Abstract:Biotrophic fungal plant pathogens establish an intimate relationship with their host to support the infection process. Central to this strategy is the secretion of a range of protein effectors that enable the pathogen to evade plant immune defences and modulate host metabolism to meet its needs. In this Review, using the smut fungus Ustilago maydis as an example, we discuss new insights into the effector repertoire of smut fungi that have been gained from comparative genomics and discuss the molecular mechanis… Show more
“…Furthermore, most effectors lack conserved functional domains as well as orthologs outside the genus (Win et al, ). Many effector proteins are cysteine‐rich and presumably able to form disulfide bonds to stabilize their tertiary structure in the harsh oxidative conditions of the plant apoplast (Lanver et al, ; Win et al, ).…”
Section: Introductionmentioning
confidence: 99%
“…In many cases, however, deletion of a single effector or even a whole cluster does not affect U. maydis virulence, presumably due to functional redundancy. U. maydis also contains core effectors, which are highly conserved among smut fungi and are likely to play a crucial role in the infection process (Lanver et al, ).…”
The biotrophic pathogen Ustilago maydis, the causative agent of corn smut disease, infects one of the most important crops worldwide - Zea mays. To successfully colonize its host, U. maydis secretes proteins, known as effectors, that suppress plant defense responses and facilitate the establishment of biotrophy. In this work, we describe the U. maydis effector protein Cce1. Cce1 is essential for virulence and is upregulated during infection. Through microscopic analysis and in vitro assays, we show that Cce1 is secreted from hyphae during filamentous growth of the fungus. Strikingly, Δcce1 mutants are blocked at early stages of infection and induce callose deposition as a plant defense response. Cce1 is highly conserved among smut fungi and the Ustilago bromivora ortholog complemented the virulence defect of the SG200Δcce1 deletion strain. These data indicate that Cce1 is a core effector with apoplastic localization that is essential for U. maydis to infect its host.
“…Furthermore, most effectors lack conserved functional domains as well as orthologs outside the genus (Win et al, ). Many effector proteins are cysteine‐rich and presumably able to form disulfide bonds to stabilize their tertiary structure in the harsh oxidative conditions of the plant apoplast (Lanver et al, ; Win et al, ).…”
Section: Introductionmentioning
confidence: 99%
“…In many cases, however, deletion of a single effector or even a whole cluster does not affect U. maydis virulence, presumably due to functional redundancy. U. maydis also contains core effectors, which are highly conserved among smut fungi and are likely to play a crucial role in the infection process (Lanver et al, ).…”
The biotrophic pathogen Ustilago maydis, the causative agent of corn smut disease, infects one of the most important crops worldwide - Zea mays. To successfully colonize its host, U. maydis secretes proteins, known as effectors, that suppress plant defense responses and facilitate the establishment of biotrophy. In this work, we describe the U. maydis effector protein Cce1. Cce1 is essential for virulence and is upregulated during infection. Through microscopic analysis and in vitro assays, we show that Cce1 is secreted from hyphae during filamentous growth of the fungus. Strikingly, Δcce1 mutants are blocked at early stages of infection and induce callose deposition as a plant defense response. Cce1 is highly conserved among smut fungi and the Ustilago bromivora ortholog complemented the virulence defect of the SG200Δcce1 deletion strain. These data indicate that Cce1 is a core effector with apoplastic localization that is essential for U. maydis to infect its host.
“…smut (Rabe et al ., ). In addition, functional analysis in U. maydis confirmed the contribution of single effector proteins to fungal virulence (Lanver et al ., ). For example, Pep1, a protein essential for fungal penetration, was initially identified outside of the effector clusters and was characterized as an apoplastic peroxidase inhibitor (Doehlemann et al ., ; Hemetsberger et al ., ), which is conserved in several grass smut species as well as the dicot‐infecting smut Melanopsichium pennsylvanicum (Hemetsberger et al ., ).…”
Summary
Biotrophic fungal plant pathogens can balance their virulence and form intricate relationships with their hosts. Sometimes, this leads to systemic host colonization over long time scales without macroscopic symptoms. However, how plant‐pathogenic endophytes manage to establish their sustained systemic infection remains largely unknown.
Here, we present a genomic and transcriptomic analysis of Thecaphora thlaspeos. This relative of the well studied grass smut Ustilago maydis is the only smut fungus adapted to Brassicaceae hosts. Its ability to overwinter with perennial hosts and its systemic plant infection including roots are unique characteristics among smut fungi.
The T. thlaspeos genome was assembled to the chromosome level. It is a typical smut genome in terms of size and genome characteristics. In silico prediction of candidate effector genes revealed common smut effector proteins and unique members. For three candidates, we have functionally demonstrated effector activity. One of these, TtTue1, suggests a potential link to cold acclimation. On the plant side, we found evidence for a typical immune response as it is present in other infection systems, despite the absence of any macroscopic symptoms during infection.
Our findings suggest that T. thlaspeos distinctly balances its virulence during biotrophic growth ultimately allowing for long‐lived infection of its perennial hosts.
“…Initially totally encased by the plant's plasma membrane, the fungus then grows into the mesophyll and nutrient-rich vascular tissue of its host. The infected plant cells divide rapidly and enlarge, forming tumors that are filled with fungal hyphae and, with time, fungal spores (Lanver et al, 2017).…”
mentioning
confidence: 99%
“…Many of the 476 effectors secreted by U. maydis lack established structural or functional domains (Schuster et al, 2017), and only 5 of these have been characterized in detail (Lanver et al, 2017). Characterizing the remaining effectors and pinpointing the stages of infection at which they are active would this fungus, and possibly suggest ways to contain it.…”
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