Plants can recruit beneficial microbes to enhance their ability to defend against pathogens. However, in contrast to the intensively studied roles of the rhizosphere microbiome in suppressing plant pathogens, the collective community-level change and effect of the phyllosphere microbiome in response to pathogen invasion remains largely elusive.Here, we integrated 16S metabarcoding, shotgun metagenomics and culture-dependent methods to systematically investigate the changes in phyllosphere microbiome between infected and uninfected citrus leaves by Diaporthe citri, a fungal pathogen causing melanose disease worldwide. Multiple microbiome features suggested a shift in phyllosphere microbiome upon D. citri infection, highlighted by the marked reduction of community evenness, the emergence of large numbers of new microbes, and the intense microbial network. We also identified the microbiome features from functional perspectives in infected leaves, such as enriched microbial functions for iron competition and potential antifungal traits, and enriched microbes with beneficial genomic characteristics. Glasshouse experiments demonstrated that several bacteria associated with the microbiome shift could positively affect plant performance under D. citri challenge, with reductions in disease index ranging from 65.7 to 88.4%. Among them, Pantoea asv90 and Methylobacterium asv41 identified as "recruited new microbes" in the infected leaves, exhibited antagonistic activities to D. citri both in vitro and in vivo, including inhibition of spore germination and/or mycelium growth. Sphingomonas spp. presented beneficial genomic characteristics and were found to be the main contributor for the functional enrichment of iron complex outer membrane receptor protein in the infected leaves. Moreover, Sphingomonas asv20 showed a stronger suppression ability against D. citri in iron-deficient conditions than iron-sufficient conditions, suggesting a role of iron competition during their antagonistic action.Overall, our study revealed how phyllosphere microbiomes differed between infected and uninfected citrus leaves by melanose pathogen, and identified potential mechanisms for how the observed microbiome shift might have helped plants cope with pathogen pressure. Our findings provide novel insights into understanding the roles of phyllosphere microbiome responses during pathogen challenge. Video abstract. 

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The phyllosphere microbiome shifts toward combating melanose pathogen

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Nitrogen (N) is the most critical nutrient that affects the establishment and stability of mangrove ecosystems. Despite the importance of biological nitrogen fixation (BNF) mediated by diazotrophs in mangrove ecosystems, current studies largely overlook the influence of arbuscular mycorrhizal fungi (AMF) on diazotrophs-driven BNF process in the N-limited ecosystems. Here, we conducted a comprehensive study on root-associated AMF and their interspecific interactions with diazotrophs in mangrove ecosystems using high throughput sequencing methods. Our results showed that the richness/diversity of diazotrophs had significant positive correlations with AMF community in mangrove rhizosphere. BNF rate in the rhizosphere of all mangrove species increased with the increasing of positive co-occurrence between AMF and diazotrophs, suggesting that the positive cooperation may promote N fixation efficiency in mangrove ecosystems. We also identified the potential keystone taxa (Zi ≥ 2.5 or Pi ≥ 0.62) and determined their crucial implications for the ecological processes of N fixation in mangrove ecosystems. The random forest analysis further indicated that the AMF keystone taxa were the most important predictors of BNF in mangrove rhizosphere. In addition, path analysis indicated that the α-diversity of AMF and diazotrophs communities, N-related enzymes and sediment nutrition components (e.g., TC, TN, Fe) were the main factors driving BNF process in mangrove ecosystems. This study provides novel insights into the interactions between AMF and diazotrophic communities during BNF process and expands our knowledge of AMF ecological functions of N cycle in mangrove ecosystems.

Co-symbiosis of arbuscular mycorrhizal fungi (AMF) and diazotrophs promote biological nitrogen fixation in mangrove ecosystems

Toward understanding the genetic bases underlying plant‐mediated “cry for help” to the microbiota

Plant diversity enhances soil fungal network stability indirectly through the increase of soil carbon and fungal keystone taxa richness.

The plant microbiome is an integral part of the host and increasingly recognized as playing fundamental roles in plant growth and health. Increasing evidence indicates that plant rhizosphere recruits beneficial microbes to the plant to suppress soil-borne pathogens. However, the ecological processes that govern plant microbiome assembly and functions in the below- and aboveground compartments under pathogen invasion are not fully understood. Here, we studied the bacterial and fungal communities associated with 12 compartments (e.g., soils, roots, stems, and fruits) of chili pepper (Capsicum annuum L.) using amplicons (16S and ITS) and metagenomics approaches at the main pepper production sites in China and investigated how Fusarium wilt disease (FWD) affects the assembly, co-occurrence patterns, and ecological functions of plant-associated microbiomes. The amplicon data analyses revealed that FWD affected less on the microbiome of pepper reproductive organs (fruit) than vegetative organs (root and stem), with the strongest impact on the upper stem epidermis. Fungal intra-kingdom networks were less stable and their communities were more sensitive to FWD than the bacterial communities. The analysis of microbial interkingdom network further indicated that FWD destabilized the network and induced the ecological importance of fungal taxa. Although the diseased plants were more susceptible to colonization by other pathogenic fungi, their below- and aboveground compartments can also recruit potential beneficial bacteria. Some of the beneficial bacterial taxa enriched in the diseased plants were also identified as core taxa for plant microbiomes and hub taxa in networks. On the other hand, metagenomic analysis revealed significant enrichment of several functional genes involved in detoxification, biofilm formation, and plant-microbiome signaling pathways (i.e., chemotaxis) in the diseased plants. Together, we demonstrate that a diseased plant could recruit beneficial bacteria and mitigate the changes in reproductive organ microbiome to facilitate host or its offspring survival. The host plants may attract the beneficial microbes through the modulation of plant-microbiome signaling pathways. These findings significantly advance our understanding on plant-microbiome interactions and could provide fundamental and important data for harnessing the plant microbiome in sustainable agriculture.

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Meng-Meng Wang

Papers

Disease-induced changes in plant microbiome assembly and functional adaptation.