strains, to differing degrees, which we hypothesise might be involved in regulation of the pathway. The two industrial strains are identical in sequence across all effector and regulatory genes but differ in duplication of the pcbAB–pcbC–penDE complex and partial duplication of fragments of regulatory genes. We conclude that evolution in the wild encompassed both sequence changes of the effector genes and gene duplication, whereas human-mediated changes through mutagenesis and artificial selection led to duplication of the penicillin pathway genes.

scholarly journals The Pleiades are a cluster of fungal effectors that inhibit host defenses

2021 ◽  
Vol 17 (6) ◽  
pp. e1009641
Author(s):  
Fernando Navarrete ◽  
Nenad Grujic ◽  
Alexandra Stirnberg ◽  
Indira Saado ◽  
David Aleksza ◽  
...  
Keyword(s):  
Plant Pathogens ◽  
Functional Characterization ◽  
Rapid Evolution ◽  
Effector Proteins ◽  
In Planta ◽  
E3 Ligases ◽  
Effector Genes ◽  
Ros Burst ◽  
Molecular Patterns

Biotrophic plant pathogens secrete effector proteins to manipulate the host physiology. Effectors suppress defenses and induce an environment favorable to disease development. Sequence-based prediction of effector function is impeded by their rapid evolution rate. In the maize pathogen Ustilago maydis, effector-coding genes frequently organize in clusters. Here we describe the functional characterization of the pleiades, a cluster of ten effector genes, by analyzing the micro- and macroscopic phenotype of the cluster deletion and expressing these proteins in planta. Deletion of the pleiades leads to strongly impaired virulence and accumulation of reactive oxygen species (ROS) in infected tissue. Eight of the Pleiades suppress the production of ROS upon perception of pathogen associated molecular patterns (PAMPs). Although functionally redundant, the Pleiades target different host components. The paralogs Taygeta1 and Merope1 suppress ROS production in either the cytoplasm or nucleus, respectively. Merope1 targets and promotes the auto-ubiquitination activity of RFI2, a conserved family of E3 ligases that regulates the production of PAMP-triggered ROS burst in plants.

scholarly journals Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity

2017 ◽  
Vol 81 (2) ◽  
Author(s):  
Marina Franceschetti ◽  
Abbas Maqbool ◽  
Maximiliano J. Jiménez-Dalmaroni ◽  
Helen G. Pennington ◽  
Sophien Kamoun ◽  
...  
Keyword(s):  
Plant Pathogens ◽  
Structural Integrity ◽  
Sequence Similarity ◽  
Large Fraction ◽  
Parasitic Infection ◽  
Effector Proteins ◽  
Host Cells ◽  
Effector Genes ◽  
Filamentous Microorganisms ◽  
Domain Integration

SUMMARY Fungi and oomycetes are filamentous microorganisms that include a diversity of highly developed pathogens of plants. These are sophisticated modulators of plant processes that secrete an arsenal of effector proteins to target multiple host cell compartments and enable parasitic infection. Genome sequencing revealed complex catalogues of effectors of filamentous pathogens, with some species harboring hundreds of effector genes. Although a large fraction of these effector genes encode secreted proteins with weak or no sequence similarity to known proteins, structural studies have revealed unexpected similarities amid the diversity. This article reviews progress in our understanding of effector structure and function in light of these new insights. We conclude that there is emerging evidence for multiple pathways of evolution of effectors of filamentous plant pathogens but that some families have probably expanded from a common ancestor by duplication and diversification. Conserved folds, such as the oomycete WY and the fungal MAX domains, are not predictive of the precise function of the effectors but serve as a chassis to support protein structural integrity while providing enough plasticity for the effectors to bind different host proteins and evolve unrelated activities inside host cells. Further effector evolution and diversification arise via short linear motifs, domain integration and duplications, and oligomerization.

scholarly journals Deciphering the Monilinia fructicola Genome to Discover Effector Genes Possibly Involved in Virulence

Genes ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 568
Author(s):  
Laura Vilanova ◽  
Claudio A. Valero-Jiménez ◽  
Jan A.L. van Kan
Keyword(s):  
Brown Rot ◽  
Biological Properties ◽  
Effector Proteins ◽  
Stone Fruit ◽  
Rna Seq ◽  
Sequencing Technology ◽  
Pathogen Virulence ◽  
Effector Genes ◽  
Gene Models ◽  
High Quality Genome

Brown rot is the most economically important fungal disease of stone fruits and is primarily caused by Monilinia laxa and Monlinia fructicola. Both species co-occur in European orchards although M. fructicola is considered to cause the most severe yield losses in stone fruit. This study aimed to generate a high-quality genome of M. fructicola and to exploit it to identify genes that may contribute to pathogen virulence. PacBio sequencing technology was used to assemble the genome of M. fructicola. Manual structural curation of gene models, supported by RNA-Seq, and functional annotation of the proteome yielded 10,086 trustworthy gene models. The genome was examined for the presence of genes that encode secreted proteins and more specifically effector proteins. A set of 134 putative effectors was defined. Several effector genes were cloned into Agrobacterium tumefaciens for transient expression in Nicotiana benthamiana plants, and some of them triggered necrotic lesions. Studying effectors and their biological properties will help to better understand the interaction between M. fructicola and its stone fruit host plants.

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