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 considered extensions of the plant body's own genes and functions that are crucial for its growth, development, and immune resistance to disease. In addition to the well-studied inter-root microbiome, the endophytic microbiome of the plant root system, which has the advantage of co-evolving with the plant host in native environmental conditions, is highly anticipated for its role in regulating plant growth and disease resistance. Plant endophytes can directly or indirectly impact plant growth and development, with functional benefits ranging from enhancing disease resistance to promoting plant growth through nitrogen fixation or hormone and enzyme synthesis. Endophytic fungi influence plant metabolism and, with their extensive mycelial network coverage in plants, have the potential to mediate between the host and the endosymbiotic microbiome. Endophytic bacteria in the endosymbiotic microbiome offer a wide range of ecological services to the host due to their diversity. However, an imbalance or disruption in the function of these microbial communities can lead to impaired plant growth and development, resulting in disease outbreaks and yield loss. The use of plant probiotics is seen as a sustainable agricultural cultivation strategy, with their positive effects on host plants extending beyond the function of a single microorganism. Increasing evidence suggests that the restructuring of the microbiota under different environmental conditions is essential 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.

Continuous planting of peanut plants without inoculation of endophytic maple mimic stem nodule molds resulted in lower height and biomass compared to non-continuous plants. However, peanut plants inoculated with P. liquidambaris showed better growth in height and biomass at all reproductive stages, with significantly higher yields. P. liquidambaris promoted peanut growth and protected against diseases under continuous cropping conditions. Inoculation with P. liquidambaris significantly decreased the severity of leaf spot and root rot diseases in continuous soil, reducing the relative content of pathogenic fungi.

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

The researchers found that the composition of peanut endophytic bacterial community varied significantly among treatments due to the colonization of P. liquidambaris, leading to changes in the endophytic bacterial community during different growth stages of the plant. This colonization induced the enrichment of potential beneficial bacteria such as slow-growing rhizobacteria and streptomycetes. Key taxa in the endophytic core microbiota of the peanut root system were identified as Burkholderia spp., Rhizobium spp., slow-growing, Pseudomonas spp., and Streptomyces spp. Evaluation of the effect of P. liquidambaris-associated endophytic bacteria on peanut plant health involved selecting 30 strains related to the core flora, including Burkholderia spp., Rhizobium spp., slow-growing, Pseudomonas spp., Bacillus spp., and Bacillus spp. Among these strains, 15 were capable of nitrogen fixation, 15 could solubilize inorganic phosphorus, 10 produced chitinase, 11 produced xylanase, and 6 produced cellulase.

Ten 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