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Review

Exploring the Potential of Russula griseocarnosa: A Molecular Ecology Perspective

by
Yuanchao Liu
,
Tianqiao Yong
,
Manjun Cai
,
Xiaoxian Wu
,
Huiyang Guo
,
Yizhen Xie
,
Huiping Hu
and
Qingping Wu
*
National Health Commission Science and Technology Innovation Platform for Nutrition and Safety of Microbial Food, Guangdong Provincial Key Laboratory of Microbial Safety and Health, State Key Laboratory of Applied Microbiology Southern China, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, China
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(6), 879; https://doi.org/10.3390/agriculture14060879
Submission received: 12 April 2024 / Revised: 29 May 2024 / Accepted: 30 May 2024 / Published: 31 May 2024
(This article belongs to the Special Issue Genetics and Breeding of Edible Mushroom)
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Abstract

:
Russula griseocarnosa, an edible and medicinal mushroom abundant in nutrients and notable bioactivities, is predominantly grown in the broad-leaved forest with trees of the family Fagaceae in southern China. This species forms ectomycorrhizal associations with plant roots and cannot be artificially cultivated currently. Previous research indicates a strong correlation between the growth of R. griseocarnosa and factors such as the host plant, climate variables (specifically mean temperature and precipitation from June to October), and the rhizosphere microbiota of its habitat. However, comprehensive studies on the fundamental biology of this species are lacking. The interaction between R. griseocarnosa and its host plant, as well as the mechanisms underlying the microbial community dynamics within its habitat, remain ambiguous. The limited repertoire and diversity of carbohydrate-active enzymes (CAZymes) in R. griseocarnosa relative to saprophytic fungi may contribute to its recalcitrance to cultivation on synthetic media. The specific core enzyme and the substances provided by the host plant to facilitate growth are yet to be elucidated, posing a significant challenge in the artificial cultivation of R. griseocarnosa. The habitat of R. griseocarnosa harbours unique microbial communities, indicating the presence of potentially beneficial microorganisms that could be exploited for artificial propagation and conservation efforts. However, the lack of definitive functional verification experiments hinders the realization of this promising prospect. This review offers a comprehensive overview of the nutritional profile and health benefits of R. griseocarnosa, emphasizing recent developments in its isolation, molecular ecology, and artificial cultivation. Additionally, it explores prospective advancements in R. griseocarnosa research, aiming to enrich our foundational understanding for applied purposes and fostering progress in the realm of ectomycorrhizal edible mushrooms.

1. Introduction

The genus Russula is widely distributed globally and has significant economic and research importance. It represents a group of ectomycorrhizal fungi utilised for culinary and medicinal purposes [1,2]. Worldwide, there are 2759 identified taxonomic units identified within Russula [3]. A total of 193 taxonomic units have been reported in China, with 158 confirmed through specimen examination [4,5]. Among these, 82 species are edible, while 22 possess medicinal properties due to their various nutrients and bioactive compounds [6,7,8,9,10,11,12]. Russula spp. have a long medicinal history in China, being used alone or combined with other herbs in traditional Chinese medicine, as documented in ancient pharmacopoeias such as “Compendium of Materia Medica” and “Comprehensive Records of the Eight Min Regions”. Valued for their health advantages, Russula spp. have been favoured by generations [13,14]. Russula griseocarnosa X.H. Wang, Zhu L. Yang, and Knudsen 2009 was a new species of Russula found in Southern China and could also be grown in Northeast India [15] and northeast Vietnam [16]. It has a distinct greyish-dense context, brownish-red pileus, and elongated spines [17,18]. Recognised as one of China’s top ten wild edible fungi at the 2016 China Nanhua Wild Mushroom Conference, R. griseocarnosa was an ectomycorrhizal mushroom with high nutrients and health care properties [15,16], including anticancer, antioxidation, antifatigue, hypolipidemic, immunoregulation, and hematopoietic properties [19,20,21,22]. Highly prized in southern Chinese regions as a postpartum health supplement, its dried form fetches up to 2000 yuan/kg (277.78 USD/kg) in Meizhou (Guangdong, China) due to limited and unstable natural yield. As it requires symbiosis with Fagaceae tree roots [23,24], artificial cultivation is currently unfeasible using the cultivation method for saprophytic mushrooms. Existing research efforts on R. griseocarnosa have predominantly focused on evaluating its nutritional profile and therapeutic potential, complemented by investigations into its genomic characteristics and the microbial ecology of its natural habitat. Nevertheless, compared to other widely studied edible mushrooms, our current knowledge of R. griseocarnosa remains relatively limited, lacking in-depth and comprehensive analyses. We used literature research methods to search for relevant research on R. griseocarnosa from databases such as the China National Knowledge Infrastructure (CNKI), Web of Science, and Google Scholar and conducted a review of this edible mushroom.
This review synthesizes the current research on the nutritional composition and bioactivity of R. griseocarnosa. It provides a comprehensive elaboration on the progress made in understanding the molecular ecology and artificial domestication of this mushroom. By integrating the ongoing research by the authors, this review offers perspectives on potential breakthroughs for the future for R. griseocarnosa research to drive fundamental investigations to enable its applications. Advancements in elucidating the nutritional profile, bioactive compounds, molecular mechanisms underlying its bioactivities, and strategies for successful cultivation will pave the way for developing R. griseocarnosa as a valuable resource for food, pharmaceutical, and other industrial applications.

2. Methods

Literature research methods were employed for this review. The literature sources are from the CNKI (China National Knowledge Infrastructure), Web of Science, and Google Scholar. The main keywords used are Russula, R. griseocarnosa, Ectomycorrhizal fungi, domestication, cultivation, symbiotic, microorganism, environmental microbiome, and genome. The retrieved literature was screened and deduplicated, low-quality literature was removed, and research not related to R. griseocarnosa was eliminated. At the same time, considering that R. griseocarnosa is a well-known ectomycorrhizal edible fungus, some of the literature related to the research background is supplemented, and then the literature was classified and recapitulated. The current research results are summarised, and the authors’ insights are presented. Finally, an outlook is provided based on the current research status and the development of new technologies.

3. Results

3.1. Nutritional Composition of R. griseocarnosa

The fruiting body of R. griseocarnosa is replete with essential nutrients such as amino acids, proteins, and efficacious components like polysaccharides. Research indicates that its protein and crude fat content surpasses that of similar edible fungi such as R. virescens and Cantharellus cibarius Fr. 1821, with the pileus of the mushroom exhibiting higher concentrations of these nutrients compared to the stipe. Mineral element analysis reveals that R. griseocarnosa is rich in phosphorus, potassium, iron, sodium, calcium, magnesium, and zinc, displaying a characteristic of high potassium and low sodium content, which holds potential health benefits for individuals with hypertension. Furthermore, this mushroom contains seven types of fatty acids, with oleic acid predominant in the pileus and linoleic acid abundant in the stipe, surpassing common foods like eggs and chicken in fatty acid content, overall; both the pileus (80.69%) and the stipe (69.13%) showed advantages over eggs (15.1 ± 0.79%) and chicken (23.34 ± 3.56%), presenting healthier characters (Table 1). Moreover, R. griseocarnosa serves as a high-quality protein source, containing a significant amount of essential amino acids such as valine, lysine, phenylalanine, tyrosine, and threonine, far exceeding the FAO/WHO standard protein model [25].
Owing to the close association between free amino acids and the taste and nutritional value of mushrooms, researchers have employed LC-MS/MS methods to determine the levels of free amino acids across different developmental stages of R. griseocarnosa. The results indicate that among the three stages of fruiting body development, the total content of free amino acids exhibits a slight increase from 19.88 mg/g (dry weight) in the first stage (Young period, egg shape) to 20.57 mg/g in the second stage (cap is not fully open), then significantly decreases to 14.42 mg/g in the third stage (cap entirely open). Concurrently, during the three developmental stages, compounds resembling monosodium glutamate, including aspartic acid and glutamic acid, exhibit substantial variations in content, all showing a decreasing trend [28]. The flavour of R. griseocarnosa is also influenced by its volatile oil components. Researchers have utilised gas chromatography-mass spectrometry (GC-MS) to analyse volatile oil extracts of R. griseocarnosa. The results indicate that the volatile oil components from the fruiting bodies of R. griseocarnosa primarily consist of compounds such as ketones, aldehydes, acids, alcohols, esters, alkanes, and alkenes. It is suggested that the unique aroma of R. griseocarnosa is attributed to its abundant content of ketones and aldehydes [29]. Combined with our own test results, we compiled Appendix A Table A1 for the volatile oil components of R. griseocarnosa. Additionally, R. griseocarnosa is also rich in other bioactive substances such as ergosterol, phenolic compounds (e.g., quercetin), and crude polysaccharides, which can serve as potential raw materials for developing health products [25,30,31].

3.2. Health Benefits of R. griseocarnosa

Over the past two decades, the efficacy of Russula mushroom extracts have been extensively studied in China, with reported benefits primarily encompassing antioxidation, free radical scavenging, antifatigue, antiaging, hepatoprotection, blood sugar and lipid reduction, tumour inhibition, and antibacterial properties. For instance, it has been reported that the extract from Russula mushroom fruit bodies can ameliorate oxidative damage induced by formaldehyde inhalation in mice [20], as well as increase the levels of glutathione and superoxide dismutase in mouse serum, enhancing their ability to adapt to exercise loads, resisting fatigue generation, and accelerating fatigue elimination [32,33,34]. Additionally, the extract exhibits antioxidative effects in aged mice [35]. Moreover, polysaccharides of Russula demonstrate significant scavenging effects on superoxide anions and hydroxyl radicals [36]. Feeding with powder and polysaccharides of Russula has been found to significantly reduce blood glucose, total cholesterol, triglycerides, and low-density lipoprotein levels in mice with hyperglycaemia and hyperlipidaemia models, showing a dose-dependent response and indicating notable hypoglycaemic and lipid-lowering effects of Russula. Similarly, injection of polysaccharides of Russula has been shown to reduce cholesterol levels in rats with hyperlipidaemia, resulting in a significant 45.2% reduction in total cholesterol compared to the control group [37,38]. The alcohol extracts from Russula fruit bodies have been tested and found to possess certain antibacterial properties against Escherichia coli and Staphylococcus aureus [39]. Additionally, lectins isolated from fresh fruit bodies of Russula exhibit potent inhibitory effects on the proliferation of HepG2 hepatoma and MCF7 breast cancer cells, although interspecies differences may exist in their inhibitory activities against ribonuclease and HIV-1 reverse transcriptase [40,41,42]. Furthermore, polysaccharides of Russula have been shown to promote lymphocyte activity, achieving an inhibitory effect on SiHa cancer cell proliferation [43].
It should be noted that most of the materials used in the above studies come from Rongxian County, Guangxi, China. Due to the difficulty of classifying the genus Russula [44], and the fact that there are many closely related species of R. griseocarnosa that have not yet been identified [45], although these materials in some studies may be R. griseocarnosa, it has not been clearly stated. Instead, some of the research indicates that the materials are Russula vinosa Lindblad 1901, Russula delica Fr. 1838, and Russula lepida Fr. 1836, which has caused confusion in accurately understanding the efficacy of R. griseocarnosa. Fortunately, to ensure the accuracy of this review, we have primarily incorporated research materials that were unambiguously identified as R griseocarnosa. The subsequent research progress discussed in this review largely stems from experiments where R. griseocarnosa was the main study material utilised.
Polysaccharides extracted from R. griseocarnosa fruit bodies demonstrate a certain clearance effect on hydroxyl radicals and superoxide radicals. In vitro cell experiments confirm the significant inhibitory effect of red mushroom polysaccharides on cancer cells Hela and SiHa, along with a noticeable enhancement in the phagocytic capability of peritoneal macrophages in mice. This enhancement promotes the secretion of NO and cytokine IL-6, demonstrating strong immunomodulatory activity [31,46]. Volatile oils and petroleum ether extracts from R. griseocarnosa fruit bodies exhibit strong antibacterial effects against Staphylococcus aureus and others, while the ethanol extract shows less significant antibacterial activity. Additionally, methanol extracts from fruit bodies demonstrate inhibition and scavenging effects on hydroxyl radicals generated by DPPH and Fenton reactions, confirming the natural antimicrobial, antioxidant, and free radical scavenging properties of R. griseocarnosa. [25]. Of these, the bioactive compounds may be phytochemicals such as phenolics, flavonoids, ergosterol, and β-carotene (Table 2). The major antioxidative component in R. griseocarnosa was quercetin, which was detected in levels up to 95.82 μg/g. On the other hand, the chemical constituents of R. vinosa were examined carefully, leading to the discovery of 15 compounds. Wherein four sesquiterpenes, eight triterpenes together, and three compounds containing N element were included, some of which showed inhibitory effects on nitric oxide (NO) production.
Studies have also shown that fresh fruit bodies of R. griseocarnosa were observed to stimulate the activities of phenylalanine ammonia-lyase (PAL) and chalcone synthase, consequently leading to an enhanced accumulation of phenolic and flavonoid contents when treated with nitric oxide fumigation. This can enhance the bioactive compounds and improve antioxidant activities in the mushrooms [48]. This result was similar to the studies on other fungi that demonstrated the promotive effect of NO on the biosynthesis of fungal secondary metabolites [49].
The polysaccharide PRG1-1, isolated from the fruiting body of R. griseocarnosa, exhibited antiproliferative effects on HeLa and SiHa cervical carcinoma cells. It significantly reduced cell viability, increased lactate dehydrogenase (LDH) and reactive oxygen species (ROS) production, and enhanced the apoptotic rate. These findings highlight the promising potential of the bioactive PRG1-1 as a natural agent for inhibiting tumour cell proliferation in the treatment of cervical cancer [50]. Also, PRG1-1 has the capacity to activate macrophages via the NF-κB and MAPK pathways, which exhibit immunomodulatory potential [51].
The latest research confirms that polysaccharide (RGP1) derived from R. griseocarnosa can improve hematopoietic function in K562 cells. Mechanism studies show that RGP1 could alleviate hematopoietic dysfunction by promoting the activation of CD4+ T cells and the Janus kinase/signal transducer and activator of the transcription three pathway; this study provides compelling evidence for the application of R. griseocarnosa to improve hematopoietic dysfunction [52]. This is similar to the reported active polysaccharide function of edible mushrooms [53]. Still, it is the first edible fungus with a blood-tonifying effect confirmed via animal experiments, and it is of great significance for the development of blood-enhancing dietary supplements. The polysaccharide RGP2 isolated from the fruiting body of R. griseocarnosa modulated gut microbiota composition and serum metabolite expression, and regulated T cell differentiation to enhance immune function in cyclophosphamide (CTX)-induced immunosuppressed mice [54]. This discovery provides a potential drug lead compound for the development of new natural immune modulators and has important application prospects for improving immune-related diseases and enhancing the body’s immunity. The above results showed that Polysaccharides from R. griseocarnosa exhibit antioxidant, antimicrobial, immunomodulatory and anticancer properties. Further research on these bioactive compounds from R. griseocarnosa holds great promise for developing novel therapeutic agents and nutraceuticals.

3.3. Isolation and Identification of ‘Strains’ from R. griseocarnosa

The mycelium of R. griseocarnosa is considered the premise and basis for its research and application. Therefore, the focus of researchers has consistently been on obtaining effective culture conditions. The predecessors mainly adopted the method of tissue and basidiospore separation to isolate the strain. Research has primarily centred on identifying suitable nutrients and conditions for its growth, such as carbon and nitrogen sources [55,56,57,58,59,60,61,62,63,64], mineral elements [65], vitamins, plant growth regulators [66], rare earth elements [67], and extracts from tree roots and insect dung [68] in the medium, as well as pH, incubation temperature, time [69,70,71], and light [72]. However, identification of most of the strains has not been confirmed. A small number of strains have been identified as other fungi [73,74,75], such as Monochaetia Sacc [56] and Nectria sp. [76], by morphological or molecular biology methods, suggesting the existence of a variety of endophytes in the fruiting bodies and making it more challenging to isolate the pure culture of R. griseocarnosa compared to other saprophytic mushrooms [77].
The work of HINTIKKA et al. suggests that the slow growth of mycorrhizal fungal mycelium may be attributed to a deficiency in specific nutrients, such as vitamins. In contrast, it is proposed that the mycelium of R. spp. can achieve better growth in media lacking an additional carbon source, implying that the nitrogen source and trace elements may be more critical factors. However, the mycelium mentioned in the study has not been determined with molecular identification [78].
Several media listed in the <Handbook of Microbiological Media (Fourth Edition)> [79], such as MMN, Hagem’s Modess Medium, and Oddoux Medium, which are suitable for isolating ectomycorrhizal fungi, were tested by the authors. However, attempts to obtain a pure culture of R. griseocarnosa were unsuccessful, and instead, multiple endophytes were isolated and identified. Additionally, efforts were made to obtain the R. griseocarnosa strain from ectomycorrhizas, referencing the work of Yamada et al. [80], as well as co-culturing basidiocarp tissue with the host plant’s callus [81]. Yet, the mycelia obtained through these methods were identified as plant endophytes using molecular techniques.
Furthermore, analyses of genome-wide genes have revealed that the types and quantities of carbohydrate-active enzymes in R. griseocarnosa are significantly less than those found in saprophytic mushrooms, which provides a molecular-level interpretation of the difficulty in obtaining a pure culture of this species on artificial media [82,83]. Given these findings, it is concluded that a verified pure strain of R. griseocarnosa cannot be obtained under artificial conditions.

3.4. The Symbiotic Characteristics of R. griseocarnosa

Ectomycorrhizal fungi are commonly observed to exhibit preferential associations with specific host plants, and these host preferences are believed to be important evolutionary drivers of ectomycorrhizal fungal diversification [84]. Current studies have shown that Fagaceae trees are necessary and play a vital role in the formation of fruiting bodies of R. griseocarnosa [31]. However, the symbiotic mechanism between R. griseocarnosa and its host plant remains unclear. It is generally accepted that ectomycorrhizal fungi are indispensable mutual aid partners for many trees and shrubs in forest ecosystems. More than 80% of plant nitrogen and phosphorus is provided by these mycorrhizal fungi, and many plant species depend on these symbionts for their growth and survival [85,86,87]. Additionally, ectomycorrhizal fungi are thought to have acquired the ability to colonise plant root tip tissues like plant pathogens to obtain host-derived glucose [88,89].
Ectomycorrhizal fungi have been thought to possess the ability to decompose organic matter in the soil. However, it is now understood that they do not directly utilise the carbon sources that are released into the soil through decomposition processes [90]. Furthermore, the ability of ectomycorrhizal fungi to decompose lignocellulose and cellulose has been found to be much lower than that of wood-decay and soil-dwelling saprotrophic microbes [87,91].
Ectomycorrhizal fungi have evolved to become highly dependent on their host plants, primarily relying on the latter to provide simple carbohydrates. This evolutionary trajectory has been shaped by the convergent loss of gene families responsible for the degradation of organic matter. Notably, ectomycorrhizal fungi do not require the ability to degrade lignocellulose, as they can maintain the integrity of host plant cells by avoiding the release of plant cell wall-degrading enzymes (PCWDEs). In this process, a substantial number of PCWDE and lignin-oxidizing class II peroxidase genes have been lost, with peroxidases for lignin oxidation and cellulases for cellulose degradation being the most extensively lost. Furthermore, ectomycorrhizal fungi have almost entirely lost the GH6 and GH7 family genes encoding cellobiohydrolase, which are present in soil saprophytes and white-rot fungi [92,93,94]. These observations suggest that ectomycorrhizal fungi have evolved repeatedly and independently from ecologically diverse ancestors, such as brown-rot fungi, white-rot fungi, and other saprotrophs, and the loss of genes encoding PCWDEs is considered a primary process in their evolution from saprophytic ancestors. However, some essential genes with a potential role in mycelial growth and fruit body development, such as those encoding lytic polysaccharide monooxygenase (LPMO), laccase, decolourising oxidase, and heme thiol peroxidase, have been maintained in ectomycorrhizal fungi [94,95,96], indicating that these genes provide apparent advantages in adaptation.
The diversity of degradative enzymes retained by different ectomycorrhizal fungi is thought to reflect their polyphyletic origins and may also indicate changes in their decay abilities [94]. During the process of symbiosis with the host, the ectomycorrhizal fungus Laccaria bicolor (Maire) P.D. Orton 1960 can block the expression of defence genes related to the jasmonic acid signaling pathway by secreting effectors such as the MiSSP7 protein, which binds to the inhibitor of the plant jasmonic acid signal pathway. This allows the fungal mycelium to be successfully colonised in the cortical cytoplasmic exosome area, ultimately forming a Hartig net. Meanwhile, the host plant can also secrete small secreted proteins (SSPs) into the fungal mycelium, affecting the growth and morphology of the mycelium [97], to maintain the mutual benefit state of ectomycorrhizal symbiosis [98,99].
Research has shown that the development of symbiosis requires the active functioning of multiple gene networks [100]. While some progress has been made in the study of the symbiosis between L. bicolor and host plants, the molecular mechanisms underlying this symbiosis have not been fully elucidated. In particular, the specific genes responsible for the establishment and maintenance of the ectomycorrhizal symbiosis remain unclear [85].
Research on the symbiotic mechanisms of R. griseocarnosa is quite limited. In the present study, the genome of R. griseocarnosa was analysed, revealing that the type and number of carbohydrate-metabolizing enzymes are significantly reduced compared to saprophytic fungi. However, the cellulose-degrading enzyme LPMO and GH6 and GH7 family genes are still found, slightly differing from previous conclusions. Notably, no homologous genes of MiSSP7 were identified in the predicted coding genes of R. griseocarnosa, suggesting that there may be other mycorrhizal-induced small secreted proteins (MiSSPs) involved in the symbiotic recognition between R. griseocarnosa and its host plant. Phylogenetic tree analysis based on whole-genome construction has shown that R. griseocarnosa and other ectomycorrhizal fungi are grouped together, clearly distinguished from saprophytic fungi, indicating their significant symbiotic properties [83].

3.5. Habitat Molecular Ecology of R. griseocarnosa

Previous studies have suggested that ectomycorrhizal fungi, such as Russula spp., tend to appear primarily during the later stages of forest succession [78,101]. Environmental selection and dispersal limitation are considered the two main processes shaping the construction of biological communities in ecosystems [102]. The dispersal of basidiospores is an essential factor affecting the diversity of fungal communities [103]. Bioinformatic analyses of operational taxonomic units (OTUs) have shown that ectomycorrhizal fungal groups in forests at different successional stages (young, intermediate, and old) are diverse and can be affected by various types of factors [104]. Furthermore, there is competition between different ectomycorrhizal fungi in forests, which in turn impacts species richness [105], the species abundance of Russula has exhibited unstable characteristics, with both increases and decreases observed along the forest succession gradient. Based on our present investigation, the appearance of R. griseocarnosa is typically associated with forests older than 50 years and without large-scale deforestation. Although the altitudinal gradient has been identified as an important factor affecting the diversity of ectomycorrhizal fungi [106,107], the findings demonstrate that R. griseocarnosa can be widely distributed, ranging from 244 m to 2100 m in the Guangdong, Fujian, and Yunnan provinces of China.
Soil is an integral component of terrestrial ecology. Soil characteristics, such as pH, organic carbon, nitrogen, and phosphorus, have significantly influenced the structure of soil microbial communities [108,109,110]. Additionally, the vertical stratification of the soil profile has been observed to exert similar effects, with the abundance of ectomycorrhizal fungi decreasing with increasing depth of the soil layer [111]. It has been observed that R. griseocarnosa generally grows in the shallow soil layer, with only a small portion of the stipe penetrating the soil. The microbiome compositions of soil at different depths within the rhizosphere of R. griseocarnosa were determined through 16S rRNA gene sequencing, revealing a significant difference in the soil diversity index between the surface and deeper soil layers in the habitat of R. griseocarnosa (unpublished data).
Among the various factors that can affect the occurrence of R. griseocarnosa, biological interactions are considered to be of critical importance. Soil bacteria, for instance, have been shown to influence the abundance of ectomycorrhizal fungi by affecting the cycling of soil nutrients [112,113]. Previous studies on mycorrhiza helper bacteria (MHB) have suggested that there are physical and metabolic interactions between soil microorganisms, mycorrhizal fungi, and host plants.
R. griseocarnosa is widely distributed across southern China, a region characterized by diverse climatic conditions. Notably, ectomycorrhizal fungi have been observed to associate with different MHB under varying climatic regimes [114]. Considering the differential composition of mycorrhizal helper bacteria in response to climatic factors, more extensive analyses of habitat microbiomes are warranted to identify the common and unique MHB associated with R. griseocarnosa throughout this region. By examining the microbial communities across the diverse environments inhabited by this fungal species, researchers can gain a comprehensive understanding of the microbial partners involved in facilitating ectomycorrhizal symbioses, and how these partnerships adapt or diverge in response to the heterogeneous climatic conditions prevalent in southern China.
The other microorganisms present in the rhizosphere affect the establishment of mycorrhizal symbiosis on plant roots [115]. For example, MHB and host plants have been reported to release substances akin to vitamins, which can promote the formation of mycorrhizal symbiosis [116,117].
Studies on soil microorganisms in the habitat of R. griseocarnosa were conducted using Illumina high-throughput sequencing, which revealed that the main rhizosphere bacteria exhibited a similar community structure. However, the diversity of rhizobacteria was significantly lower than that of non-rhizosphere bacteria. Notably, the bacterial secretion system, tyrosine metabolism, biosynthesis of unsaturated fatty acids, and vitamin metabolism were much more abundant in the rhizosphere. The results suggest that soil pH and available nitrogen were the primary factors influencing the microbial community structure, and these rhizosphere bacteria play a vital role in the growth of R. griseocarnosa [118].
Similarly, research employing comparable methods has been conducted to study the dynamic composition of microbial communities associated with Russula in the Russula-Fagaceae nature areas of Fujian province, China. The findings revealed that the fungal diversity of the Russula habitat was negatively correlated with the occurrence of Russula. These potential indicator species associated with sporocarp production in Russula may provide a new strategy for improving Russula symbiosis and sporocarp yield [119]. The research highlighted above has focused on exploring the microbial community structure within the native habitat of R. griseocarnosa. However, it is essential to note that the wild environment contains not only R. griseocarnosa but also other microorganisms, particularly those similar to R. griseocarnosa. Are there any similarities in the habitat microorganisms associated with these related species? In addition, rare microorganisms with relatively low abundance in ectomycorrhizal fungal habitats are often overlooked. Wei Ge et al. [110]. conducted a study on the bacterial community in the fruiting body and mycosphere of Cantharellus cibarius. Similar to previous research findings, they observed a higher proportion of specialist bacteria compared to generalist bacteria in the fruiting body and mycosphere. Analysis of the metabolic functions and phenotypes of abundant and rare bacteria revealed that while abundant bacteria exhibited specific potential functions, rare bacteria may contribute supplementary or unique metabolic pathways (such as sulfite oxidizer and sulfur reducer) that enhance the ecological function of C. cibarius. This study elucidates the distribution and function of specific microorganisms from the perspective of the fruiting bodies of ectomycorrhizal fungi and rare bacteria in their mycosphere, providing a new perspective for deepening our understanding of the ecological functions of microbiota on ectomycorrhizal fungi.
The habitat microbial populations of R. griseocarnosa and its similar species were also studied. The results indicate that the evenness of soil fungi in the habitats of various species’ fruiting bodies is not significantly different. However, R. griseocarnosa was found to have higher species richness, and there was no notable difference in the abundance of the top 10 soil microorganisms corresponding to the relative abundance of each species. Interestingly, the soil fungus Aspergillus citocrescens, which has a lower relative abundance, was significantly higher in the habitat of R. griseocarnosa. So, A. citocrescens was inferred to be a key species in the soil microhabitat under the fruiting bodies of R. griseocarnosa and may play an essential role in the formation of the rhizosphere microecology [120]. The study has also revealed that different ectomycorrhizal fungi may be able to reshape the soil microecology within their respective habitats. An analogous investigation for mycosphere soil microbiomes associated with R. griseocarnosa and its similar species R. rosea by Yu Fei et al. [121] revealed findings that were not entirely congruent; although significant differences were observed in the dominant microbial flora between the two ectomycorrhizal rhizospheres, certain bacterial and fungal taxa emerged as dominant ectomycorrhizal helper microorganisms shared by both Russula species. The bacterial taxa identified as prominent in this mutualistic association included Variibacter, Candidatus_Solibacter, Sorangium, Mycobacterium, Singulisphaera, Isosphaera, Bdellovibrio, and Paenibacillus. Additionally, the fungal genera Trichoderma, Penicillium, and Hypomyces were found to be prevalent ectomycorrhizal helper microorganisms. Remarkably, these bacterial groups possess diverse functional capabilities that facilitate the establishment of symbiotic relationships between the mushrooms and plant roots. Notably, these bacteria exhibit traits conducive to plant cell wall degradation, atmospheric nitrogen fixation, and solubilization of phosphorus, thereby enhancing nutrient acquisition and promoting the formation of ectomycorrhizal association. The study highlights the significance of these microbial consortia in mediating the intricate symbiotic interactions between ectomycorrhizal fungi and their plant hosts.
The research findings described above have indeed indicated the potential presence of indicator microorganisms or growth-promoting microbes within the habitat of R. griseocarnosa. However, field investigations revealed that, despite significant variations in soil physical and chemical properties, such as soil particle size and soil humus content, across different growth sites—which can lead to alterations in the microbial community composition [109]—R. griseocarnosa was still capable of thriving normally as long as the host plant was present within the forest ecosystem. This suggests that the specific microbial community structure observed within the habitat of R. griseocarnosa may not be solely attributable to the presence of the fungus itself. Rather, the root exudates of the host plant, which can potentially influence the physical and chemical properties of the habitat soil, may be an essential factor affecting the growth and development of R. griseocarnosa.
It also further indicates that the complex interactions between R. griseocarnosa, its host plant, and the soil environment, including the physicochemical characteristics and microbial community composition, collectively contribute to the successful establishment and thriving of this ectomycorrhizal fungus. The influence of host plant-derived metabolites on the soil habitat appears to be a crucial component in understanding the ecology and niche requirements of R. griseocarnosa. Further research is needed to elucidate the specific mechanisms by which the host plant and its root exudates shape the soil environment and microbiome, thereby supporting the growth and fruiting of R. griseocarnosa. This holistic perspective, considering the tripartite relationship between the fungus, host plant, and soil, is essential for gaining a comprehensive understanding of the ecology and habitat preferences of this economically and ecologically critical ectomycorrhizal species.

3.6. Artificial Domestication

As an ectomycorrhizal fungus, effective isolation of pure cultures of R. griseocarnosa has not been achieved to date [122,123]. Existing studies have attempted to increase yield or obtain fruiting bodies by improving the forest environment or inoculating the wild habitat. Related reports [124,125,126,127] have indicated that spraying spore suspensions of R. griseocarnosa into the forest or applying solid inoculum formulations containing the isolated ‘strain’ under seedbeds or seedlings can be beneficial for the formation of mycorrhizal seedlings or increasing the diversity of ectomycorrhizal fungi in the forest. These approaches are expected to improve the production of R. griseocarnosa eventually. Transforming the woodland environment has also been considered as a means to increase the yield [128,129].
Current research on the soil microbiome has shown that mycorrhiza helper bacteria (MHB), such as Mycobacterium spp. and Acidophilus spp., may be present when comparing the bacterial communities in the rhizosphere and non-rhizosphere soil of R. griseocarnosa [118]. Another analysis of the network structure and interactions within the sporocarp soil of R. griseocarnosa revealed that the genera Bacillus, Burkholderia, and Streptomyces exhibited the highest abundance. Furthermore, numerous effective partnerships and close associations were observed between the genera Bacillus and Burkholderia, suggesting a potential role in promoting the growth of R. griseocarnosa. However, the high-throughput sequencing results indicated a relatively higher abundance only for the genus Burkholderia, while Bacillus did not exhibit a similarly high abundance [130]. Therefore, a combinatorial approach employing traditional pure culture methods and high-throughput sequencing technology can provide a more comprehensive understanding of the rhizosphere microbial diversity associated with R. griseocarnosa. This integrated strategy could unravel the intricate microbial interactions and elucidate their contributions to the growth and development of this economically and ecologically significant mushroom species.
Additionally, applying nitrogen fertilisers and microbial fertilisers containing MHB may promote the protection, reproduction, and sustainable use of R. griseocarnosa. The existing literature in the field has put forward the notion that various interventions, including increasing surface water content, humidity control, raising soil temperature, and winter pruning of mycorrhizal trees, could be implemented in the woodland habitat where R. griseocarnosa grows and could significantly augment mushroom yield [131].
Artificially manipulating the number of basidiospores and the living environment of R. griseocarnosa through the methods described in the above studies may have a positive effect on increasing production. However, it has been difficult to conclusively prove the effectiveness of the process of inoculating ‘cultures’ that have not been accurately identified, in terms of increasing yield. It may also be that the inoculation of MHB into the habitat of R. griseocarnosa could increase production [132], but the mechanisms are not yet clear.

4. Discussion

With its delicious flavour, significant nutrition, and efficacy, R. griseocarnosa is highly sought after by consumers and researchers. However, the fundamental research related to hyphal physiology was relatively backward. Currently, there are still difficulties in the separation and identification of R. griseocarnosa fruiting bodies and strains. The challenge of distinguishing species similar to R. griseocarnosa and the existence of chaotic molecular sequences have led to confusion about the Russula species produced in regions such as Fujian, Guangxi, and Yunnan. The use of molecular identification techniques to verify the identity of the isolated cultures has not been adequately demonstrated in the existing research. While numerous attempts have been made to separate and cultivate strains, the reliability of the so-called “cultures” mentioned in the literature has not been conclusively established through the application of rigorous molecular biological methods. It is widely accepted that achieving a sequence alignment similarity of over 97% is requisite for categorizing specimens within the same species [133,134,135]. However, there is no documented instance where the sequence similarity between the isolated mycelium and the fruiting body of R. griseocarnosa has exceeded 97%. Research efforts aimed at augmenting R. griseocarnosa production through artificial field expansion and other methodologies confront a multitude of variables, rendering them challenging to substantiate through data or effective technical methodologies scientifically and objectively. Leveraging our existing research and integrating recent advancements in ectomycorrhizal fungi studies, plant root-microbe communication, and the application of cutting-edge technology, we have synthesised and speculated upon the molecular ecological interplay among R. griseocarnosa, associated microorganisms, and host plants (see Figure 1), in this process, the application of multi-omics technology should be valued and attempted to make up for the disadvantage of difficulty in isolating the mycelium and/or habitat microorganisms of R. griseocarnosa [136]. We contend that the following vital issues warrant firm attention:
1.
Enhancing the accurate identification of R. griseocarnosa
Traditional mushroom species identification predominantly relies on holotype characteristics, encompassing macroscopic and microscopic features alongside molecular sequence data [137]. The taxonomy of the genus Russula presents significant challenges, particularly in the classification of closely related species to R. griseocarnosa [44,138]. Notably, the taxonomic status of many closely related species remains contentious [45] although phylogenetic trees constructed based on ITS sequences were able to distinguish a few Russula species [139], and this is compounded by the extensive genetic diversity and differentiation within R. griseocarnosa populations [140,141]. In our investigation, we utilised the ITS sequence [17] of the R. griseocarnosa holotype to compare it with recently published genomic data [142,143]. Our analysis revealed a maximum similarity of 94.1%, contrasting with up to 99% similarity observed with our own genomic data of R. griseocarnosa [83]. Given the advancing precision of contemporary sequencing technologies, ensuring accurate identification of sequencing materials is fundamental to research integrity. During our preliminary resource survey, numerous specimens exhibited ITS sequences closely resembling those of R. griseocarnosa. However, discernible disparities in macroscopic morphology persisted, particularly evident in variations in pileus colour and thickness, dried lamellae colour, and fresh fruit body hardness. Consequently, there is an urgent imperative to establish standardised gene barcodes to facilitate accurate and expedient identification of R. griseocarnosa.
2.
Navigating challenges for isolation of R. griseocarnosa culture
Culture isolation of R. griseocarnosa presents significant challenges. As previously noted, achieving pure cultures of this fungus proves arduous. Given the success in obtaining pure cultures of ectomycorrhizal fungi through mycorrhizal separation [144], it merits investigation whether this approach is applicable to R. griseocarnosa. Various media were employed in attempts to isolate R. griseocarnosa strains at different growth stages; however, these efforts yielded no pure cultures. Instead, numerous endophytic fungi were isolated. Further investigation is warranted to ascertain whether these endophytic fungi play a role in the growth and development of R. griseocarnosa. Additionally, whole-genome analysis revealed significant disparities in carbohydrate-related enzymes compared to saprophytic fungi. Nonetheless, it remains inconclusive whether the absence of certain enzyme genes directly hinders growth on artificial media. Transcriptome research may provide complementary insights for verification.
3.
The Symbiotic Interaction between R. griseocarnosa and its host plant
Investigation into the interaction between R. griseocarnosa and its host plant reveals Castanopsis hystrix as the primary host, fostering a mutually beneficial relationship. Analogous to the pivotal role of other ectomycorrhizal fungi within forest ecosystems [145] the formation of mycorrhiza prompts R. griseocarnosa mycelium to release various molecular secretions into the soil. These secretions facilitate the growth of the host plant’s root system and enhance nutrient uptake. Concurrently, they bolster the host plant’s resilience to stress and its survival rate during transplantation [146]. However, the specific substance provided by the host plant to R. griseocarnosa remains undetermined. Whether it pertains to sugars or fatty acids, reminiscent of the metabolic processes of arbuscular mycorrhizal fungi [147], necessitates elucidation through further interaction research.
4.
Clarify the functional interaction of R. griseocarnosa with microorganisms in habitat soil and endophytic fungi in the fruiting body
The study focuses on examining the interaction between R. griseocarnosa and microorganisms present in soil and fruiting bodies. Soil microorganisms, integral to terrestrial ecosystems, play pivotal roles in biogeochemical cycles and exert significant influence across diverse environmental conditions [108]. They also impact the abundance of ectomycorrhizal fungi [113]. Furthermore, eukaryotic organisms, including mushrooms, engage in intricate interactions with microbial communities [148], with specific microbial helper bacteria (MHB) identified in R. griseocarnosa habitats [118]. Nonetheless, the precise mechanism by which these microorganisms promote growth remains unclear. Similarly, akin to the beneficial effects of ectomycorrhizal fungi on plant growth and development, endophytic microorganisms are presumed to positively influence the growth of R. griseocarnosa [149]. However, whether endophytic microorganisms associated with the host of R. griseocarnosa exert similar effects on R. griseocarnosa itself remains uncertain. Furthermore, the function of endophytic microorganisms from R. griseocarnosa remains unexplored. Additionally, investigating potential variations in microbial structures associated with different growth stages of R. griseocarnosa, akin to other ectomycorrhizal edible mushrooms [150], is imperative.
5.
Challenges in the artificial domestication of R. griseocarnosa
Research on the artificial domestication of R. griseocarnosa remains the ultimate goal of many researchers. At present, the cultivation and development of ectomycorrhizal edible mushrooms mainly rely on the introduction of mycorrhizal seedlings to simulate the natural ecological conditions of the mushroom and establish artificially cultivated plantations (forests) to achieve semi-artificial or wild-like cultivation [151,152]. Using this method, various ectomycorrhizal mushrooms have been successfully cultivated. However, there is still controversy over the artificially cultivated Suillus luteus [153] and Phlebopus portentosus [154,155]; after the first report of the former, no follow-up research and progress have been made, while the latter was considered not to be an ectomycorrhizal fungus, with some researchers suggesting it might be a facultative ectomycorrhizal fungus [156]. Controversy also surrounds Morchella spp., as studies have shown that it can form mycorrhiza with plants [157,158,159,160,161], while some cultivated Morchella spp. were considered to be saprophytes [162], a finding supported by the latest research results [163]. Whether there is a saprophytic species in the genus Russula is currently unclear and requires further research through large-scale isolate tests or comparative genomics analysis based on enough Russula species. In addition, research on mycorrhizal seedlings requires continuous efforts, as under the current situation, only by obtaining mycorrhizal seedlings is it possible to induce or promote the formation of fruiting bodies by improving soil biological and abiotic factors and to achieve semi-artificial domestication.

5. Conclusions

R. griseocarnosa was regarded as a rare and precious edible ectomycorrhizal mushroom in southern China, possessing outstanding nutritional value and health benefits due to its rich composition of nutrients and bioactive compounds. It has garnered substantial market demand and has become a significant source of income for local mountain communities. However, the lack of systematic and in-depth research on its symbiotic relationships with host plants and microorganisms in its habitat has hindered successful isolation and artificial cultivation of its mycelium to date. To overcome this challenge, future research should leverage multi-omics technologies, particularly proteomics and metabolomics, to conduct comprehensive investigations into the material basis provided by host plants and microorganisms in the Russula’s habitat. Specifically, studies should focus on elucidating the intricate exchange of carbon sources, signalling molecules, and other key factors that govern the symbiotic associations. By unravelling these intricate mechanisms, researchers could potentially develop interventional strategies to promote and facilitate the artificial cultivation and domestication of this valuable ectomycorrhizal mushroom.
The successful implementation of such interventional approaches would not only enable sustainable development and application of R. griseocarnosa as an ectomycorrhizal edible mushroom resource but also contribute to a deeper understanding of the complex ecological interactions within its natural ecosystem. Moreover, the insights gained from this research could potentially inform sustainable cultivation practices for other ectomycorrhizal mushroom, thereby unlocking their vast potential for diverse applications in agriculture, food production, and biotechnology. In conclusion, by synergistically integrating multi-omics technologies and garnering comprehensive insights into the intricate symbiotic relationships of R. griseocarnosa, researchers are poised to harness the full potential of this valuable ectomycorrhizal mushroom, paving the path for its sustainable cultivation and utilization, while concomitantly advancing the overarching field of mycorrhizal biology and ecology.

Author Contributions

Conceptualization, Methodology, Writing—original draft, Y.L.; Review and editing, T.Y., M.C., X.W., H.G. and Y.X.; Conceptualization, Methodology, Funding acquisition, Review, H.H. and Q.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the National Key R&D Program of China (2023YFF1000801), GDAS’Project of Science and Technology Development (2022GDASZH-2022010101), Guangdong Edible Mushroom (Shaoguan) Seed Industry Innovation Park (2022-440000-43010404-9497).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. Volatile oil components of R. griseocarnosa.
Table A1. Volatile oil components of R. griseocarnosa.
Volatile CompoudsSecondary (CAS)NameFormula
157-10-3Palmitic acidC16H32O2
260-12-82-PhenylethanolC8H10O
31002-43-33-MethylundecaneC12H26
41004-29-12-butyl tetrahydrofuranC8H16O
5100-52-7BenzaldehydeC7H6O
61014-60-4Benzene,1,3-bis(1,1-dimethylethyl)-C14H22
7104-46-1cis-AnetholC10H12O
810482-56-1(-)-α-TerpineolC10H18O
9107-50-6Tetradecamethyl CycloheptasiloxaneC14H42O7Si7
10109-08-0methylpyrazineC5H6N2
11110-43-02-HeptanoneC7H14O
12111150-30-2Pyrazine, 3,5-dimethyl-2-(3-methylbutyl)-(9CI)C11H18N2
13111-71-7HeptanalC7H14O
141120-21-4UndecaneC11H24
15112-12-92-UndecanoneC11H22O
16112-31-2DecanalC10H20O
17112-40-3DodecaneC12H26
181124-11-4TetramethylpyrazineC8H12N2
19112-41-4dodeceneC12H24
20112-44-7UndecanalC11H22O
211125-21-92,6,6-Trimethyl-2-cyclohexene-1,4-dioneC9H12O2
22116-53-02-Methylbutyric acidC5H10O2
23118-65-0isocaryophylleneC15H24
24120-94-51-MethylpyrrolidineC5H11N
25122-78-1PhenylacetaldehydeC8H8O
26123-32-02,5-DimethylpyrazineC6H8N2
27124-13-0OctanalC8H16O
28124-19-6NonanalC9H18O
2913019-16-42-Butyl-2-octenalC12H22O
3013152-44-8ButylcyclobutaneC8H16
3113286-73-23-EthyltridecaneC15H32
3213360-65-12-Ethyl-3,5-dimethylpyrazineC8H12N2
33140-67-0EstragoleC10H12O
34142-50-7Nerolidol, cis-(+)C15H26O
3514309-57-03-Nonen-2-oneC9H16O
361472-09-9octylcyclopropaneC11H22
371502-38-1methylcyclooctaneC9H18
3815870-10-72-Methyl-1-hepteneC8H16
3917301-25-62,8-DimethylundecaneC13H28
4017301-28-9Undecane,3,6-dimethyl-C13H28
4117301-29-0Undecane,3,7-dimethyl-C13H28
4217301-30-33,8-DimethylundecaneC13H28
4317301-32-5Undecane,4,7-dimethyl-C13H28
4417302-28-2NONANE,2,6-DIMETHYL-C11H24
4517312-68-44,4-DimethylundecaneC13H28
4617312-80-02,4-Dimethyl-undecaneC13H28
4717453-93-95-methyldodecaneC13H28
4817615-91-7Undecane,5,6-dimethyl-C13H28
4919132-06-0(+)-2,3-ButanediolC4H10O2
50192823-15-72,3,5,8-tetramethyldecaneC14H30
5119780-34-8Tridecane, 3-methylene-C14H28
5219780-74-65-Ethyl-1-noneneC11H22
532027-47-6octadec-9-enoic acidC18H34O2
542471-84-31H-Indene,1-methilene-C10H8
5525117-31-15-MethyltridecaneC14H30
5625117-33-35-methylpentadecaneC16H34
572801-84-52,4-dimethyldecaneC12H26
582882-96-43-MethylpentadecaneC16H34
59295-17-0cyclotetradecaneC14H28
6031295-56-42,6,11-TrimethyldodecaneC15H32
613391-86-4Oct-1-en-3-olC8H16O
623393-45-15,6-DIHYDRO-2H-PYRAN-2-ONEC5H6O2
633777-69-32-AmylfuranC9H14O
643879-26-3neryl acetoneC13H22O
654126-78-7MethylcycloheptaneC8H16
6641446-67-7(Z)-tetradec-3-eneC14H28
674292-19-71-IodododecaneC12H25I
684411-89-62-phenyl-2-butenalC10H10O
694457-00-5hexylcyclopentaneC11H22
70503-74-23-Methylbutanoic acidC5H10O2
7150656-61-6(3aR,8aS)-2,2,8-trimethyl-3,3a,6,8a-tetrahydro-1H-azulene-5,6-dicarbal dehydeC15H20O2
7251756-29-73-Butyl-3-methylcyclohexanoneC11H20O
7351945-98-31,5-Heptadiene-3,4-diolC7H12O2
74540-97-6DodecamethylcyclohexasiloxaneC12H36O6Si6
75541-02-6DecamethylcyclopentasiloxaneC10H30O5Si5
76541-05-9hexamethylcyclotrisiloxaneC6H18O3Si3
77544-76-3HexadecaneC16H34
78556-67-2OctamethylcyclotetrasiloxaneC8H24O4Si4
79556-68-3hexadecamethylcyclooctasiloxaneC16H48O8Si8
80563-16-63,3-DimethylhexaneC8H18
815876-87-91,11-DodecadieneC12H22
82590-86-3IsovaleraldehydeC5H10O
8361141-72-8dodecane,4,6-dimethylC14H30
8462016-37-92,4,6-trimethyl octaneC11H24
8562108-21-86-ethyl-2-methyl-decaneC13H28
8662108-22-92,5,9-trimethyldecaneC13H28
8762108-23-0Trimethyldecane, 2,5,6-C13H28
88622-39-92-PropylpyridineC8H11N
8962338-50-5(E)-8-Methyl-4-deceneC11H22
90629-50-5TridecaneC13H28
91629-59-4TetradecaneC14H30
926418-41-33-methyltridecaneC14H30
936418-43-53-methylhexadecaneC17H36
9464-19-7acetic acidC2H4O2
9566-25-1HexanalC6H12O
9667-64-1AcetoneC3H6O
976831-17-0aristoloneC9H11N3
98693-54-92-DecanoneC10H20O
9969460-62-4(4aS,8R)-4,4a,5,6,7,8-Hexahydro-4a,8-dimethyl-2(3H)-naphthalenoneC12H18O
10071138-64-2Undecane, 3-methylene-C12H24
1017154-79-22,2,3,3-TetramethylpentaneC9H20
10274630-39-04-Methyl-1-undeceneC12H24
10374645-98-0DODECANE,2,7,10-TRIMETHYL-C15H32
10474663-85-7NonylcyclopropaneC12H24
10574685-36-2Oxacyclotetradecane-2,11-dione, 13 methyl-C14H24O3
1067473-98-52-Hydroxy-2-methyl propiophenoneC10H12O2
10775-50-3TrimethylamineC3H9N
10878-84-2IsobutyraldehydeC4H8O
10979-31-2Isobutyric acidC4H8O2
11079-50-5DL-PantolactoneC6H10O3
11184-69-5Diisobutyl phthalateC16H22O4
11291010-41-22-methyl-6-(3-methyl-butyl)-pyrazineC10H16N2
11391-20-3NaphthaleneC10H8
11496-17-32-MethylbutanalC5H10O
11596-76-42,4-Di-t-butylphenolC14H22O
11698-55-5alpha-TerpineolC10H18O

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Agriculture 14 00879 g001
Figure 1. The challenges and pertinent issues encountered by R. griseocarnosa.
Figure 1. The challenges and pertinent issues encountered by R. griseocarnosa.
Agriculture 14 00879 g001
Table 1. Comparations of fatty acid content of R. griseocarnosa with eggs, chicken, and deep-sea fish oil.
Table 1. Comparations of fatty acid content of R. griseocarnosa with eggs, chicken, and deep-sea fish oil.
Fatty Acids aPileusStipeEggChickenDeep-Sea Fish Oil
C16:019.30 ± 1.1130.87 ± 4.4225.56 ± 1.2029.37 ± 1.5819.10
C16:10.42 ± 0.040.90 ± 0.113.58 ± 0.560.20 ± 0.05c5.68
C16:30.38 ± 0.092.04 ± 0.23---
C18:l47.92 ± 6.4714.20 ± 2.0642.81 ± 1.4719.80 ± 2.3717.18
C18:228.40 ± 5.7950.22 ± 8.0718.79 ± 0.6321.29 ± 1.0511.88
C18:31.02 ± 0.11a1.29 ± 0.160.32 ± 0.300.19 ± 0.104.28
C20:42.55 ± 0.100.48 ± 0.071.87 ± 0.10-2.2
total saturates19.3030.8734.34 ± 1.2055.94 ± 3.85-
total unsaturates80.6969.1315.1 ± 0.7923.34 ± 3.56-
a Values are expressed as percentage of total fatty acids, references for chicken [26], and deep-sea fish oil [27].
Table 2. Chemical composition versus biological activity of Russula species.
Table 2. Chemical composition versus biological activity of Russula species.
CompoundNameStructureBiological ActivityTargetSpeciesSource
1ergosterolAgriculture 14 00879 i001antioxidantDPPHR. griseocarnosa[30]
2β-caroteneAgriculture 14 00879 i002antioxidantDPPHas above[30]
3quercetinAgriculture 14 00879 i003antioxidantDPPHas above[30]
4caffeic acidAgriculture 14 00879 i004antioxidantDPPHas above[30]
5protocatechuicacidAgriculture 14 00879 i005antioxidative, antibacterial, and antimutagenic activitiesDPPHas above[30]
6vinosaneAgriculture 14 00879 i006inhibiting NO production-R. vinosa[47]
7rulepidadione CAgriculture 14 00879 i007--as above[47]
87α,8α,13-trihydroxy-marasm-5-oic acid-lactone Agriculture 14 00879 i008inhibiting NO production-as above[47]
9aristoloneAgriculture 14 00879 i009inhibiting NO production-as above[47]
10(24E)-3,4-seco-cucurbita-4,24-diene-26,29-dioic acid-3-methyl esterAgriculture 14 00879 i010inhibiting NO production-as above[47]
11(24E)-3,4-seco-cucurbita-4,24-diene-26-oic acid-3-ethyl esterAgriculture 14 00879 i011inhibiting NO production-as above[47]
12(24E)-3β-hydroxycucurbita-5,24-diene-26,29-dioic acidAgriculture 14 00879 i012--as above[47]
13(24E)-3,4-secocucurbita-4,24-diene-3,26,29-trioic acidAgriculture 14 00879 i013inhibiting NO production-as above[47]
14(24E)-3,4-secocucurbita-4,24-diene-3,26-dioic acid Agriculture 14 00879 i014--as above[47]
15(24E)-3β-hydroxycucurbita-5,24-diene-26-oic acid Agriculture 14 00879 i015--as above[47]
16rosacea acid BAgriculture 14 00879 i016--as above[47]
17rosacea acid AAgriculture 14 00879 i017--as above[47]
18(2S,3S,4R,20R)-2-(20-hydroxydocosanoylamino)eicosane-1,3,4-triolAgriculture 14 00879 i018--as above[47]
197,8-dimethylalloxazineAgriculture 14 00879 i019--as above[47]
20L-pyroglutamic acidAgriculture 14 00879 i020--as above[47]
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Liu, Y.; Yong, T.; Cai, M.; Wu, X.; Guo, H.; Xie, Y.; Hu, H.; Wu, Q. Exploring the Potential of Russula griseocarnosa: A Molecular Ecology Perspective. Agriculture 2024, 14, 879. https://doi.org/10.3390/agriculture14060879

AMA Style

Liu Y, Yong T, Cai M, Wu X, Guo H, Xie Y, Hu H, Wu Q. Exploring the Potential of Russula griseocarnosa: A Molecular Ecology Perspective. Agriculture. 2024; 14(6):879. https://doi.org/10.3390/agriculture14060879

Chicago/Turabian Style

Liu, Yuanchao, Tianqiao Yong, Manjun Cai, Xiaoxian Wu, Huiyang Guo, Yizhen Xie, Huiping Hu, and Qingping Wu. 2024. "Exploring the Potential of Russula griseocarnosa: A Molecular Ecology Perspective" Agriculture 14, no. 6: 879. https://doi.org/10.3390/agriculture14060879

APA Style

Liu, Y., Yong, T., Cai, M., Wu, X., Guo, H., Xie, Y., Hu, H., & Wu, Q. (2024). Exploring the Potential of Russula griseocarnosa: A Molecular Ecology Perspective. Agriculture, 14(6), 879. https://doi.org/10.3390/agriculture14060879

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