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Mahdi, L. K.

Publications and source records attributed to Mahdi, L. K..

4 recordsLinked to original sources

Low intra-microbiota antagonism underlies stable and protective barley root microbiota

Plants rely on root-associated microbiota for growth and pathogen protection, yet the community properties underlying stable beneficial functions remain unclear. Here, we show that low intra-microbiota antagonism is associated with stability and pathogen protection in the barley root microbiota. Using a comprehensive culture collection of barley root endophytes, we reconstructed bacterial synthetic communities (SynComs) and compared a core SynCom resembling the natural microbiota with a trait-prioritized SynCom assembled from strains selected for predicted host benefits. Although strains from both communities exhibited broad pathogen-inhibitory potential, the communities behaved differently in planta. The core SynCom showed low internal antagonism, remained stable, and protected barley roots against fungal pathogens without impairing growth. In contrast, the trait-prioritized SynCom exhibited strong internal antagonism, unstable assembly, loss of protection, and reduced root growth. Together, our findings indicate that microbiota function cannot be predicted from individual strain traits alone. Rather, low intra-microbiota antagonism promotes community stability and enables protective functions to emerge in barley roots. Significance statementPlants rely on root microbiota for disease protection, yet the principles governing community stability and protective function remain poorly understood. Here, we show that low intra-microbiota antagonism is associated with a stable and protective barley root microbiota, whereas strong internal antagonism destabilizes communities, impairs root growth, and abolishes pathogen protection. These findings show that microbiota function depends not only on beneficial traits of individual strains, but also on compatibility among community members. HighlightsO_LILow intra-microbiota antagonism is associated with stable and protective barley root microbiota. C_LIO_LITrait-prioritized SynCom assembly with higher intra-microbiota antagonism can lead to dysbiosis. C_LIO_LIA highly antagonistic Pseudomonas strain is buffered by the core SynCom but detrimental in an unstable community. C_LIO_LICommunity compatibility better explains protection than individual strain traits. C_LIO_LIStable bacterial communities support fungal endophyte-mediated protection and maintain pathogen protection across barley genotypes. C_LI

plant biology↗

Time-resolved transcriptomics reveal a mechanism of host niche defense: beneficial root endophytes deploy a host-protective antimicrobial GH18-CBM5 chitinase

Associations between plants and beneficial root-endophytic fungi enhance plant performance by improving nutrient uptake, abiotic stress tolerance and disease resistance. To successfully colonize different host plants and defend their host niche against competing microbes, but also to cooperate with beneficial bacterial members of the microbiota, root endophytes such as Sebacinales secrete a multitude of tightly regulated effector-proteins and carbohydrate-active enzymes. However, the functions, specificity, and regulation of these proteins remain poorly understood. In this study, we employ time-resolved transcriptomics to analyse the gene expression profiles of two Sebacinales members interacting with organisms from different kingdoms of life. We identified crucial genes for plant colonization and intermicrobial competition, including a fungal GH18-CBM5 chitinase specifically upregulated in response to the phytopathogenic fungus Bipolaris sorokiniana. This chitinase protects the plant hosts against the pathogen, reducing fungal biomass and disease symptoms in barley and Arabidopsis thaliana. Our findings shed light on interaction partner specific gene expression in Sebacinales endophytes, with potential applications in enhancing plant health and resilience. Bullet pointsO_LIBoth Serendipita indica (Si) and Serendipita vermifera (Sv) show similar transcriptional responses to three host species and the phytopathogen Bipolaris sorokiniana (Bs), indicating common interaction principles between Sebacinales and plant hosts or fungi. C_LIO_LIThese shared mechanisms involve the activation of effector genes like small secreted proteins and carbohydrate-active enzymes. C_LIO_LICooperation with beneficial bacteria elicits only minimal transcriptomic alterations in Sebacinales compared to plants and Bs. C_LIO_LISebacinales respond to Bs by upregulating a specific GH18-CBM5 chitinase unique to Basidiomycota within the fungal kingdom, inhibiting Bs growth and reducing disease symptoms in Arabidopsis thaliana and barley. C_LI

microbiology↗

A GH81-type β-glucan-binding protein facilitates colonization by mutualistic fungi in barley

Cell walls are important interfaces of plant-fungal interactions. Host cell walls act as robust physical and chemical barriers against fungal invaders, making them an essential line of defense. Upon fungal colonization, plants deposit phenolics and callose at the sites of fungal penetration to reinforce their walls and prevent further fungal progression. Alterations in the composition of plant cell walls significantly impact host susceptibility. Furthermore, plants and fungi secrete glycan hydrolases acting on each others cell walls. These enzymes release a wide range of sugar oligomers into the apoplast, some of which trigger the activation of host immunity via host surface receptors. Recent characterization of cell walls from plant-colonizing fungi have emphasized the abundance of {beta}-glucans in different cell wall layers, which makes them suitable targets for recognition. To characterize host components involved in immunity against fungi, we performed a protein pull-down with the biotinylated {beta}-glucan laminarin. Thereby, we identified a glycoside hydrolase family 81-type glucan-binding protein (GBP) as the major {beta}-glucan interactor. Mutation of GBP1 and its only paralogue GBP2 in barley led to decreased colonization by the beneficial root endophytes Serendipita indica and S. vermifera, as well as the arbuscular mycorrhizal fungus Rhizophagus irregularis. The reduction of symbiotic colonization was accompanied by enhanced responses at the host cell wall. Moreover, GBP mutation in barley also increased resistance to fungal infections in roots and leaves by the hemibiotrophic pathogen Bipolaris sorokiniana and the obligate biotrophic pathogen Blumeria graminis f. sp. hordei, respectively. These results indicate that GBP1 is involved in the establishment of symbiotic associations with beneficial fungi, a role that has potentially been appropriated by barley-adapted pathogens. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=134 SRC="FIGDIR/small/536646v1_figu1.gif" ALT="Figure 1"> View larger version (39K): org.highwire.dtl.DTLVardef@c47957org.highwire.dtl.DTLVardef@fa6727org.highwire.dtl.DTLVardef@18a54d2org.highwire.dtl.DTLVardef@c6b103_HPS_FORMAT_FIGEXP M_FIG C_FIG In BriefGBP1, a family 81 glycoside hydrolase, is an important {beta}-glucan interactor in barley. Mutation of GBP1 and its sole paralogue GBP2 leads to reduced colonization by beneficial root endophytes, AM fungi and pathogens, accompanied by enhanced responses at the plant cell wall. This indicates that GBP1 and {beta}-glucans are compatibility factors involved in the establishment of symbiotic associations with beneficial fungi, a role possibly hijacked by pathogens.

plant biology↗

The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally show early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. HighlightsO_LIThe root endophytic fungus Serendipita vermifera can functionally replace core bacterial microbiota members in mitigating pathogen infection and disease symptoms. C_LIO_LIS. vermifera additionally stabilizes and potentiates the protective activities of root-associated bacteria and mitigates the negative effects of a non-native bacterial community in A. thaliana. C_LIO_LIInter-kingdom synergistic beneficial effects do not require extensive host transcriptional reprogramming nor high levels of S. vermifera colonisation. C_LIO_LIInter-kingdom protective benefits are largely independent of the host while synergism leading to early inter-kingdom growth promotion is driven by host species and microbiota composition. C_LI

plant biology↗