The Intricate World of Plant-Microbe Metabolite Interactions

Plants are fascinating organisms that play a crucial role in maintaining the balance of our ecosystem. One of the remarkable ways they do this is by releasing up to 40% of their photosynthetic products as root exudates into the rhizosphere. These root exudates are like a secret language that plants use to communicate with the surrounding soil microorganisms. They act as powerful recruiters, attracting beneficial microbes and skillfully regulating the composition and structure of the rhizosphere microbiome.
When combined with the metabolites produced by rhizosphere microorganisms, they form what is known as the rhizosphere metabolome. This metabolome is not just a random collection of chemicals; it’s a sophisticated toolkit that plants and microbes use to enhance nutrient acquisition and boost the plant’s immune response. In essence, it’s the key to promoting healthy plant growth and ensuring the plant’s survival in various environmental conditions.
The plant roots are like discerning shoppers, carefully selecting and luring specific microbial species from the surrounding soil. This process leads to the establishment of a highly specialized and functionally diverse microbial community in the rhizosphere. The rhizosphere metabolites, which include both root exudates and microbial metabolites, serve dual purposes. They function as both signals, transmitting important information between plants and microbes, and as nutrients, providing essential nourishment for the growth and survival of these microorganisms. In this way, they have a significant impact on the formation of the rhizosphere microbial community and play a pivotal role in the communication between plants and microbes.
However, the environment and its complex feedback loops further complicate these already intricate interactions. Despite the significant progress made in understanding plant-microbe relationships, there are still many mysteries surrounding how specific metabolites shape these interactions and contribute to the diverse functions observed in the rhizosphere. A recent comprehensive review has attempted to shed light on these questions. It has summarized the latest advancements in compound-mediated plant-microbe communication and explored the role of these interactions in plant adaptation and ecosystem function. Additionally, the review has proposed several promising future research directions aimed at manipulating metabolite-mediated plant-microbe interactions to enhance crop productivity and improve plant health.
 
By uncovering the biological functions of specific metabolites produced by plants and microbes, we can bridge the gap between basic research and practical applications, opening up new possibilities for sustainable agriculture and environmental conservation.

Plants produce an astonishingly large number of root exudates, which are a complex mixture of various compounds. These compounds can be broadly classified into two main categories: primary metabolites and secondary metabolites. Primary metabolites, such as sugars, amino acids, and organic acids, are essential for the basic physiological functions of the plant. They are involved in processes like energy production, growth, and reproduction. On the other hand, secondary metabolites, which include terpenoids, flavonoids, phenolic acids, siderophores, peptides, and enzymes, are not directly involved in these basic functions but play crucial roles in plant defense, communication, and adaptation to the environment.

2. Characteristics and Functions of Rhizosphere Microbial Metabolites

In addition to root exudates, microbial metabolites are increasingly recognized as a promising source of functional chemicals in the rhizosphere, which can contribute to the sustainable development of agriculture. However, similar to root exudates, the classification of microbial metabolites lacks standardization, and many compounds are mainly classified based on their structures and functions. According to the elemental composition of microbial metabolites, they can be divided into seven categories: lignin-like, lipid-like, unsaturated hydrocarbons, condensed aromatics, proteins, carbohydrates, and tannins (Yang et al., 2024). Based on their functions, primary metabolites, which are essential for microbial growth, drive the synthesis of a series of low molecular weight (MW) chemicals, such as amino acids, vitamins, fatty acids, and nucleotides. These substances are crucial for DNA replication and the rapid proliferation of microorganisms.
In addition to these growth-related compounds, some secondary metabolites function as signal molecules or aid in nutrient absorption. These compounds can be released as low or high molecular weight substances to establish long-distance communication with surrounding cells or compete with antagonistic organisms for habitats. It is worth noting that microorganisms, especially bacteria and archaea, produce special substances that are different from root exudates. These special substances are called extracellular polymeric substances (EPS), which are key components of biofilms. Unlike single-compound metabolites, EPS is a complex metabolic consortium composed of polysaccharides, proteins, lipids, and even extracellular DNA. Due to their plasticity under environmental perturbations, EPS is of great significance for the environmental adaptability of microorganisms. Moreover, the composition and diversity of microbial metabolites, including the properties of EPS, vary depending on the microbial species and their genomic constitution. Generally, microorganisms with larger genomes have more diverse metabolite profiles.

3. The Impact of Metabolite-Mediated Plant-Microbe Interactions on Environmental Adaptation and Ecosystem Function

By releasing specific exudates, plants establish a close relationship with the surrounding rhizosphere microbial community, initiating plant-microbe interactions that help alleviate various adverse conditions. Root exudates mainly consist of labile carbon compounds, which promote the reproduction of microorganisms and facilitate the interaction between plants and microbes in the rhizosphere. Although rhizosphere symbiotic microorganisms are mostly neutral in most cases, some symbiotic microorganisms can form symbiotic relationships with host plants. Among the interactions between plants and microbes, the most well-known processes are the symbiosis between plants and symbiotic mycorrhizal fungi and rhizobia. Once a symbiotic relationship is established, the host plant provides lipids to AM fungi, and in return, the fungi provide the host with a large amount of phosphorus and nitrogen (Jiang et al., 2017). Leguminous plants can obtain ammonia from root nodules and provide carbohydrates to rhizobia as nutrients. Although the symbiotic relationship of rhizobia is less common than that of mycorrhizal fungi, the reciprocal interaction between leguminous plants and rhizobia shares a common symbiotic signaling pathway with AM fungi. Interestingly, the formation of the AM symbiotic relationship can also promote the symbiosis between leguminous plants and rhizobia, indicating a potential promoting effect between these two reciprocal interactions.

In recent years, significant progress has been made in revealing the diversity and chemical structures of root exudates and microbial metabolites. Evidence shows that plant genetics drives the assembly and function of the rhizosphere microbiome through metabolic control. Therefore, uncovering the chemical and genetic clues in plant-microbe communication will contribute to the development of sustainable agriculture. However, due to the complex plant-microbe interactions involving metabolites, the application of metabolite-triggered microbial engineering in improving plant adaptability and the sustainability of agricultural ecosystems has had mixed results. The latest advancements in technologies such as mass spectrometry, multi-omics, and synthetic community research will help us gain a more detailed understanding of the mechanisms of plant-microbe interactions mediated by root exudates and microbial metabolites. In addition, the targeted manipulation of SynComs designed through machine learning may pave the way for precision agriculture microbiome engineering to enhance plant stress resistance and nutrient absorption capacity.

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