Biotrophic fungal plant pathogens cause billions of dollars in losses to north american crops annually. To test the impact of pep1 on maize peroxidases, apoplastic fluid of maize leaves was isolated. Apr 15, 2019 by genetic complementation, we show that pep1 homologs from the supposedly apathogenic yeasts restore virulence in pep1 deficient mutants ustilago maydis. The fungal core effector p ep1 is conserved across. Expressedsequence tag libraries and microarray hybridizations have provided insight regarding.
Jan 01, 2012 ustilago maydis is a basidiomycete that infects corn and serves as an excellent model for plant pathogenicity banuett, 1995. Hemetsberger c, herrberger c, zechmann b, hillmer m, doehlemann g 2012 the ustilago maydis effector pep1 suppresses plant immunity by inhibition of host peroxidase activity. The pep1 gene um01987 resides on chromosome 3 of the u. The deletion mutants for these regions demonstrate participation in fungal virulence kamper et al. A secreted effector protein of ustilago maydis guides maize leaf cells to form tumors. Ustilagohordei is a member of the order ustilaginales, which contains pathogens of several economically important crops, such as maize, wheat, oat, barley and sugar cane. Jan 28, 2014 the fungus ustilago maydis is one such biotrophic pathogen that colonizes maize plants and causes a disease called corn smut. Pep1, a secreted effector protein of ustilago maydis,is. A secreted effector protein of ustilago maydis guides maize leaf cells to form tumors amey redkar,a,1 rafal hoser,b lena schilling,a bernd zechmann,c magdalena krzymowska,b virginia walbot,d and gunther doehlemanna,e,2 a max planck institute for terrestrial microbiology, department of organismic interactions, d35043 marburg, germany b institute of biochemistry and biophysics, polish academy. We identified a novel secreted protein, termed pep1, that is essential for. Pep1, which inhibits plant peroxidases, and pit2, which. We could show that pep1 directly inhibits plant peroxidases. To identify pathogenesisrelated proteins in ustilago maydis.
Degradation of the plant defence hormone salicylic acid by. Cas9hf1 enhanced specificity in ustilago maydis sciencedirect. Ustilago hordei is a facultative biotrophic fungal pathogen that causes covered smut disease on both barley and oat plants gaudet et al. Thus, it is concluded that pseudozyma species have likely retained a suite of effectors, which hints at the possibility that pseudozyma species have kept an unknown plant pathogenic stage for. Extracellular effector proteins are thought to play a crucial role in establishing a successful infection. Pep1 function is conserved in the ustilago hordei barley interaction after 454 sequencing of the genome of the barley covered smut fungus ustilago hordei j. A secreted ustilago maydis effector promotes virulence by. The corn smut ustilago maydis establishes a biotrophic interaction with its host plant maize. Ustilago maydis is an obligate fungal pathogen of maize that causes disease known as the common smut of corn. Pep1 inhibits maize oxidative burst triggered by heat inactivated ustilago maydis cells. A secreted effector protein of ustilago maydis guides maize leaf cells to form tumors amey redkar,a,1 rafal hoser,b lena schilling,a bernd zechmann,c magdalena krzymowska,b virginia walbot,d and gunther doehlemanna,e,2 a max planck institute for terrestrial microbiology, department of organismic interactions, d35043 marburg, germany. The biotrophic development of ustilago maydis studied by rna. A secreted effector protein of ustilago maydis guides maize.
Previously, pep1 was found to be an inhibitor of apoplastic plant peroxidases, which suppresses the oxidative burst, a primary immune response of the host plant and enables fungal colonization. The ustilago maydis effector pep1 suppresses plant immunity by inhibition of host peroxidase activity, plos pathogens, 2012, 5, doi. Compatibility in biotrophic plantfungal interactions. The ustilago maydis effector pep1 suppresses plant immunity. Virulence of the maize smut ustilago maydis is shaped by organspeci. It infects all aerial parts of maize resulting in large tumors that contain melanized, black spores. Pathogenicity determinants in smut fungi revealed by genome.
During the establishment of an infection in its maize host, the basidiomycete fungus ustilago maydis. Characterization of the largest effector gene cluster of. Pathogenicity determinants in smut fungi revealed by. Pdf pep1, a secreted effector protein of ustilago maydis. The basidiomycete ustilago maydis causes smut disease in maize. Maize tumors caused by ustilago maydis require organ.
These data indicate that cce1 is a core effector with apoplastic localization that is essential for u. Because a pep1 ortholog of the barleycovered smut fungus u. The fungal core effector pep1 is conserved across smuts of. The pep1 protein comprises 178 aa and is expected to be cleaved behind a putative nterminal secretion signal figure. Formation of these prominent symptoms is associated with comprehensive reprogramming of the hosts physiology, cell morphology and organ development. Pseudozyma saprotrophic yeasts have retained a large.
Lipid and acetate metabolism influence host colonization. Pdf identification and characterization of secreted and. Based on these results, we conclude that pep1 has a conserved function essential for establishing compatibility that is not restricted to the u. Virulence function of the ustilago maydis sterol carrier. The basidiomycete ustilago maydis causes smut disease in maize, with large plant tumors being formed as the most prominent disease symptoms. Insertion pool sequencing for insertional mutant analysis in complex hostmicrobe interactions simon uhse,1,5 florian g. Dec 10, 2010 biotrophic pathogens, such as the related maize pathogenic fungi ustilago maydis and sporisorium reilianum, establish an intimate relationship with their hosts by secreting protein effectors. Transcriptome analysis of smut fungi reveals widespread. Although many gene expression profiling studies of maize leaves infected with ustilago maydis have been published, heterogeneity of the results, caused by various data processing methods and pathogenic strains in different data sets, remains strong. Summary the secreted fungal effector pep1 is essential for penetration of the host epidermis and establishment of biotrophy in the ustilago maydismaize pathosystem. The basidiomycete ustilago maydis is the causal agent of corn smut disease and induces tumor formation during biotrophic growth in its host maize zea mays. In our analysis, we focused on fungal metabolism, nutritional strategies, secreted effectors, and regulatory networks. However, it is also known to be a delicacy in central america for hundreds of years and has even found its place in the food industry fig. Ustilago maydis is a pathogenic fungus that causes smut disease in maize.
We hypothesized that transformation of different primordia into plant tumors would require organspecific gene expression by both. The core effector cce1 is required for early infection of. Lipid and acetate metabolism influence host colonization by. Jan 27, 2015 the secreted fungal effector pep1 is essential for penetration of the host epidermis and establishment of biotrophy in the ustilago maydismaize pathosystem. Colonization of the plant presents numerous challenges for u. Infection of maize by corn smut ustilago maydis provides an agronomically important model of biotrophic hostpathogen interactions. Virulence of the maize smut u stilago maydis is shaped by. Ustilago maydis as a pathogen thomas brefort, gunther doehlemann, artemio mendozamendoza, stefanie reissmann, armin djamei, and regine kahmann max planck institute for terrestrial microbiology, department of organismic interactions, d35043 marburg, germany. Using ustilago maydis as a trojan horse for in situ delivery. Here, we performed an in depth transcriptional profiling of the entire plantassociated development of u. The biotrophic pathogen ustilago maydis is the causative agent of the corn smut disease 1. Haploids with compatible mating loci fuse to form a dikaryotic cell type that is filamentous and pathogenic.
Patterns of variation at ustilago maydis virulence. The maize smut fungus ustilago maydis is a model organism for elucidating host colonization strategies of biotrophic fungi. The biotrophic development of ustilago maydis studied by. Arabidopsis infection by haploid or diploid strains of ustilago. The smut fungus ustilago maydis parasitizes maize and establishes a. Previously we identified pep1 protein essential during penetration1 as a secreted effector with an essential role for u. The ustilago maydiseffector pep1 suppresses plant immunity by. We have conducted a combined metabolome and transcriptome survey of infected leaves between 1 d post infection dpi and 8 dpi, representing infected leaf primordia and fully developed tumors, respectively. Ustilago maydis is the causal agent of the disease known as corn smut or huitlacohe.
The invading hyphae are surrounded by the plant plasma membrane and proliferate within the plant tissue. The pep1 protein comprises 178 aa and is expected to be cleaved. Pep1, a secreted effector protein of ustilago maydis, is. A secreted effector protein of ustilago maydis guides. Ustilago maydis, the causal agent of corn smut disease, is a. Hallmarks of this infection are the formation of large plant tumors and the production of a red pigment, called anthocyanin, in infected plant tissues. Maize tumors caused by ustilago maydis require organspecific.
Because secreted effectors interacting with plant proteins should rapidly evolve, we identified variable genomic regions by sequencing the genome of s. May 10, 2012 given the finding that pep1 resides in the plant apoplast, one could hypothesize that during u. Cmu1 is taken up into the cytosol of host cells and competes with the endogenous sa biosynthesis pathway. The smut fungus ustilago maydis establishes a biotrophic interaction with its. Summary the secreted fungal effector pep1 is essential for penetration of the. Pep1, a secreted effector protein of ustilago maydis. Mb annotated genome sequence has been an excellent resource for investigating biotrophic plant pathogenesis. Huitlacoche is a typical mexican food with interesting nutritional properties and distinctive flavor. Comparison of cell morphology of ustilago maydis ust1 deletion mutant and. Apr, 20 the basidiomycete ustilago maydis causes smut disease on maize, which is characterized by plant tumors that develop on all aerial parts of the host plant. Our research aims to understand this modulation of the plant immune system both by. In a previous study, we identified the secreted effector protein pit2, which is essential for maintenance of biotrophy.
Kahmann, unpublished we identified an ortholog of pep1 that shows 61% identity to u. Hence, we conducted a combined analysis of six genomewide expression data sets of maize leaves infected with five different u. In mexico there is an evidence of its use as human food since prehispanic times. The ustilago maydis effector pep1 suppresses plant immunity by inhibition of host peroxidase.
This interaction requires efficient suppression of plant immune responses, which is attributed to secreted effector proteins. Abstractthe maintenance of an intimate interaction between plantbiotrophic fungi and their hosts over evolutionary. Pdf ustilago maydis, a delicacy of the aztec cuisine and a model. The fungal core effector pep1 is conserved across smuts of dicots. Pdf compatibility in the ustilago maydismaize interaction. Pep1, a secreted effector protein of ustilago maydis, is required for successful invasion of plant cells. Characterization of the largest effector gene cluster of ustilago maydis thomas brefort. Ustilago maydis, a delicacy of the aztec cuisine and a model. Ustilago maydis is a basidiomycota fungus that naturally infects only. The pep1 gene was found to be specifically expressed during pathogenic development of u. After penetration of the maize epidermis, fungal colonization of host tissue induces tumor formation on all aerial maize organs. The biotrophic pathogen ustilago maydis, the causative agent of corn smut disease, infects one of the most important crops worldwide zea mays. Such fungi form specialized infection structures which allow direct penetration of the plant cuticle.
Therefore, suppression of the host immune system is essential for successful infection. It can infect all aboveground tissues of maize plants and induces local tumor formation within two weeks after infection under glasshouse conditions kamper et al. The ustilago maydis effector pep1 suppresses plant. The smut fungus ustilago maydis establishes a biotrophic interaction with its host plant maize in which the infected host cells stay alive. Similar to other phytopathogenic smut fungi, the pathogenic. Oct 17, 2017 the common smut of corn, caused by ustilago maydis is a troublesome disease of maize. Cells were washed in water and recalibrated to an od600 of 1. Insertion pool sequencing for insertional mutant analysis. The ustilago maydis effector pep1 suppresses plant immunity by. The ustilago maydiseffector pep1 suppresses plant immunity. Combined analysis of genomewide expression profiling of. Previously, pep1 was found to be an inhibitor of apoplastic plant peroxidases, which suppresses the oxidative burst. The model for functional investigation of these fungi is ustilago maydis. Using ustilago maydis as a trojan horse for in situ.
The resulting strain was fully pathogenic towards maize figure 8f, which illustrates that the two proteins are exchangeable. An ear of maize infected with ustilago maydis showing a number of sori filled with. Ustilago maydis is a plant pathogenic fungus that causes tumors on all aerial parts of its host plant maize zea mays. The barley covered smut fungus ustilago hordei contains an ortholog of pep1 which is needed for penetration of barley and which is able to complement the u.
The smut fungus ustilago maydis establishes a biotrophic interaction with its host plant maize in which the infected host cells. We identified a novel secreted protein, termed pep1, that is essential for penetration. Ustilago maydis, a delicacy of the aztec cuisine and a. Author summary for many fungi that infect plants, successful invasion is coupled to a series of differentiation steps that are necessary to breach the plant cuticle. Fungal development of the plant pathogen ustilago maydis. Mining the effector repertoire of the biotrophic fungal. Jun, 2018 the fungal pathogen ustilago maydis is the causative agent of corn smut, a disease characterized by the formation of tumors on all aerial parts of its host plant zea mays. Cell biology of corn smut disease ustilago maydis as a.
1455 1007 14 1052 729 945 1492 979 1080 191 1222 1412 816 872 963 270 767 344 1388 360 1326 1461 922 1289 791 162 352 977 52 319 1242 40