Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce

Abstract

Fertilization management can affect plant performance and soil microbiota, involving still poorly understood rhizosphere interactions. We hypothesized that fertilization practice exerts specific effects on rhizodeposition with consequences for recruitment of rhizosphere microbiota and plant performance. To address this hypothesis, we conducted a minirhizotron experiment using lettuce as model plant and field soils with contrasting properties from two long-term field experiments (HUB-LTE: loamy sand, DOK-LTE: silty loam) with organic and mineral fertilization history. Increased relative abundance of plant-beneficial arbuscular mycorrhizal fungi and fungal pathotrophs were characteristic of the rhizospheres in the organically managed soils (HU-org; BIODYN2). Accordingly, defense-related genes were systemically expressed in shoot tissues of the respective plants. As a site-specific effect, high relative occurrence of the fungal lettuce pathogen Olpidium sp. (76–90%) was recorded in the rhizosphere, both under long-term organic and mineral fertilization at the DOK-LTE site, likely supporting Olpidium infection due to a lower water drainage potential compared to the sandy HUB-LTE soils. However, plant growth depressions and Olpidium infection were exclusively recorded in the BIODYN2 soil with organic fertilization history. This was associated with a drastic (87–97%) reduction in rhizosphere abundance of potentially plant-beneficial microbiota (Pseudomonadaceae, Mortierella elongata) and reduced concentrations of the antifungal root exudate benzoate, known to be increased in presence of Pseudomonas spp. In contrast, high relative abundance of Pseudomonadaceae (Gammaproteobacteria) in the rhizosphere of plants grown in soils with long-term mineral fertilization (61–74%) coincided with high rhizosphere concentrations of chemotactic dicarboxylates (succinate, malate) and a high C (sugar)/N (amino acid) ratio, known to support the growth of Gammaproteobacteria. This was related with generally lower systemic expression of plant defense genes as compared with organic fertilization history. Our results suggest a complex network of belowground interactions among root exudates, site-specific factors and rhizosphere microbiota, modulating the impact of fertilization management with consequences for plant health and performance.

Role of Benzoic Acid and Lettucenin A in the Defense Response of Lettuce against Soil-Borne Pathogens

“…To address the question whether benzoic acid, detected in rhizosphere soil solutions of soil-grown lettuce plants in previous studies [17,20,22,25] was released from plant roots or alternatively produced by rhizosphere microorganisms, lettuce was cultivated in a soil-free hydroponic culture system. Intensive microbial root colonization was reduced by frequent replacement (2-day intervals) of the nutrient solution prepared with demineralized membrane-filtered water, since a completely axenic culture of plants in hydroponics is technically difficult and not reliable for longer time periods required for the experiment.…”

“…However, so far, a causal relationship has not yet been demonstrated since it is still unknown whether the rhizosphere concentrations measured for benzoic acid in lettuce plants are sufficient to exert any inhibitory effects on growth and pathogenesis of R. solani. Based on the benzoic acid concentration determined in the rhizosphere of lettuce grown on a loamy sand with a suppressive potential against R. solani [22], a benzoic acid concentration of approx. 500 µg L −1 was calculated for the rhizosphere soil solution at a distance of 1 mm from the root surface.…”

“…RU47 and Serratia plymuthica 3Re-4-18) against the fungal pathogen were also detectable in model experiments and under field conditions [17,20,21]. Accordingly, the role of root-secreted benzoic acid in plant defense modified by the presence of beneficial rhizosphere microorganisms in the lettuce rhizosphere has been discussed [20,22].…”

“…However, investigations on root exudation of benzoic acid in lettuce have never been conducted under axenic conditions [17,18,20,22]. Therefore, it is still poorly understood whether this compound is released from plant roots or accumulates in the rhizosphere solution as rhizosphere product of microbial origin.…”

Genome-Based Characterization of Plant-Associated Rhodococcus qingshengii RL1 Reveals Stress Tolerance and Plant–Microbe Interaction Traits

“…This report emphasizes the importance to understand the role of all relevant members in the plant holobiont. The multifaceted interactions of plants and several plant-associated bacteria have been widely studied to understand the underlying molecular mechanisms and to exploit plant beneficial traits for sustainable agriculture ( Berg et al, 2017 ; Rodriguez et al, 2019 ; Babin et al, 2021 ; Windisch et al, 2021 ). In this context it is important to further the knowledge of the functional repertoire also of yet lesser known members of the plant microbiome such as Rhodococcus to understand what enables them to interact with the plant as well as other microbes and which traits could be useful for an application in specifically demanding agricultural scenarios.…”