Fungi are among the dominant causal agents of plant diseases. To colonize plants and cause disease, pathogenic fungi use diverse strategies. Some fungi kill their hosts and feed on dead material ...(necrotrophs), while others colonize the living tissue (biotrophs). For successful invasion of plant organs, pathogenic development is tightly regulated and specialized infection structures are formed. To further colonize hosts and establish disease, fungal pathogens deploy a plethora of virulence factors. Depending on the infection strategy, virulence factors perform different functions. While basically all pathogens interfere with primary plant defense, necrotrophs secrete toxins to kill plant tissue. In contrast, biotrophs utilize effector molecules to suppress plant cell death and manipulate plant metabolism in favor of the pathogen. This article provides an overview of plant pathogenic fungal species and the strategies they use to cause disease.
•The manuscript is on the fundamental mechanisms that shape biotrophic interactions.•Biotrophic model organisms Cladosporium fulvum and Ustilago maydis are highlighted.•Limited number of host ...proteins (hubs) is addressed by unrelated pathogens.•Intracellular pathogens address more targets compared to apoplastic interactions.
Filamentous plant pathogens that establish biotrophic interactions need to avoid plant immune responses. Recent findings from different pathosystems suggest that sufficient suppression of host immunity is based on the modulation of a rather limited number of host targets. Microbial strategies to target host physiology dependent on the duration of biotrophy, the style of host tissue colonization and the degree of interference with plant development. In this article, we present current concepts in biotrophic virulence strategies and discuss mechanisms of pathogen adaptation and effector specialization.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK
Ustilago maydis is a biotrophic fungus causing corn smut disease in maize. The secreted effector protein Pit2 is an inhibitor of papain-like cysteine proteases (PLCPs) essential for virulence. Pit2 ...inhibitory function relies on a conserved 14 amino acids motif (PID14). Here we show that synthetic PID14 peptides act more efficiently as PLCP inhibitors than the full-length Pit2 effector. Mass spectrometry shows processing of Pit2 by maize PLCPs, which releases an inhibitory core motif from the PID14 sequence. Mutational analysis demonstrates that two conserved residues are essential for Pit2 function. We propose that the Pit2 effector functions as a substrate mimicking molecule: Pit2 is a suitable substrate for apoplastic PLCPs and its processing releases the embedded inhibitor peptide, which in turn blocks PLCPs to modulate host immunity. Remarkably, the PID14 core motif is present in several plant associated fungi and bacteria, indicating the existence of a conserved microbial inhibitor of proteases (cMIP).
During host colonization, plant-associated microbes, including fungi and oomycetes, deliver a collection of glycoside hydrolases (GHs) to their cell surfaces and surrounding extracellular ...environments. The number and type of GHs secreted by each organism is typically associated with their lifestyle or mode of nutrient acquisition. Secreted GHs of plant-associated fungi and oomycetes serve a number of different functions, with many of them acting as virulence factors (effectors) to promote microbial host colonization. Specific functions involve, for example, nutrient acquisition, the detoxification of antimicrobial compounds, the manipulation of plant microbiota, and the suppression or prevention of plant immune responses. In contrast, secreted GHs of plant-associated fungi and oomycetes can also activate the plant immune system, either by acting as microbe-associated molecular patterns (MAMPs), or through the release of damage-associated molecular patterns (DAMPs) as a consequence of their enzymatic activity. In this review, we highlight the critical roles that secreted GHs from plant-associated fungi and oomycetes play in plant-microbe interactions, provide an overview of existing knowledge gaps and summarize future directions.
Clash between the borders Ökmen, Bilal; Doehlemann, Gunther
The New phytologist,
December 2016, Volume:
212, Issue:
4
Journal Article
Peer reviewed
Open access
This article is a Commentary on De Wit, 212: 805–813; Derevnina et al., 212: 888–895; Rovenich et al., 212: 896–901 and Misas‐Villamil et al., 212: 902–907.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Fungalysins from several phytopathogenic fungi have been shown to be involved in cleavage of plant chitinases. While fungal chitinases are responsible for cell wall remodeling during growth and ...morphogenesis, plant chitinases are important components of immunity. This study describes a dual function of the Ustilago maydis fungalysin UmFly1 in modulation of both plant and fungal chitinases.
Genetic, biochemical and microscopic experiments were performed to elucidate the in vitro and in planta functions of U. maydis UmFly1.
U. maydis Δumfly1 mutants show significantly reduced virulence, which coincides with reduced cleavage of the maize chitinase ZmChiA within its chitin-binding domain. Moreover, deletion of umfly1 affected the cell separation of haploid U. maydis sporidia. This phenotype is associated with posttranslational activation of the endogenous chitinase UmCts1. Genetic complementation of the Δumfly1 mutant with a homologous gene from closely related, but nonpathogenic, yeast fully rescued the cell separation defect in vitro, but it could not recover the Δumfly1 defect in virulence and cleavage of the maize chitinase.
We report on the dual function of the secreted fungalysin UmFly1. We hypothesize that co-evolution of U. maydis with its host plant extended the endogenous function of UmFly1 towards the modulation of plant chitinase activity to promote infection.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Summary
The success of plant‐pathogenic fungi mostly relies on their arsenal of virulence factors which are expressed and delivered into the host tissue during colonization. The biotrophic fungal ...pathogen Ustilago hordei causes covered smut disease on both barley and oat. In this study, we combined cytological, genomics and molecular biological methods to achieve a better understanding of the molecular interactions in the U. hordei–barley pathosystem. Microscopic analysis revealed that U. hordei densely colonizes barley leaves on penetration, in particular the vascular system. Transcriptome analysis of U. hordei at different stages of host infection revealed differential expression of the transcript levels of 273 effector gene candidates. Furthermore, U. hordei transcriptionally activates core effector genes which may suppress even non‐host early defence responses. Based on expression profiles and novelty of sequences, knockout studies of 14 effector candidates were performed in U. hordei, which resulted in the identification of four virulence factors required for host colonization. Yeast two‐hybrid screening identified potential barley targets for two of the effectors. Overall, this study provides a first systematic analysis of the effector repertoire of U. hordei and identifies four effectors (Uvi1–Uvi4) as virulence factors for the infection of barley.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
Abstract
Smut fungi comprise one of the largest groups of fungal plant pathogens causing disease in all cereal crops. They directly penetrate host tissues and establish a biotrophic interaction. To ...do so, smut fungi secrete a wide range of effector proteins, which suppress plant immunity and modulate cellular functions as well as development of the host, thereby determining the pathogen’s lifestyle and virulence potential. The conserved effector Erc1 (enzyme required for cell-to-cell extension) contributes to virulence of the corn smut
Ustilago maydis
in maize leaves but not on the tassel. Erc1 binds to host cell wall components and displays 1,3-β-glucanase activity, which is required to attenuate β-glucan-induced defense responses. Here we show that Erc1 has a cell type-specific virulence function, being necessary for fungal cell-to-cell extension in the plant bundle sheath and this function is fully conserved in the Erc1 orthologue of the barley pathogen
Ustilago hordei
.
Most fungal effectors characterized so far are species-specific and facilitate virulence on a particular host plant. During infection of its host tomato, Cladosporium fulvum secretes effectors that ...function as virulence factors in the absence of cognate Cf resistance proteins and induce effector-triggered immunity in their presence. Here we show that homologs of the C. fulvum Avr4 and Ecp2 effectors are present in other pathogenic fungi of the Dothideomycete class, including Mycosphaerella fijiensis, the causal agent of black Sigatoka disease of banana. We demonstrate that the Avr4 homolog of M. fijiensis is a functional ortholog of C. fulvum Avr4 that protects fungal cell walls against hydrolysis by plant chitinases through binding to chitin and, despite the low overall sequence homology, triggers a Cf-4-mediated hypersensitive response (HR) in tomato. Furthermore, three homologs of C. fulvum Ecp2 are found in M. fijiensis, one of which induces different levels of necrosis or HR in tomato lines that lack or contain a putative cognate Cf-Ecp2 protein, respectively. In contrast to Avr4, which acts as a defensive virulence factor, M. fijiensis Ecp2 likely promotes virulence by interacting with a putative host target causing host cell necrosis, whereas Cf-Ecp2 could possibly guard the virulence target of Ecp2 and trigger a Cf-Ecp2-mediated HR. Overall our data suggest that Avr4 and Ecp2 represent core effectors that are collectively recognized by single cognate Cf-proteins. Transfer of these Cf genes to plant species that are attacked by fungi containing these cognate core effectors provides unique ways for breeding disease-resistant crops.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Excessive soil salinity is an important problem for agriculture, however, salt tolerance is a complex trait that is not easily bred into plants. Exposure of cultivated tomato to salt stress has been ...reported to result in increased antioxidant content and activity. Salt tolerance of the related wild species, Solanum pennellii, has also been associated with similar changes in antioxidants. In this work, S. lycopersicum M82, S. pennellii LA716 and a S. pennellii introgression line (IL) population were evaluated for growth and their levels of antioxidant activity (total water-soluble antioxidant activity), major antioxidant compounds (phenolic and flavonoid contents) and antioxidant enzyme activities (superoxide dismutase, catalase, ascorbate peroxidase and peroxidase) under both control and salt stress (150 mM NaCl) conditions. These data were then used to identify quantitative trait loci (QTL) responsible for controlling the antioxidant parameters under both stress and nonstress conditions.
Under control conditions, cultivated tomato had higher levels of all antioxidants (except superoxide dismutase) than S. pennellii. However, under salt stress, the wild species showed greater induction of all antioxidants except peroxidase. The ILs showed diverse responses to salinity and proved very useful for the identification of QTL. Thus, 125 loci for antioxidant content under control and salt conditions were detected. Eleven of the total antioxidant activity and phenolic content QTL matched loci identified in an independent study using the same population, thereby reinforcing the validity of the loci. In addition, the growth responses of the ILs were evaluated to identify lines with favorable growth and antioxidant profiles.
Plants have a complex antioxidant response when placed under salt stress. Some loci control antioxidant content under all conditions while others are responsible for antioxidant content only under saline or nonsaline conditions. The localization of QTL for these traits and the identification of lines with specific antioxidant and growth responses may be useful for breeding potentially salt tolerant tomato cultivars having higher antioxidant levels under nonstress and salt stress conditions.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
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