Soil chemistry, metabarcoding, and metabolome analyses reveal that a sugarcane—Dictyophora indusiata intercropping system can enhance soil health by reducing soil nitrogen loss
Abstract:IntroductionGreater amounts of fertilizer are applied every year to meet the growing demand for food. Sugarcane is one of the important food sources for human beings.MethodsHere, we evaluated the effects of a sugarcane—Dictyophora indusiata (DI) intercropping system on soil health by conducting an experiment with three different treatments: (1) bagasse application (BAS process), (2) bagasse + DI (DIS process), and (3) the control (CK). We then analyzed soil chemistry, the diversity of soil bacteria and fungi, … Show more
“…Interestingly, in the sugarcane root of DI, the Bacillus genus was associated with the same abundance as D. indusiata (Phallaceae) ( Figures 3E, F ). Interestingly, based on my preliminary research, it was also found that the DI treatment has the ability to reduce soil fungal diversity, which aligns with the observed decreasing trend in endophytic fungal diversity in this study ( Duan et al., 2023a ). This indicates that the cultivation of D. indusiata may invasive and symbiotic growth with sugarcane root, which in turn may regulate the metabolism of sugarcane roots and ultimately impact sugarcane growth.…”
Section: Discussionsupporting
confidence: 88%
“…In this study’s intercropping system, D. indusiata significantly improved the metabolism of sugarcane roots through root symbiosis. Studies have found that the D. indusiata fruiting bodies synthesize IAA ( Duan et al., 2023b ), and D. indusiata improves soil metabolism, accumulating carbohydrate metabolites ( Duan et al., 2023a ). These earlier reports suggested that D. indusiata promotes plant growth metabolism.…”
Section: Discussionmentioning
confidence: 99%
“…Therefore, we conducted an experiment intercropping sugarcane and D. indusiata from March to October 2022. The studies have reported that the intercropping system, D. indusiata and sugarcane, enhances soil chemical properties and activates soil metabolism ( Duan et al., 2023a ); Additionally, the same genomic and metabolomic study revealed that the fruiting body of D. indusiata could synthesize IAA (indole-3-acetic acid) ( Duan et al., 2023b ), which probably leads to improved soil fertility and sugarcane yield. These preliminary studies suggest that intercropping D. indusiata with sugarcane benefits both species.…”
IntroductionEndophytes play a significant role in regulating plant root development and facilitating nutrient solubilization and transportation. This association could improve plant growth. The present study has uncovered a distinct phenotype, which we refer to as "white root", arising from the intricate interactions between endophytic fungi and bacteria with the roots in a sugarcane and bamboo fungus (Dictyophora indusiata) intercropping system.MethodsWe investigated the mechanisms underlying the formation of this “white root” phenotype and its impact on sugarcane yield and metabolism by metabarcoding and metabolome analysis.Results and DiscussionInitial analysis revealed that intercropping with D. indusiata increased sugarcane yield by enhancing the number of viable tillers compared with bagasse and no input control. Metabarcoding based on second-generation and third-generation sequencing indicated that D. indusiate and Bacillus aryabhattai dominates the fungal and bacterial composition in the “white root” phenotype of sugarcane root. The coexistence of D. indusiata and B. aryabhattai as endophytes induced plant growth-promoting metabolites in the sugarcane root system, such as lysoPC 18:1 and dihydrobenzofuran, probably contributing to increased sugarcane yield. Furthermore, the association also enhanced the metabolism of compounds, such as naringenin-7-O-glucoside (Prunin), naringenin-7-O-neohesperidoside (Naringin)*, hesperetin-7-O-neohesperidoside (Neohesperidin), epicatechin, and aromadendrin (Dihydrokaempferol), involved in flavonoid metabolism during the formation of the endophytic phenotype in the sugarcane root system. These observations suggest that the “white root” phenotype promotes sugarcane growth by activating flavonoid metabolism. This study reports an interesting phenomenon where D. indusiata, coordinate with the specific bacteria invade, forms a “white root” phenotype with sugarcane root. The study also provides new insights into using D. indusiata as a soil inoculant for promoting sugarcane growth and proposes a new approach for improve sugarcane cultivation.
“…Interestingly, in the sugarcane root of DI, the Bacillus genus was associated with the same abundance as D. indusiata (Phallaceae) ( Figures 3E, F ). Interestingly, based on my preliminary research, it was also found that the DI treatment has the ability to reduce soil fungal diversity, which aligns with the observed decreasing trend in endophytic fungal diversity in this study ( Duan et al., 2023a ). This indicates that the cultivation of D. indusiata may invasive and symbiotic growth with sugarcane root, which in turn may regulate the metabolism of sugarcane roots and ultimately impact sugarcane growth.…”
Section: Discussionsupporting
confidence: 88%
“…In this study’s intercropping system, D. indusiata significantly improved the metabolism of sugarcane roots through root symbiosis. Studies have found that the D. indusiata fruiting bodies synthesize IAA ( Duan et al., 2023b ), and D. indusiata improves soil metabolism, accumulating carbohydrate metabolites ( Duan et al., 2023a ). These earlier reports suggested that D. indusiata promotes plant growth metabolism.…”
Section: Discussionmentioning
confidence: 99%
“…Therefore, we conducted an experiment intercropping sugarcane and D. indusiata from March to October 2022. The studies have reported that the intercropping system, D. indusiata and sugarcane, enhances soil chemical properties and activates soil metabolism ( Duan et al., 2023a ); Additionally, the same genomic and metabolomic study revealed that the fruiting body of D. indusiata could synthesize IAA (indole-3-acetic acid) ( Duan et al., 2023b ), which probably leads to improved soil fertility and sugarcane yield. These preliminary studies suggest that intercropping D. indusiata with sugarcane benefits both species.…”
IntroductionEndophytes play a significant role in regulating plant root development and facilitating nutrient solubilization and transportation. This association could improve plant growth. The present study has uncovered a distinct phenotype, which we refer to as "white root", arising from the intricate interactions between endophytic fungi and bacteria with the roots in a sugarcane and bamboo fungus (Dictyophora indusiata) intercropping system.MethodsWe investigated the mechanisms underlying the formation of this “white root” phenotype and its impact on sugarcane yield and metabolism by metabarcoding and metabolome analysis.Results and DiscussionInitial analysis revealed that intercropping with D. indusiata increased sugarcane yield by enhancing the number of viable tillers compared with bagasse and no input control. Metabarcoding based on second-generation and third-generation sequencing indicated that D. indusiate and Bacillus aryabhattai dominates the fungal and bacterial composition in the “white root” phenotype of sugarcane root. The coexistence of D. indusiata and B. aryabhattai as endophytes induced plant growth-promoting metabolites in the sugarcane root system, such as lysoPC 18:1 and dihydrobenzofuran, probably contributing to increased sugarcane yield. Furthermore, the association also enhanced the metabolism of compounds, such as naringenin-7-O-glucoside (Prunin), naringenin-7-O-neohesperidoside (Naringin)*, hesperetin-7-O-neohesperidoside (Neohesperidin), epicatechin, and aromadendrin (Dihydrokaempferol), involved in flavonoid metabolism during the formation of the endophytic phenotype in the sugarcane root system. These observations suggest that the “white root” phenotype promotes sugarcane growth by activating flavonoid metabolism. This study reports an interesting phenomenon where D. indusiata, coordinate with the specific bacteria invade, forms a “white root” phenotype with sugarcane root. The study also provides new insights into using D. indusiata as a soil inoculant for promoting sugarcane growth and proposes a new approach for improve sugarcane cultivation.
“…Soil non-targeted metabolomics can be used to characterize the differential activity of microbial communities ( Abram, 2015 ) and reflect the interaction between the microbial genome and the environment ( Tang, 2011 ), providing a novel approach for assessing soil health. For example, alterations in soil carbohydrate metabolite abundance are influenced by factors such as soil organic matter content and microbial activity ( Duan et al, 2023 ). Therefore, soil metabolomics is valuable for assessing the impact on soil quality and microbial function ( Withers et al, 2020 ).…”
It is of utmost importance to understand the characteristics and regulatory mechanisms of soil in order to optimize soil management and enhance crop yield. Poly-γ-glutamic acid (γ-PGA), a stress-resistant amino acid polymer, plays a crucial role in plant drought stress resistance. However, little is known about the effects of γ-PGA on soil characteristics during drought treatments. In this study, the effects of different forms of γ-PGA on soil texture and basic physical and chemical properties under short-term drought conditions were investigated. Furthermore, the impact of γ-PGA on the microbial community and metabolic function of maize was analyzed. Under drought conditions, the introduction of γ-PGA into the soil resulted in notable improvements in the mechanical composition ratio and infiltration capacity of the soil. Concurrently, this led to a reduction in soil bulk density and improved soil organic matter content and fertility. Additionally, metagenomic analysis revealed that under drought conditions, the incorporation of γ-PGA into the soil enhanced the soil microbiota structure. This shift led to the predominance of bacteria that are crucial for carbon, nitrogen, and phosphorus cycles in the soil. Metabolomics analysis revealed that under drought treatment, γ-PGA affected soil metabolic patterns, with a particular focus on alterations in amino acid and vitamin metabolism pathways. Correlation analysis between the soil metagenome and metabolites showed that microorganisms played a significant role in metabolite accumulation. These results demonstrated that γ-PGA could improve soil characteristics under drought conditions and play an important role in soil microorganisms and microbial metabolism, providing further insights into the changes in soil characteristics under drought conditions.
“…For example, the growth of Leucocalocybe mongolica mycelium in soil in a fairy ring ecosystem has been shown to increase soil nutrient abundance ( Duan et al, 2022a ); this can in turn enhance plant growth, increase the abundance of flavonoid metabolites, and promote hormone synthesis ( Duan et al, 2022b ). The cultivation of Dictyophora indusiata inhibits the activity of soil urease, which reduces the environmental loss of soil N ( Duan et al, 2023a ). Therefore, the cultivation of macrofungi (mushrooms) has a major effect on soil ecology.…”
The properties of paddy field (DT) and dry land (HD) soil and food production can be enhanced by the cultivation of Morchella esculenta (ME) during the fallow period. However, whether ME cultivation affects the soil health and microbial diversity of paddy fields and drylands during the cultivation period remains unclear, and this has greatly limited the wider use of this cultivation model. Here, we analyzed the soil chemical properties and bacterial diversity (via metabarcoding sequencing) of DT and HD soils following ME cultivation. Our findings indicated that ME cultivation could enhance soil health. The content of soil phosphorus and potassium (K) was increased in DT soil under ME cultivation, and the K content was significantly higher in HD soil than in DT soil under ME cultivation. ME cultivation had a weak effect on alpha diversity, and ME cultivation affected the abundance of some genera of soil bacteria. The cultivation of ME might reduce the methane production capacity of DT soil and enhance the nitrogen cycling process of HD soil based on the results of functional annotation analysis. Network analysis and correlation analysis showed that Gemmatimonas, Bryobacter, and Anaeromyxobacter were the key bacterial genera regulating soil chemical properties in DT soil under ME cultivation, and Bryobacter, Bacillus, Streptomyces, and Paenarthrobacter were the key taxa associated with the accumulation of K in HD soil. The results of our study will aid future efforts to further improve this cultivation model.
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