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Significance
Monoterpenes are a class of organic compounds commonly found in the essential oils of many plants, including Citrus reticulata ‘Chachi’, a species known for producing delicious and fragrant fruits like mandarins, tangerines, and oranges. Monoterpenes are responsible for the characteristic scents and flavors of numerous fruits, flowers, and herbs. In addition to their role in scent and flavor, monoterpenes may have other biological functions within the plant, such as acting as natural insect repellents or participating in plant defense mechanisms. They can also have potential health benefits for humans, including antioxidant and anti-inflammatory properties. In a new study published in the peer-reviewed Microbiome Journal led by Professor Hong Wu from the College of Life Sciences at South China Agricultural University investigated the role of microorganisms in the production of monoterpenes in Citrus reticulata ‘Chachi.’ Microbes, particularly endophytes and rhizosphere soil microorganisms, are recognized as indispensable contributors to plant health and secondary metabolite production.
The authors identified a diverse community of endophyte operational taxonomic units (OTUs) in the citrus roots and rhizosphere soil. Remarkably, some of these endophyte strains were found to have a positive correlation with monoterpene production, highlighting their potential role as microbial partners in the synthesis of these bioactive compounds. The presence of endophyte microbes in the root cortical cells and vascular cylinder cells was further substantiated through microscopy observations. These endophytes exhibited a range of morphologies and were even found to contain lipid droplets, suggesting their active participation in monoterpene synthesis. These observations underline the complexity of the microcosm within the plant root, where diverse microbial communities interact with the host plant, influencing its metabolic pathways and ultimately impacting the composition of essential oils.
To unravel the molecular mechanisms governing monoterpene production, the authors ventured into the realm of genomics. They identified genes responsible for synthesizing the precursor compounds of monoterpenes, shedding light on the biosynthetic pathways involved. The expression of these genes, particularly those encoding key enzymes for terpene synthesis, was found to be notably higher in the leaves and roots of the core region, where monoterpenes were more abundant in citrus peels.
The authors’ finding aligns with existing knowledge in the field of plant biology, where it is well-established that plants often adapt their metabolic pathways in response to environmental stressors. In this case, the higher expression of genes involved in terpene synthesis may be linked to the elevated salinity of the soil in the core region. Salt stress has previously been shown to upregulate genes associated with terpene production in plants, providing a plausible explanation for the observed patterns.
The soil in which citrus plants are cultivated plays a pivotal role in determining the composition of essential oils. In this study, soil properties were identified as a crucial factor influencing monoterpene production. Specifically, the core region soil exhibited higher electrical conductivity and elevated levels of micro-elements, including magnesium, manganese, and others. These soil properties were positively correlated with both monoterpene content and terpene backbone biosynthesis pathways. Mg, in particular, was found to serve as a cofactor that enhances the activity of terpene synthases, providing a mechanistic link between soil properties and monoterpene biosynthesis. The presence of specific micro-elements in the soil can thus be regarded as a driver for increased monoterpene production, with potential implications for agricultural practices. Formulation of fertilizers tailored to the specific needs of citrus plants in different regions could be a promising avenue for optimizing monoterpene content.
One intriguing aspect of this study was the observation that a greater number of plant immune-responsive genes were induced in the root, leaf, and peel samples of the core region. These included genes associated with resistance to abiotic stress, as well as those involved in plant immune signaling pathways. The expression of these genes was positively correlated with the content of seven monoterpenes, suggesting a potential link between plant immunity and monoterpene production. The activation of abiotic resistance genes in response to salt stress in the soil is not surprising, as plants often employ such mechanisms to cope with adverse environmental conditions. However, the study hints at a more nuanced relationship between plant immunity and terpene production. It raises the intriguing possibility that certain microorganisms in the rhizosphere may modulate plant defense responses, influencing the synthesis of monoterpenes.
The researchers explored the rhizosphere soil and endophyte microbiome. The core region’s unique soil environment, characterized by its proximity to seawater, supports a distinct microbial community. These microorganisms, enriched in salt resistance genes and terpene biosynthetic gene clusters, have the potential to influence monoterpene production in citrus plants. The findings also suggest that soil microbes with terpene synthesis potential can enter the plant roots, further substantiating the role of endophytes in monoterpene production. The interplay between soil microbes and plant roots is a dynamic process, with the potential for bidirectional signaling. Understanding the mechanisms by which plants recruit specific microbial groups and how these microbes, in turn, influence plant metabolism remains an exciting avenue for future research.
One of the most compelling aspects of this study is the synthetic community (SynCom) experiments conducted using bacterial strains derived from the rhizosphere soil and roots. Notably, Streptomyces strain Strep-4 and its SynCom were found to significantly boost monoterpene accumulation in citrus leaves, and this effect was immune-dependent. This finding underscores the intricate relationship between specific microbial strains and plant metabolism.
The Streptomyces genus, known for its prolific production of bioactive compounds, may serve as a key player in promoting monoterpene production. The results of these SynCom experiments open up exciting possibilities for targeted microbial interventions in agriculture. Harnessing the potential of specific microbial strains to enhance the bioactive compound content of crops represents a promising avenue for future research. Additionally, the Streptomyces strain Strep-4 is a halotolerant bacterium which was enriched by high soil salinity. The higher soil salinity in the core region led to the enrichment of specific halotolerant bacteria, which in turn can boost the accumulation of monoterpenes.
The findings from Professor Hong Wu and his team study have far-reaching implications for both agriculture and medicine. In the field of agriculture, the identification of soil properties and microbial communities that promote monoterpene production provides valuable insights for optimizing crop management practices. Tailoring soil conditions, including nutrient content and salinity levels, could be a strategy for enhancing the bioactive compound content of citrus fruits, ultimately improving fruit quality. From a medical perspective, the bioactive properties of monoterpenes are of great interest. Monoterpenes have demonstrated various potential health benefits, including anti-inflammatory, antioxidant, and antimicrobial properties. Understanding the factors that influence monoterpene production in citrus fruits could pave the way for the development of specialized cultivars with enhanced bioactive compound profiles. Such fruits could potentially contribute to dietary interventions aimed at improving human health. The multidisciplinary exploration of monoterpene production in Citrus reticulata ‘Chachi’ offers a captivating glimpse into the complex web of interactions between plants, soil, and microorganisms. It underscores the pivotal role of soil properties, soil microorganisms, and endophytes in shaping the bioactive compound content of citrus fruits.
Reference
Su J, Wang Y, Bai M, Peng T, Li H, Xu HJ, Guo G, Bai H, Rong N, Sahu SK, He H, Liang X, Jin C, Liu W, Strube ML, Gram L, Li Y, Wang E, Liu H, Wu H. Soil conditions and the plant microbiome boost the accumulation of monoterpenes in the fruit of Citrus reticulata ‘Chachi’. Microbiome. 2023 ;11(1):61. doi: 10.1186/s40168-023-01504-2.