The endodermis—development and differentiation of the plant's inner skin

Controlling external compound entrance is essential for plant survival. To set up an efficient and selective sorting of nutrients, free diffusion via the apoplast in vascular plants is blocked at the level of the endodermis. Although we have learned a lot about endodermal specification in the last years, information regarding its differentiation is still very limited. A differentiated endodermal cell can be defined by the presence of the "Casparian strip” (CS), a cell wall modification described first by Robert Caspary in 1865. While the anatomical description of CS in many vascular plants has been very detailed, we still lack molecular information about the establishment of the Casparian strips and their actual function in roots. The recent isolation of a novel protein family, the CASPs, that localizes precisely to a domain of the plasma membrane underneath the CS represents an excellent point of entry to explore CS function and formation. In addition, it has been shown that the endodermis contains transporters that are localized to either the central (stele-facing) or peripheral (soil-facing) plasma membranes. These features suggest that the endodermis functions as a polar plant epitheliu

A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects

We thank the Genomic Technologies Facility (GTF) and the Central Imaging Facility (CIF) of the University of Lausanne for expert technical support. We thank Valérie Dénervaud Tendon, Guillaume Germion, Deborah Mühlemann, and Kayo Konishi for technical assistance and John Danku and Véronique Vacchina for ICP-MS analysis. This work was funded by grants from the Swiss National Science Foundation (SNSF), the European Research Council (ERC) to NG and a Human Frontiers Science Program (HFSP) grant to JT and NG. GL and CM were supported by the Agropolis foundation (Rhizopolis) and the Agence Nationale de la Recherche (HydroRoot; ANR-11-BSV6-018). MB was supported by a EMBO long-term postdoctoral fellowship, JEMV by a Marie Curie IEF fellowship and TK by the Japan Society for the Promotion of Sciences (JSPS).Peer reviewedPublisher PD

Mixed infections alter transmission potential in a fungal plant pathogen

Infections by more than one strain of a pathogen predominate under natural conditions. Mixed infections can have significant, though often unpredictable, consequences for overall virulence, pathogen transmission and evolution. However, effects of mixed infection on disease development in plants often remain unclear and the critical factors that determine the outcome of mixed infections remain unknown. The fungus Zymoseptoria tritici forms genetically diverse infections in wheat fields. Here, for a range of pathogen traits, we experimentally decompose the infection process to determine how the outcomes and consequences of mixed infections are mechanistically realized. Different strains of Z. tritici grow in close proximity and compete in the wheat apoplast, resulting in reductions in growth of individual strains and in pathogen reproduction. We observed different outcomes of competition at different stages of the infection. Overall, more virulent strains had higher competitive ability during host colonization, and less virulent strains had higher transmission potential. We showed that within‐host competition can have a major effect on infection dynamics and pathogen population structure in a pathogen and host genotype‐specific manner. Consequently, mixed infections likely have a major effect on the development of septoria tritici blotch epidemics and the evolution of virulence in Z. tritici

A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen

Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen

Asexual reproductive potential trumps virulence as a predictor of competitive ability in mixed infections

13 Pàg.Natural infections frequently involve several co-infecting pathogen strains. These mixed infections can affect the extent of the infection, the transmission success of the pathogen and the eventual epidemic outcome. To date, few studies have investigated how mixed infections affect transmission between hosts. Zymoseptoria tritici is a highly diverse wheat pathogen in which multiple strains often coexist in the same lesion. Here we demonstrate that the most competitive strains often exclude their competitors during serial passages of mixed infections. The outcome of the competition depended on both the host genotype and the genotypes of the competing pathogen strains. Differences in virulence among the strains were not associated with competitive advantages during transmission, while differences in reproductive potential had a strong effect on strain competitive ability. Overall, our findings suggest that host specialization is determined mainly by the ability to successfully transmit offspring to new hosts during mixed infections.This project was supported by the ETH research grant ETH-23 15-2 to A.S.-V. and B.A.M. and by Ministerio de Ciencia e Innovación research grant RYC2018-025530-I to A.S.-V.Peer reviewe

Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections.

Plants interact with a plethora of pathogenic microorganisms in nature. Pathogen-plant interaction experiments focus mainly on single-strain infections, typically ignoring the complexity of multi-strain infections even though mixed infections are common and critical for the infection outcome. The wheat pathogen Zymoseptoria tritici forms highly diverse fungal populations in which several pathogen strains often colonize the same leaf. Despite the importance of mixed infections, the mechanisms governing interactions between a mixture of pathogen strains within a plant host remain largely unexplored. Here we demonstrate that avirulent pathogen strains benefit from being in mixed infections with virulent strains. We show that virulent strains suppress the wheat immune response, allowing avirulent strains to colonize the apoplast and to reproduce. Our experiments indicate that virulent strains in mixed infections can suppress the plant immune system, probably facilitating the persistence of avirulent pathogen strains in fields planted with resistant host plants

Chromatin Dynamics Contribute to the Spatiotemporal Expression Pattern of Virulence Genes in a Fungal Plant Pathogen

18 Pág.Dynamic changes in transcription profiles are key for the success of pathogens in colonizing their hosts. In many pathogens, genes associated with virulence, such as effector genes, are located in regions of the genome that are rich in transposable elements and heterochromatin. The contribution of chromatin modifications to gene expression in pathogens remains largely unknown. Using a combination of a reporter gene-based approach and chromatin immunoprecipitation, we show that the heterochromatic environment of effector genes in the fungal plant pathogen Zymoseptoria tritici is a key regulator of their specific spatiotemporal expression patterns. Enrichment in trimethylated lysine 27 of histone H3 dictates the repression of effector genes in the absence of the host. Chromatin decondensation during host colonization, featuring a reduction in this repressive modification, indicates a major role for epigenetics in effector gene induction. Our results illustrate that chromatin modifications triggered during host colonization determine the specific expression profile of effector genes at the cellular level and, hence, provide new insights into the regulation of virulence in fungal plant pathogens.IMPORTANCE Fungal plant pathogens possess a large repertoire of genes encoding putative effectors, which are crucial for infection. Many of these genes are expressed at low levels in the absence of the host but are strongly induced at specific stages of the infection. The mechanisms underlying this transcriptional reprogramming remain largely unknown. We investigated the role of the genomic environment and associated chromatin modifications of effector genes in controlling their expression pattern in the fungal wheat pathogen Zymoseptoria tritici Depending on their genomic location, effector genes are epigenetically repressed in the absence of the host and during the initial stages of infection. Derepression of effector genes occurs mainly during and after penetration of plant leaves and is associated with changes in histone modifications. Our work demonstrates the role of chromatin in shaping the expression of virulence components and, thereby, the interaction between fungal pathogens and their plant hosts.This research was supported by the Swiss National Science Foundation (grant 31003A_155955 to B.A.M.). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.Peer reviewe

Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections

Plants interact with a plethora of pathogenic microorganisms in nature. Pathogen-plant interaction experiments focus mainly on single-strain infections, typically ignoring the complexity of multi-strain infections even though mixed infections are common and critical for the infection outcome. The wheat pathogen Zymoseptoria tritici forms highly diverse fungal populations in which several pathogen strains often colonize the same leaf. Despite the importance of mixed infections, the mechanisms governing interactions between a mixture of pathogen strains within a plant host remain largely unexplored. Here we demonstrate that avirulent pathogen strains benefit from being in mixed infections with virulent strains. We show that virulent strains suppress the wheat immune response, allowing avirulent strains to colonize the apoplast and to reproduce. Our experiments indicate that virulent strains in mixed infections can suppress the plant immune system, probably facilitating the persistence of avirulent pathogen strains in fields planted with resistant host plants.ISSN:1553-7374ISSN:1553-736

Chromatin Dynamics Contribute to the Spatiotemporal Expression Pattern of Virulence Genes in a Fungal Plant Pathogen

Dynamic changes in transcription profiles are key for the success of pathogens in colonizing their hosts. In many pathogens, genes associated with virulence, such as effector genes, are located in regions of the genome that are rich in transposable elements and heterochromatin. The contribution of chromatin modifications to gene expression in pathogens remains largely unknown. Using a combination of a reporter gene-based approach and chromatin immunoprecipitation, we show that the heterochromatic environment of effector genes in the fungal plant pathogen Zymoseptoria tritici is a key regulator of their specific spatiotemporal expression patterns. Enrichment in trimethylated lysine 27 of histone H3 dictates the repression of effector genes in the absence of the host. Chromatin decondensation during host colonization, featuring a reduction in this repressive modification, indicates a major role for epigenetics in effector gene induction. Our results illustrate that chromatin modifications triggered during host colonization determine the specific expression profile of effector genes at the cellular level and, hence, provide new insights into the regulation of virulence in fungal plant pathogens.ISSN:2150-7511ISSN:2161-212

Tuning self-renewal in the Arabidopsis stomatal lineage by hormone and nutrient regulation of asymmetric cell division

Asymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate most cells on the leaf surface. Systemic and environmental signals modify tissue development, but the mechanisms by which plants incorporate such cues to regulate asymmetric divisions are elusive. In a screen for modulators of cell polarity, we identified CONSTITUTIVE TRIPLE RESPONSE1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem cells. Quantitative analysis of cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. These results provide a framework for a mechanistic understanding of how nutritional status and environmental factors tune stem-cell behavior in the stomatal lineage, ultimately enabling flexibility in leaf size and cell-type composition.ISSN:2050-084