Endophytic fungi reshape the core microbiota of the root system to promote peanut growth and disease resistance

Endophytic fungi reshape the core microbiota of the root system to promote peanut growth and disease resistance

Plant-associated microbial communities are often regarded as extensions of the plant body's own genes and functions that are critical for its growth, development and immune resistance to disease. In addition to the widely explored inter-root microbiome, the endophytic microbiome of the plant root system, which has the advantage of co-evolving with the plant host under native environmental conditions, has been given higher expectations in regulating plant growth and disease resistance. Plant endophytes directly or indirectly affect plant growth and development, and their functional values range from enhancing disease resistance to promoting plant growth through nitrogen fixation or hormone and enzyme synthesis. Among them, the influence of endophytic fungi on plant metabolism and their extensive mycelial network coverage in plants endow endophytic fungi with the potential to act as mediators between the host and the endosymbiotic microbiome, whereas endophytic bacteria in the endosymbiotic microbiome provide a diverse range of ecological service functions to the host due to their great diversity. However, imbalance and functional disruption of these microbial communities can lead to impaired plant growth and development, resulting in disease outbreaks and yield loss. The application of plant probiotics is recognized as a sustainable agricultural cultivation strategy, and the positive effects of probiotics on host plants go far beyond the function of a single microorganism. There is growing evidence that the remodeling of the microbiota under different environmental conditions is crucial for the beneficial ecological services of plant probiotics.

The endophytic fungus Phomopsis liquidambaris was able to significantly alleviate production barriers caused by continuous cropping on peanut and increase peanut yield. Effective colonization of this endophyte can promote plant growth, lateral root and root hair growth, nitrogen uptake and metabolism, as well as increase plant resistance to biotic and abiotic stresses, among other beneficial effects. However, little is known about the microbial composition of the root endophyte core and the effects of its variation on plant health. The researchers hypothesized that colonization of P. liquidambaris could reshape the core root endophytic microbial community in favor of plant adaptation, empowering plants to thrive in continuous soils.

The researchers evaluated the effects of inoculation of endophytic maple mimic stem nodule molds on peanut plant growth in continuous soils and found that the height and biomass of continuous plants were significantly lower than that of non-continuous plants. However, for the treatment group inoculated with P. liquidambaris peanut plants showed better growth advantage in height and biomass at all reproductive stages, which were significantly higher than the control treatment group, and the final crop yield was also significantly higher. These results demonstrated that P. liquidambaris promotes peanut growth and protects peanut from diseases under continuous cropping conditions. Meanwhile, the occurrence of root rot and leaf spot diseases of peanut under no treatment was explored. Compared with the non-continuous planting treatment group, the severity of leaf spot disease at pod set and root rot at seedling stage was significantly increased in peanut grown under continuous planting, and the disease severity increased by 47.62% and 113.37%, respectively. However, the severity of both leaf spot and root rot diseases of peanut in continuous soil inoculated with P. liquidambaris significantly decreased by 27.41% and 62.5%, respectively, compared with continuous soil. In addition, the relative content of pathogenic fungi in the soil of Fusarium acuminatum and Colletotrichum anthracnose was significantly reduced after inoculation with P. liquidambaris, with the relative content reduced by 48.2% and 70.16%, respectively.

Fig. 1 Promoting effect of P. liquidambaris on growth and disease resistance of peanut plants

Further, the researchers examined the effect of P. liquidambaris inoculation on peanut endophytic bacterial community, and found that the composition of peanut endophytic bacterial community differed significantly among treatments, suggesting that the colonization of P. liquidambaris triggered the changes of endophytic bacterial community at different growth stages of the plant, and induced the potential beneficial bacteria such as slow-growing rhizobacteria and streptomycetes to Enrichment. NetShift analysis indicated that Burkholderia spp., Rhizobium spp. slow-growing, Pseudomonas spp. and Streptomyces spp. may be the key taxa in the endophytic core microbiota of peanut root system. To evaluate the effect of P. liquidambaris-associated endophytic bacteria on the health of peanut plants, 30 strains of Burkholderia spp, Rhizobium spp. slow-growing, Pseudomonas spp., Bacillus spp. and Bacillus spp. related to the core flora were selected. Among them, 15 strains were able to fix nitrogen, 15 strains were able to solubilize inorganic phosphorus, 10 strains were able to produce chitinase, 11 strains were able to produce xylanase and 6 strains were able to produce cellulase.

Ten of these strains with potential growth-promoting or bacteriostatic activities were selected to construct a synthetic colony. The fresh weight of peanut roots treated with the synthetic colony was 37.08% higher than that of the uninoculated treatment; the fresh weight of the plants increased by 34.06%. In addition, inoculation of synthetic colonies reduced the occurrence of peanut root rot and the content of Fusarium acnes in the soil, and was able to promote peanut root development. The endophytic fungus P. liquidambaris alone and the synthetic flora reduced the severity of peanut root rot by 51.26% and 57.46%, respectively. At peanut maturity, application of synthetic mycorrhizal flora significantly increased aboveground, root biomass and peanut yield by 35.56%, 81.19% and 34.31%, respectively.

This study provides a new perspective to reveal the multiple beneficial effects of probiotics, i.e., endophytic fungi as inducers used to improve the core endophytic microbiome of the root system thereby promoting plant growth and disease resistance.

Fig. 2 Disease resistance and growth promoting effects of synthetic flora