Inherited microbiome engineers: Seed endophytes shape rhizosphere microbiome assembly through host-mediated priority effects

Description

Seeds serve not only as reproductive propagules but also as vehicles for microbial inheritance. Through vertical transmission, seed endophytes colonize emerging seedlings before most environmental microorganisms and may therefore exert priority effects on microbiome assembly. However, whether inherited seed endophytes influence rhizosphere microbiome assembly and the mechanisms remain poorly understood. Here, we used the pioneer metallophyte Desmodium sequax naturally colonizing polymetallic mine tailings in Southwest China as a model system. Revegetation by D. sequax significantly improved soil quality, microbial diversity, and ecosystem multifunctionality. Seed-associated bacterial communities were highly diverse and were largely linked to maternal microbial sources, particularly among abundant taxa, indicating extensive microbial inheritance across generations. A dominant seed endophyte, Pantoea agglomerans D905, was isolated and used to investigate priority effects during microbiome assembly. Early colonization by D905 significantly altered root exudation profiles, resulting in extensive metabolic reprogramming and distinct rhizosphere microbiome assembly trajectories. Rhizosphere microbiomes assembled following D905-mediated priority colonization exhibited greater biomass, altered community structure, and enhanced ecological stability relative to control microbiomes. Importantly, these reassembled microbiomes significantly improved plant growth and reduced cadmium translocation under metal stress. Together, these findings support a mechanistic framework linking seed microbiome inheritance, priority colonization, root exudate reprogramming, and rhizosphere microbiome assembly. Vertically transmitted seed endophytes function as inherited microbial engineers that influence host adaptation indirectly through microbiome assembly and highlight inherited microbial symbionts as potential targets for microbiome- assisted.

Steps to reproduce

Figure 1: Soil physicochemical properties and enzyme activity data were standardized using Z-scores. The average Z-score was then calculated to determine the soil multifunctionality index. Calculate the ratio of the soil multifunctionality index to its standard error to assess the stability of soil multifunctionality. The total metal concentrations in soils were measured using a flame atomic absorption spectrometer (Hitachi, FAAS ZA-3000, Japan). The bioavailability of heavy metals in the soils was evaluated through extraction using a diethylenetriaminepentaacetic acid (DTPA) extraction solution. Figure 5: Plants were grown for 90 days in a greenhouse (natural light, 15–30 °C). At harvest, height and biomass (DW) were recorded. For plant samples, wet digestion was performed using a mixture of HNO3-HClO4 (4: 1, v / v) following the Chinese national standard method (GB/T 3799-2011). The bioavailability of heavy metals in the soils, are referenced in Figure 1. BCF and TF were calculated as: BCF = Croot / Csoil and TF = Cshoot / Croot (Croot, Cshoot, Csoil: total heavy metal concentrations in roots, shoots, and soil). Figure 6: The 16S gene copy numbers of mpRs, opRs, nmRs and Bs were quantified using absolute quantitative real-time PCR. Figure 8: Detection methods for Desmodium sequax plant height, biomass, heavy metal and DTPA-Cd concentrations, as well as BCF and TF, are referenced in Figure 1 and Figure 5. Root parameters (length, average diam, tips, volume, forks, and surface area) were measured with a root scanner (EPSON Perfection V850 Pro, Japan). Figure S2: Detection methods for Desmodium sequax heavy metal and DTPA-Cd concentrations, as well as BCF and TF, are referenced in Figure 1 and Figure 5. Figure S5: Phosphate-solubilizing activity was assessed in PVK medium containing 5 g/L tricalcium phosphate or calcium phytate as the sole phosphorus source after incubation at 30 °C for 2 days. Soluble phosphate concentration was quantified using the molybdenum blue colorimetric method (NY/T 2017-2011) at 700 nm, and culture filtrate pH was recorded. Figure S6: Siderophore production was determined by culturing the strain in iron-deficient MKB liquid medium at 30°C for 2 days, followed by absorbance measurement at 630 nm. Figure S7: Bacterial growth was measured at 630 nm in LB liquid medium with and without 1 mg/L Cd2+ (added as CdCl2·2.5H2O), and the cadmium tolerance index (TI) was calculated. Jasmonic acid (JA) concentration in LB culture supernatants was determined using a competitive enzyme-linked immunosorbent assay (ELISA; Shanghai Youxuan Biotechnology Co., Ltd., China) with absorbance measured at 450 nm.

Institutions

• Yunnan University

  Yunnan, Kunming

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