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 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 Cause and Effectors: Whole-Genome Comparisons Reveal Shared but Rapidly Evolving Effector Sets among Host-Specific Plant-Castrating Fungi

mBio ◽  
2019 ◽  
Vol 10 (6) ◽  
Author(s):  
William C. Beckerson ◽  
Ricardo C. Rodríguez de la Vega ◽  
Fanny E. Hartmann ◽  
Marine Duhamel ◽  
Tatiana Giraud ◽  
...  
Keyword(s):  
Positive Selection ◽  
Plant Pathogens ◽  
Pfam Domain ◽  
Rapid Evolution ◽  
Host Specialization ◽  
Secreted Proteins ◽  
Smut Fungi ◽  
Core Proteins ◽  
Genes Encoding ◽  
Species Specific

ABSTRACT Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi (Microbotryum), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed in planta; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all Microbotryum species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses. IMPORTANCE Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons.

scholarly journals Host targets of effectors of the lettuce downy mildew Bremia lactucae from cDNA-based yeast two-hybrid screening

2019 ◽  
Author(s):  
Alexandra J.E. Pelgrom ◽  
Claudia-Nicole Meisrimler ◽  
Joyce Elberse ◽  
Thijs Koorman ◽  
Mike Boxem ◽  
...  
Keyword(s):  
Downy Mildew ◽  
Pathogenic Bacteria ◽  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Effector Proteins ◽  
Bremia Lactucae ◽  
Yeast Two Hybrid ◽  
Target Proteins ◽  
Successful Infection ◽  
Two Hybrid

AbstractPlant pathogenic bacteria, fungi and oomycetes secrete effector proteins to manipulate host cell processes to establish a successful infection. Over the last decade the genomes and transcriptomes of many agriculturally important plant pathogens have been sequenced and vast candidate effector repertoires were identified using bioinformatic analyses. Elucidating the contribution of individual effectors to pathogenicity is the next major hurdle. To advance our understanding of the molecular mechanisms underlying lettuce susceptibility to the downy mildew Bremia lactucae, we mapped a network of physical interactions between B. lactucae effectors and lettuce target proteins. Using a lettuce cDNA library-based yeast-two-hybrid system, 61 protein-protein interactions were identified, involving 21 B. lactucae effectors and 46 unique lettuce proteins. The top ten targets based on the number of independent colonies identified in the Y2H and two targets that belong to gene families involved in plant immunity, were further characterized. We determined the subcellular localization of the fluorescently tagged target proteins and their interacting effectors. Importantly, relocalization of effectors or targets to the nucleus was observed for four effector-target pairs upon their co-expression, supporting their interaction in planta.

scholarly journals Cross-species analysis between the maize smut fungi Ustilago maydis and Sporisorium reilianum highlights the role of transcriptional plasticity of effector orthologs for virulence and disease

2020 ◽  
Author(s):  
Weiliang Zuo ◽  
Deepak K Gupta ◽  
Jasper RL Depotter ◽  
Marco Thines ◽  
Gunther Doehlemann
Keyword(s):  
Ustilago Maydis ◽  
Effector Proteins ◽  
Differentially Expressed ◽  
Transcriptional Level ◽  
Smut Fungi ◽  
List Type ◽  
Sequencing Analysis ◽  
Distinct Disease ◽  
Sporisorium Reilianum ◽  
Transcriptional Plasticity

SummaryThe constitution and regulation of effector repertoires determines and shapes the outcome of the interaction with the host. Ustilago maydis and Sporisorium reilianum are two closely related smut fungi, which both infect maize, but cause distinct disease symptoms. Understanding how effector orthologs are regulated in these two pathogens can therefore provide insights to pathogen evolution and host adaption.We tracked the infection progress of U. maydis and S. reilianum in maize leaves, characterized two distinct infection stages for cross species RNA-sequencing analysis and identified 207 out of 335 one-to-one effector orthologs being differentially regulated during host colonization, while transcriptional plasticity of the effector orthologs correlated with the distinct disease development strategies.By using CRISPR-Cas9 mediated gene conversion, we identified two differentially expressed effector orthologs with conserved function between two pathogens. Thus, differential expression of functionally conserved genes contributes to species specific adaptation and symptom development. Interestingly, another differentially expressed orthogroup (UMAG_05318/sr1007) showed diverged protein function during speciation, providing a possible case for neofunctionalization.Together, we showed the diversification of effector genes in related pathogens can be caused both by plasticity on the transcriptional level, as well as through neofunctionalization of the encoded effector proteins.

scholarly journals Molecular mechanisms of host cell manipulation by plant pathogens

2014 ◽  
Vol 70 (a1) ◽  
pp. C801-C801
Author(s):  
Richard Hughes ◽  
Stuart King ◽  
Abbas Maqbool ◽  
Hazel McLellan ◽  
Tolga Bozkurt ◽  
...  
Keyword(s):  
Cell Death ◽  
Crop Production ◽  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Complex Structure ◽  
Effector Proteins ◽  
Plant Diseases ◽  
Cell Manipulation ◽  
Cell Physiology ◽  
Structural Studies

An estimated 15% of global crop production is lost to pre-harvest disease every year. New ways to manage plant diseases are required. A mechanistic understanding of how plant pathogens re-program their hosts to enable colonisation may provide novel genetic or chemical opportunities to interfere with disease. One notorious plant parasite is the Irish potato famine pathogen Phytophthora infestans. This pathogen remains a considerable threat to potato/tomato crops today as the agent of late blight. Plant pathogens secrete effector proteins outside of and into plant cells to suppress host defences and manipulate cell physiology. Structural studies have provided insights into effector evolution and enabled experiments to probe function [1-3]. Crystal structures of 4 Phytophthora RXLR-type effectors, which are unrelated in primary sequence, revealed similarities in the fold of these proteins. This fold was proposed to act as a stable scaffold that supports diversification of effectors. Further, molecular modelling has enabled mapping of single-site variants responsible for specialisation of a Phytophthora Cystatin-like effector, revealing how effectors can adapt to new hosts after a "host jump". Structural studies describing how RXLR-effectors interact with host targets are lacking. We have used Y2H/co-IP studies to identify host proteins that interact with P. infestans effectors PexRD2 and PexRD54. PexRD2 interacts with MAPKKKe, a component of plant immune signalling pathways, and suppressed cell death activities of this protein. We used the structure of PexRD2 to design mutants that fail to interact with MAPKKKe, and no longer suppress cell-death activities. We found that PexRD54 interacts with potato homologues of the autophagy protein ATG8. We have obtained a crystal structure for PexRD54 in the presence of ATG8. We are now using X-ray scattering to verify the complex structure in solution prior to establishing the role of this interaction during infection.

scholarly journals Effector proteins of extracellular fungal plant pathogens that trigger host resistance

2010 ◽  
Vol 37 (10) ◽  
pp. 901 ◽  
Author(s):  
Ann-Maree Catanzariti ◽  
David A. Jones
Keyword(s):  
Biological Activity ◽  
Host Resistance ◽  
Fungal Pathogens ◽  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Host Tissue ◽  
Effector Proteins ◽  
Resistance Proteins ◽  
Recognitional Capacity ◽  
Fungal Plant Pathogens

An understanding of the molecular mechanisms that plant pathogens use to successfully colonise host tissue can be gained by studying the biological activity of pathogen proteins secreted during infection. Several secreted ‘effector’ proteins with possible roles in virulence have been isolated from extracellular fungal pathogens, including three that have been shown to negate host defences. In most cases, significant effector variation is observed between different pathogen isolates, driven by the recognitional capacity of disease resistance proteins arrayed against the pathogen by the host plant. This review summarises what is known about the expression, function and variation of effectors isolated from extracellular fungal pathogens.

scholarly journals YopJ Family Effectors Promote Bacterial Infection through a Unique Acetyltransferase Activity

2016 ◽  
Vol 80 (4) ◽  
pp. 1011-1027 ◽  
Author(s):  
Ka-Wai Ma ◽  
Wenbo Ma
Keyword(s):  
Plant Pathogens ◽  
Molecular Mechanisms ◽  
Bacterial Species ◽  
Cysteine Proteases ◽  
Catalytic Triad ◽  
Effector Proteins ◽  
Host Cells ◽  
Target Proteins ◽  
Acetyltransferase Activity ◽  
Type Iii

SUMMARYGram-negative bacterial pathogens rely on the type III secretion system to inject virulence proteins into host cells. These type III secreted “effector” proteins directly manipulate cellular processes to cause disease. Although the effector repertoires in different bacterial species are highly variable, theYersiniaouter protein J (YopJ) effector family is unique in that its members are produced by diverse animal and plant pathogens as well as a nonpathogenic microsymbiont. All YopJ family effectors share a conserved catalytic triad that is identical to that of the C55 family of cysteine proteases. However, an accumulating body of evidence demonstrates that many YopJ effectors modify their target proteins in hosts by acetylating specific serine, threonine, and/or lysine residues. This unique acetyltransferase activity allows the YopJ family effectors to affect the function and/or stability of their targets, thereby dampening innate immunity. Here, we summarize the current understanding of this prevalent and evolutionarily conserved type III effector family by describing their enzymatic activities and virulence functions in animals and plants. In particular, the molecular mechanisms by which representative YopJ family effectors subvert host immunity through posttranslational modification of their target proteins are discussed.

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 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.

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