The biomechanical and ecophysiological properties of plant seed/fruit structures are fundamental to survival in distinct environments. Dispersal of fruits with hard pericarps (fruit coats) encasing seeds has evolved many times independently within taxa that have seed dispersal as their default strategy. The mechanisms by which the constraint of a hard pericarp determines germination timing in response to the environment are currently unknown. Here, we show that the hard pericarp of Lepidium didymum controls germination solely by a biomechanical mechanism. Mechanical dormancy is conferred by preventing full phase-II water uptake of the encased non-dormant seed. The lignified endocarp has biomechanically and morphologically distinct regions that serve as predetermined breaking zones. This pericarp-imposed mechanical dormancy is released by the activity of common fungi, which weaken these zones by degrading non-lignified pericarp cells. We propose that the hard pericarp with this biomechanical mechanism contributed to the global distribution of this species in distinct environments.

 Nutrient imbalances cause the deterioration of tree health in European forests, but the underlying physiological mechanisms are unknown. Here, we investigated the consequences of decreasing root carbohydrate reserves for phosphorus (P) mobilization and uptake by forest trees.  In P-rich and P-poor beech (Fagus sylvatica) forests, naturally grown, young trees were girdled and used to determine root, ectomycorrhizal and microbial activities related to P mobilization in the organic layer and mineral topsoil in comparison with those in nongirdled trees.  After girdling, root carbohydrate reserves decreased. Root phosphoenolpyruvate carboxylase activities linking carbon and P metabolism increased. Root and ectomycorrhizal phosphatase activities and the abundances of bacterial genes catalysing major steps in P turnover increased, but soil enzymes involved in P mobilization were unaffected. The physiological responses to girdling were stronger in P-poor than in P-rich forests. P uptake was decreased after girdling. The soluble and total P concentrations in roots were stable, but fine root biomass declined after girdling.  Our results support that carbohydrate depletion results in reduced P uptake, enhanced internal P remobilization and root biomass trade-off to compensate for the P shortage. Since reductions in root biomass render trees more susceptible to drought, our results link tree deterioration with disturbances in the P supply as a consequence of decreased belowground carbohydrate allocation.

Phosphorus (P) availability shows large differences among different soil types, affecting P nutrition of forest trees. Chemical binding of P to soil moieties affects partitioning of P between soil particles and solution, influencing soluble P concentrations upon which plants, their associated mycorrhizal symbionts, and microbes feed. The goal of this study was to characterize root P uptake by mycorrhizal and non-mycorrhizal root tips in competition with microbes in situ in the organic and mineral layer of a P-rich and a P-poor forest. We used intact soil cores (0.2 m depth) from beech (Fagus sylvatica) forests to tracing the fate of 33 P in soil, plant and microbial fractions. We used the dilution of 33 P in the rhizosphere of each soil layer to estimate the enrichment with new P in mycorrhizal and non-mycorrhizal root tips and root P uptake. In soil cores from P-rich conditions, 25 and 75% of root P uptake occurred in the organic and mineral layer, respectively, whereas in the P-poor forest, 60% occurred in the organic and 40% in the mineral layer. Mycorrhizal P efficiency, determined as enrichment of new P in mycorrhizal root tips, differed between soil layers. Root P uptake was correlated with mycorrhizal P efficiency and root tip abundance but not with root tip abundance as a single factor. This finding underpins the importance of the regulation of mycorrhizal P acquisition for root P supply. The composition of mycorrhizal assemblages differed between forests but not between soil layers. Therefore, differences in P efficiencies resulted from physiological adjustments of the symbionts. Non-mycorrhizal root tips were rare and exhibited lower enrichment with new P than mycorrhizal root tips. Their contribution to root P supply was negligible. Microbes were strong competitors for P in P-poor but not in P-rich soil. Understory roots were present in the P-rich soil but did not compete for P. Our results uncover regulation of mycorrhizal P efficiencies and highlight the complexity of biotic and abiotic factors that govern P supply to trees in forest ecosystems.

N and P are essential macronutrients for all organisms. How shifts in the availability of N or P affect fungal communities in temperate forests is not well understood. Here, we conducted a factorial P × N fertilization experiment to disentangle the effects of nutrient availability on soil-residing, root-associated, and ectomycorrhizal fungi in beech (Fagus sylvatica) forests differing in P availability. We tested the hypotheses that in P-poor forests, P fertilization leads to enhanced fungal diversity in soil and roots, resulting in enhanced P nutrition of beech, and that N fertilization aggravates P shortages, shifting the fungal communities toward nitrophilic species. In response to fertilizer treatments (1 × 50 kg ha−1 P and 5 × 30 kg ha−1 N within 2 years), the labile P fractions increased in soil and roots, regardless of plant-available P in soil. Root total P decreased in response to N fertilization and root total P increased in response to P addition at the low P site. Ectomycorrhizal species richness was unaffected by fertilizer treatments, but the relative abundances of ectomycorrhizal fungi increased in response to P or N addition. At the taxon level, fungal assemblages were unaffected by fertilizer treatments, but at the order level, different response patterns for saprotrophic fungi among soil and ectomycorrhizal fungi on roots were found. Boletales increased in response to P, and Russulales decreased under N + P addition. Our results suggest that trait conservatism in related species afforded resistance of the resident mycobiome composition to nutritional imbalances.

Phosphorus (P) solubilization is an important process for P acquisition by plants and soil microbes in most temperate forests. The abundance of inorganic P solubilizing bacteria (PSB) is affected by the P concentration in the soil and the carbon input by plants. We used a girdling approach to investigate the interplay of root-derived C and initial P content on the community composition of gcd-harboring bacteria as an example of PSB, which produce gluconic acid. We hypothesized that gcd-harboring PSB communities from P-poor sites are more vulnerable to girdling, because of their lower diversity, and that a shift in gcd-harboring PSB communities by girdling is caused by a response of few, mostly oligotrophic, taxa. We used a high-throughput metabarcoding approach targeting the gcd gene, which codes for the quinoprotein glucose dehydrogenase, an enzyme involved in the solubilization of inorganic P. We compared the diversity of gcd-harboring PSB in the mineral topsoil from two temperate beech forests with contrasting P stocks, where girdling was applied and compared our data to the respective control plots with untreated young beech trees. At both sites, gcd-harboring PSB were dominated by Proteobacteria and Acidobacteria, however, with differences in relative abundance pattern on the higher phylogenetic levels. The P-poor site was characterized by a high relative abundance of Kaistia, whereas at the P-rich site, Dongia dominated the gcd-harboring bacterial communities. Girdling induced an increase in the relative abundance of Kaistia at the P-poor site, whereas other bacterial groups of the family Rhizobiaceae were reduced. At the P-rich site, major microbial responders differed between treatments and mostly Bradyrhizobium and Burkholderia were positively affected by girdling in contrast to uncultured Acidobacteria, where reduced relative abundance was found. Overall, these effects were consistent at different time points analyzed after the introduction of girdling. Our data demonstrate that plant-derived carbon influences community structure of gcd-harboring bacteria in temperate beech forest soils.