Multifeature analysis of age‐related microbiome structures reveals defense mechanisms of <i>Populus tomentosa</i> trees

Xie, Jianbo; Ma, Yue; Li, Xian; Wu, Jiadong; Martin, Francis; Zhang, Deqiang

doi:10.1111/nph.18847

Cited by 15 publications

(19 citation statements)

References 72 publications

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“…We noticed that several plant growth-promoting rhizobacterias (PGPRs) such as Actinobacteriota and Tumebacillus were highly abundant in the Turanga. These microbes have been reported to be associated with plant growth and stress responses 3,30,31 . The PGPR Bacillus, known for promoting plant growth through the production of hormone and nitrogen fixation, was found to be enriched in Aigeiros 32 .…”

Section: Taxonomic Features Of the Rhizosphere Microbial Composition ...mentioning

confidence: 99%

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Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and lateral root growth in Populus

Xie,

Zhang,

et al. 2024

Preprint

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Plant growth behavior is a function of genetic network architecture. The importance of root microbiome variation driving plant functional traits is increasingly recognized, but the genetic mechanisms governing this variation are less studied. Here, we collected roots and rhizosphere soils from nine Populus species belonging to four sections, generated metabolite and transcription data for roots and microbiota data for rhizospheres, and conducted comprehensive multi-omics analyses. We demonstrated that the roots of robust Leuce poplar enriched more plant growth-promoting rhizobacteria, which compared with the poorly performing poplar, agreeing with the ‘Matthew effect’ on poplar-microbe interaction. Moreover, we confirmed that Pseudomonas was strongly associated with tricin and apigenin biosynthesis and identified that gene GL3 was critical for tricin secretion. The elevated tricin secretion via constitutive transcription of PopGL3 and PopCHS4 could drive Pseudomonas colonization in the rhizosphere and further enhance poplar growth, nitrogen acquisition, and lateral root development in nitrogen-poor soil. This study reveals plant-metabolite-microbe regulation patterns contribute to the poplar fitness and thoroughly decoded the key regulatory mechanisms of tricin, and provided new insights into the interactions of the plant’s key metabolites with its transcriptome, rhizosphere microbes.

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Section: Taxonomic Features Of the Rhizosphere Microbial Composition ...mentioning

confidence: 99%

“…Rhizosphere microbial community structure is highly dynamic in part due to the changes in root exudation over the course of plant development [1][2][3][4] . Although some chemical signals released by plants facilitate specific interactions, many have been recognized by previous studies.…”

Section: Introductionmentioning

confidence: 99%

Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and lateral root growth in Populus

Xie,

Zhang,

et al. 2024

Preprint

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“…For instance, the composition of rhizosphere bacterial and fungal communities was influenced by the age of plant cultivation, a phenomenon documented in a limited number of cultivated crops such as mulberry, rice, and ginseng (Liu et al, 2016; Xiao et al, 2016; Tong et al, 2021). A recent study by Xie et al (2023) found that age‐related microbiome structures are related to the defence mechanisms of Populus tomentosa trees. Continuous cultivation of American ginseng ( Panax quinquefolius ) resulted in decreased bacterial diversity and increased fungal diversity in the soils compared to those used for traditional crops (Dong et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

Ancient bayberry increased stress resistance by enriching tissue‐specific microbiome and metabolites

Li,

Wang,

Ren

et al. 2024

Physiologia Plantarum

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The ancient bayberry demonstrates superior resistance to both biotic and abiotic stresses compared to cultivated bayberry, yet the underlying mechanisms remain largely unexplored. This study investigates whether long‐term bayberry cultivation enhances stress resistance through modulation of tissue‐specific microbes and metabolites. Employing microbiome amplicon sequencing alongside untargeted mass spectrometry analysis, we scrutinize the role of endosphere and rhizosphere microbial communities and metabolites in shaping the differential resistance observed between ancient and cultivated bayberry trees. Our findings highlight the presence of core microbiome and metabolites across various bayberry tissues, suggesting that the heightened resistance of ancient bayberry may stem from alterations in rhizosphere and endosphere microbial communities and secondary metabolites. Specifically, enrichment of Bacillus in roots and stems, Pseudomonas in leaves, and Mortierella in rhizosphere soil of ancient bayberry was noted. Furthermore, correlation analysis underscores the significance of enriched microbial species in enhancing ancient bayberry's resistance to stresses, with elevated levels of resistance‐associated metabolites such as beta‐myrcene, benzothiazole, L‐glutamic acid, and gamma‐aminobutyric acid identified through GC–MS metabolomics analysis. The beneficial role of these resistance‐associated metabolites was further elucidated through assessment of their promotive and allelopathic effects, as well as their phytostatic and antioxidant functions in lettuce plants. Ultimately, our study delves into the intrinsic reasons behind the greater resistance of ancient bayberry to biotic and abiotic stresses by evaluating the impact of long‐term planting on the microbial community and metabolites in the bayberry endosphere and rhizosphere, shedding light on the complex dynamics of host‐microbial interactions.

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“…Although trees are long-lived perennials whose microbiota evolves over the course of their lives and the stage of forest cover (Xie et al, 2023), the initial assembly of the microbiota is thought to influence plant health and physiology (De Zelicourt et al, 2013; Dove et al, 2021; Mangeot-Peter et al, 2020). Previous studies have demonstrated that the microbiota of belowground and aboveground tissues of poplars ( Populus sp.)…”

Section: Introductionmentioning

confidence: 99%

Microbe tree metabolite interactions in the soil - phyllosphere continuum of poplar tree: when microbes rewire poplar root exudate and metabolome

Fracchia,

Guinet,

Engle

et al. 2024

Preprint

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Trees are associated with a broad range of microorganisms colonising the diverse tissues of their host. However, the early dynamics of the assembly of the microbiota from the root to shoot axis and how it is linked to root exudates and metabolite contents of tissues remain unclear. Here, we characterized how fungal and bacterial communities are altering root exudates as well as root and shoot metabolomes in parallel with their establishment in poplar cuttings (Populus tremula x tremuloides clone T89) over 30 days of growth. Sterile poplar cuttings were planted in natural or gamma-irradiated soils. Bulk and rhizospheric soils, root and shoot tissues were collected from day 1 to day 30 to track the dynamic changes of fungal and bacterial communities in the different habitats by DNA metabarcoding. Root exudates and root and shoot metabolites were analysed in parallel by gas chromatography-mass spectrometry. Our study reveals that microbial colonization triggered rapid and substantial alterations in both the composition and quantity of root exudates, with over 70 metabolites exclusively identified in remarkably high abundances in the 32 absence of microorganisms. Noteworthy among these were lipid-related 33 metabolites and defence compounds. The microbial colonization of both roots and shoots exhibited a similar dynamic response, initially involving saprophytic microorganisms and later transitioning to endophytes and symbionts. Key constituents of the shoot microbiota were also discernible at earlier time points in the rhizosphere and roots, indicating that the soil constituted a primary source for shoot microbiota. Furthermore, the microbial colonization of belowground and aerial compartments induced a reconfiguration of plant metabolism. Specifically, microbial colonization predominantly instigated alterations in primary metabolism in roots, while in shoots, it primarily influenced defence metabolism. This highlighted the profound impact of microbial interactions on metabolic pathways of plants, shedding light on the intricate interplay between plants and their associated microbial communities.

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Multifeature analysis of age‐related microbiome structures reveals defense mechanisms of Populus tomentosa trees

Cited by 15 publications

References 72 publications

Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and lateral root growth in Populus

Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and lateral root growth in Populus

Ancient bayberry increased stress resistance by enriching tissue‐specific microbiome and metabolites

Microbe tree metabolite interactions in the soil - phyllosphere continuum of poplar tree: when microbes rewire poplar root exudate and metabolome

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