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Hortic Res
2020 Jan 01;7:144. doi: 10.1038/s41438-020-00365-2.
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Rhizosphere microbial communities associated to rose replant disease: links to plant growth and root metabolites.
Yim B
,
Baumann A
,
Grunewaldt-Stöcker G
,
Liu B
,
Beerhues L
,
Zühlke S
,
Sapp M
,
Nesme J
,
Sørensen SJ
,
Smalla K
,
Winkelmann T
.
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Growth depression of Rosa plants at sites previously used to cultivate the same or closely related species is a typical symptom of rose replant disease (RRD). Currently, limited information is available on the causes and the etiology of RRD compared to apple replant disease (ARD). Thus, this study aimed at analyzing growth characteristics, root morphology, and root metabolites, as well as microbial communities in the rhizosphere of the susceptible rootstock Rosacorymbifera 'Laxa' grown in RRD-affected soil from two sites (Heidgraben and Sangerhausen), either untreated or disinfected by γ-irradiation. In a greenhouse bioassay, plants developed significantly more biomass in the γ-irradiated than in the untreated soils of both sites. Several plant metabolites detected in R. corymbifera 'Laxa' roots were site- and treatment-dependent. Although aloesin was recorded in significantly higher concentrations in untreated than in γ-irradiated soils from Heidgraben, the concentrations of phenylalanine were significantly lower in roots from untreated soil of both sites. Rhizosphere microbial communities of 8-week-old plants were studied by sequencing of 16S rRNA, ITS, and cox gene fragments amplified from total community DNA. Supported by microscopic observations, sequences affiliated to the bacterial genus Streptomyces and the fungal genus Nectria were identified as potential causal agents of RRD in the soils investigated. The relative abundance of oomycetes belonging to the genus Pythiogeton showed a negative correlation to the growth of the plants. Overall, the RRD symptoms, the effects of soil treatments on the composition of the rhizosphere microbial community revealed striking similarities to findings related to ARD.
Fig. 1. Effects of RRD on R. corymbifera ‘Laxa’.Appearance (a) and biomass (b) at the end of the bioassay, i.e., after 8 weeks of growth in soil from Heidgraben (H) and Sangerhausen (S), either untreated (U) or γ-irradiated (G). Data are means ± SD (n = 10 and 5 for shoot and root dry masses, respectively). Letters indicate significant differences between variants within sites (t-test, p < 0.05)
Fig. 2. Symptoms of replant disease in fine roots of R. corymbifera ‘Laxa’.Symptoms were detected after eight weeks of cultivation in RRD soil from the site Heidgraben (H) in whole-mount samples (a–g) and thin sections stained with toluidine blue (f–m). a Healthy fine root with intact root hair zone; b constricted root structure and brown necrotic zones with black cell clusters (arrows) in a toluidine blue-stained root segment; c, d black root tips and clusters (arrows) of necrotic rhizodermal and cortical cells; e fine root with intracellular cauliflower-like (CF) fungal structures (arrows) in necrotic rhizodermal and cortex cells; f CF structures and black cell inclusions (arrows); g green fluorescent Actinobacteria in cortex cells after FUN®1 cell vital staining. h Longitudinal thin section through healthy fine root tissues with rhizodermis R, cortex C, endodermis E, stele St, and xylem X; i cross section of an infected fine root with fungal hyphae and CF structures (arrows) in necrotic cortex cells; j infected fine root with fungal CF structures and hyphae (arrows) in rhizodermal and cortical cells; k thick fungal hyphae, intercellular entry point and developing intracellular CF structure (black arrows) and Actinobacteria (white arrows); l mixed infection with a CF structure-forming fungus (black arrows), rod-shaped bacteria, and thread-like Actinobacteria (white arrows); m cortex cells with fungal CF structures and round-shaped fungal chlamydospores (arrows)
Fig. 3. Concentration (µg g−1 DM) profiles of selected metabolites in roots of R. corymbifera ‘Laxa’.Contents of the secondary metabolites (catechin, epicatechin, gallic acid, phlorizin, hyperoside, aloesin, and quercitrin) and a primary metabolite (phenylalanine) were detected by HPLC-HR-MS and GC-MS (epicatechin and gallic acid). HU and SU, untreated RRD soils from Heidgraben and Sangerhausen, respectively; HG and SG, γ-irradiated RRD soils from Heidgraben and Sangerhausen, respectively. Letters indicate significant differences in the contents of compounds between untreated and γ-irradiated samples within a site, t-test at p < 0.05 and n = 5
Fig. 4. Microbial community compositions in the rhizosphere of R. corymbifera ‘Laxa’ grown for eight weeks in untreated (U) and γ-irradiated (G) RRD soils from two sites (Sangerhausen S and Heidgraben H).Bacterial (a) and fungal (b) community compositions were revealed by principal coordinate analysis (PCoA) using Bray–Curtis distance metric, based on operational taxonomic units (OTUs). Past3, n = 4 and 5 for sites H and S, respectively, for a and n = 4 for b, except for SU with n = 5
Fig. 5. Dominant microbial phyla in the rhizosphere of R. corymbifera ‘Laxa’ grown for eight weeks in untreated (U) and γ-irradiated (G) RRD soils from two sites (H and S).The relative abundance of dominant bacterial (a) and fungal (b) phyla (>1%) is indicated. Letters indicate significant differences between treatments within a site and phylum, t-test, p < 0.05 and n = 4 and 5 for sites H (Heidgraben) and S (Sangerhausen), respectively (a), n = 4, except for SU with n = 5 (b)
Fig. 6. Effects of soil treatments on relative abundance of bacteria at the genus level (>0.5%) in the rhizosphere of R. corymbifera ‘Laxa’.Plants were grown for eight weeks in untreated (U) and γ-irradiated (G) RRD soils from two sites (S and H). Asterisks (*) in red and green color indicate significantly decreased and increased relative abundances of bacteria, respectively, in γ-irradiated compared to untreated RRD soils at both sites (H and S). T-test at p < 0.05, n = 4 and 5 for sites H (Heidgraben) and S (Sangerhausen), respectively. OTU, operational taxonomic unit. The relative abundance of the respective taxon below detection limit is indicated in black color
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