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We reviewed the impact of fungal volatile organic compounds (VOCs) on soil-inhabiting organisms and their physiological and molecular consequences for their targets. Because fungi can only move by growth to distinct directions, a main mechanism to protect themselves from enemies or to manipulate their surroundings is the secretion of exudates or VOCs. The importance of VOCs in this regard has been significantly underestimated. VOCs not only can be means of communication, but also signals that are able to specifically manipulate the recipient. VOCs can reprogram root architecture of symbiotic partner plants or increase plant growth leading to enlarged colonization surfaces. VOCs are also able to enhance plant resistance against pathogens by activating phytohormone-dependent signaling pathways. In some cases, they were phytotoxic. Because the response was specific to distinct species, fungal VOCs may contribute to regulate the competition of plant communities. Additionally, VOCs are used by the producing fungus to attack rivaling fungi or bacteria, thereby protecting the emitter or its nutrient sources. In addition, animals, like springtails, nematodes, and earthworms, which are important components of the soil food web, respond to fungal VOCs. Some VOCs are effective repellents for nematodes and, therefore, have applications as biocontrol agents. In conclusion, this review shows that fungal VOCs have a huge impact on soil fauna and flora, but the underlying mechanisms, how VOCs are perceived by the recipients, how they manipulate their targets and the resulting ecological consequences of VOCs in inter-kingdom signaling is only partly understood. These knowledge gaps are left to be filled by future studies.

Mycorrhizal fungi have a key role in nitrogen (N) cycling, particularly in boreal and temperate ecosystems. However, the significance of ectomycorrhizal fungal (EMF) diversity for this important ecosystem function is unknown. Here, EMF taxon-specific N uptake was analyzed via 15 N isotope enrichment in complex root-associated assemblages and non-mycorrhizal root tips in controlled experiments. Specific 15 N enrichment in ectomycorrhizas, which represents the N influx and export, as well as the exchange of 15 N with the N pool of the root tip, was dependent on the fungal identity. Light or water deprivation revealed interspecific response diversity for N uptake. Partial taxon-specific N fluxes for ectomycorrhizas were assessed, and the benefits of EMF assemblages for plant N nutrition were estimated. We demonstrated that ectomycorrhizal assemblages provide advantages for inorganic N uptake compared with non-mycorrhizal roots under environmental constraints but not for unstressed plants. These benefits were realized via stress activation of distinct EMF taxa, which suggests significant functional diversity within EMF assemblages. We developed and validated a model that predicts net N flux into the plant based on taxon-specific 15 N enrichment in ectomycorrhizal root tips. These results open a new avenue to characterize the functional traits of EMF taxa in complex communities.

Climatic stresses limit plant growth and productivity. In the past decade, tree improvement programs were mainly focused on yield but it is obvious that enhanced stress resistance is also required. In this review we highlight important drought avoidance and tolerance mechanisms in forest trees. Genomes of economically important trees species with divergent resistance mechanisms can now be exploited to uncover the mechanistic basis of long-term drought adaptation at the whole plant level. Molecular tree physiology indicates that osmotic adjustment, antioxidative defense and increased water use efficiency are important targets for enhanced drought tolerance at the cellular and tissue level. Recent biotechnological approaches focused on overexpression of genes involved in stress sensing and signaling, such as the abscisic acid core pathway, and down-stream transcription factors. By this strategy, a suite of defense systems was recruited, generally enhancing drought and salt stress tolerance under laboratory conditions. However, field studies are still scarce. Under field conditions trees are exposed to combinations of stresses that vary in duration and magnitude. Variable stresses may overrule the positive effect achieved by engineering an individual defense pathway. To assess the usability of distinct modifications, large-scale experimental field studies in different environments are necessary. To optimize the balance between growth and defense, the use of stress-inducible promoters may be useful. Future improvement programs for drought resistance will benefit from a better understanding of the intricate networks that ameliorate molecular and ecological traits of forest trees.

Increasing salinity is one of the major drawbacks for plant growth. Besides the ion itself being toxic to plant cells, it greatly interferes with the supply of other macronutrients like potassium, calcium and magnesium. However, little is known about how sodium affects the translocation of these nutrients from the root to the shoot. The major driving force of this translocation process is thought to be the water flow through the xylem driven by transpiration. To dissect the effects of transpiration from those of salinity we compared salt stressed, ABA treated and combined salt- and ABA treated poplars with untreated controls. Salinity reduced the root content of major nutrients like K + , Ca 2+ and Mg 2+ . Less Ca 2+ and Mg 2+ in the roots resulted in reduced leaf Ca 2+ and leaf Mg 2+ levels due to reduced stomatal conductance and reduced transpiration. Interestingly, leaf K + levels were positively affected in leaves under salt stress although there was less K + in the roots under salt. In response to ABA, transpiration was also decreased and Mg 2+ and Ca 2+ levels decreased comparably to the salt stress treatment, while K + levels were not affected. Thus, our results suggest that loading and retention of leaf K + is enhanced under salt stress compared to merely transpiration driven cation supply.

Background Phosphorus (P) is a major plant nutrient. It is transported into and allocated inside plants by four families of phosphate transporters (PHT1 to PHT4) with high or low affinity to phosphate. Here, we studied whole-plant P uptake kinetics and expression profiles of members of the PHT families under high, intermediate and low P availability in the woody crop poplar ( Populus  ×  canescens ) in relation to plant performance. Results Poplars exhibited strong growth reduction and increased P use efficiency in response to lower P availabilities. The relative P uptake rate increased with intermediate and decreased with low P availability. This decrease was not energy-limited because glucose addition could not rescue the uptake. The maximum P uptake rate was more than 13-times higher in P-starved than in well-supplied poplars. The K m for whole-root uptake ranged between 26 μM and 20 μM in poplars with intermediate and low P availability, respectively. In well-supplied plants, only low uptake rate was found. The minimum concentration for net P uptake from the nutrient solution was 1.1 μM. All PHT1 members studied showed significant up-regulation upon P starvation and were higher expressed in roots than leaves, with the exception of PtPHT1;3. PtPHT1;1 and PtPHT1;2 showed root- and P starvation-specific expression. Various members of the PHT2, PHT3 and PHT4 families showed higher expression in leaves than in roots, but were unresponsive to P deprivation. Other members ( PtPHT3;1 , PtPHT3;2 , PtPHT3;6 , PtPHT4;6 to PtPHT4;8 ) exhibited higher expression in roots than in leaves and were in most cases up-regulated in response to P deficiency. Conclusions Expression profiles of distinct members of the PHT families, especially those of PHT1 were linked with changes in P uptake and allocation at whole-plant level. The regulation was tissue-specific with lower P responsiveness in leaves than in roots. Uptake efficiency for P increased with decreasing P availability, but could not overcome a threshold of about 1 μM P in the nutrient solution. Because the P concentrations in soil solutions are generally in the lower micro-molar range, even below the apparent K m -values, our findings suggest that bare-rooted poplars are prone to suffer from P limitations in most environments.

Ectomycorrhizal fungi (EMF) grow as saprotrophs in soil and interact with plants, forming mutualistic associations with roots of many economically and ecologically important forest tree genera. EMF ensheath the root tips and produce an extensive extramatrical mycelium for nutrient uptake from the soil. In contrast to other mycorrhizal fungal symbioses, EMF do not invade plant cells but form an interface for nutrient exchange adjacent to the cortex cells. The interaction of roots and EMF affects host stress resistance but uncovering the underlying molecular mechanisms is an emerging topic. Here, we focused on local and systemic effects of EMF modulating defenses against insects or pathogens in aboveground tissues in comparison with arbuscular mycorrhizal induced systemic resistance. Molecular studies indicate a role of chitin in defense activation by EMF in local tissues and an immune response that is induced by yet unknown signals in aboveground tissues. Volatile organic compounds may be involved in long-distance communication between below- and aboveground tissues, in addition to metabolite signals in the xylem or phloem. In leaves of EMF-colonized plants, jasmonate signaling is involved in transcriptional re-wiring, leading to metabolic shifts in the secondary and nitrogen-based defense metabolism but cross talk with salicylate-related signaling is likely. Ectomycorrhizal-induced plant immunity shares commonalities with systemic acquired resistance and induced systemic resistance. We highlight novel developments and provide a guide to future research directions in EMF-induced resistance.

The work has been supported by the DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories”. Field work permits were issued by the responsible state environmental offices of Baden-Württemberg, Thüringen and Brandenburg (according to § 72 BbgNatSchG). S.S. was supported by the Spanish Government under a Ramón y Cajal contract (RYC-2016-20604).

To investigate N metabolism of two contrasting Populus species in acclimation to low N availability, saplings of slow-growing species (Populus popularis, Pp) and a fast-growing species (Populus alba × Populus glandulosa, Pg) were exposed to 10, 100, or 1000 μM NH4NO3. Despite greater root biomass and fine root surface area in Pp, lower net influxes of NH4 + and NO3 – at the root surface were detected in Pp compared to those in Pg, corresponding well to lower NH4 + and NO3 – content and total N concentration in Pp roots. Meanwhile, higher stable N isotope composition (δ15N) in roots and stronger responsiveness of transcriptional regulation of 18 genes involved in N metabolism were found in roots and leaves of Pp compared to those of Pg. These results indicate that the N metabolism of Pp is more sensitive to decreasing N availability than that of Pg. In both species, low N treatments decreased net influxes of NH4 + and NO3 –, root NH4 + and foliar NO3 – content, root NR activities, total N concentration in roots and leaves, and transcript levels of most ammonium (AMTs) and nitrate (NRTs) transporter genes in leaves and genes involved in N assimilation in roots and leaves. Low N availability increased fine root surface area, foliar starch concentration, δ15N in roots and leaves, and transcript abundance of several AMTs (e.g. AMT1;2) and NRTs (e.g. NRT1;2 and NRT2;4B) in roots of both species. These data indicate that poplar species slow down processes of N acquisition and assimilation in acclimation to limiting N supply.

Increases in summer droughts and nitrogen (N) deposition have raised concerns of widespread biodiversity loss and nutrient imbalances, but our understanding of the ecological role of ectomycorrhizal fungal (ECMF) diversity in mediating root functions remains a major knowledge gap. We used different global change scenarios to experimentally alter the composition of ECMF communities colonizing European beech saplings and examined the consequences for phosphorus (P) uptake (H3 33PO4 feeding experiment) and use efficiencies of trees. Specifically, we simulated increases in temperature and N deposition and decreases in soil moisture and P availability in a factorial experiment. Here, we show that ECMF α diversity is a major factor contributing to root functioning under global change. P uptake efficiency of beech significantly increased with increasing ECMF species richness and diversity, as well as with decreasing P availability. As a consequence of decreases in ECMF diversity, P uptake efficiency decreased when soil moisture was limiting. By contrast, P use efficiencies were a direct (negative) function of P availability and not of ECMF diversity. We conclude that increasing summer droughts may reduce ECMF diversity and the complementarity of P uptake by ECMF species, which will add to negative growth effects expected from nutrient imbalances under global change.

Phosphorus (P) is an essential plant nutrient, but its availability is often limited in soil. Here, we studied changes in the transcriptome and in nutrient element concentrations in leaves and roots of poplars (Populus × canescens) in response to P deficiency. P starvation resulted in decreased concentrations of S and major cations (K, Mg, Ca), in increased concentrations of N, Zn and Al, while C, Fe and Mn were only little affected. In roots and leaves >4,000 and >9,000 genes were differently expressed upon P starvation. These genes clustered in eleven co-expression modules of which seven were correlated with distinct elements in the plant tissues. One module (4.7% of all differentially expressed genes) was strongly correlated with changes in the P concentration in the plant. In this module the GO term \"response to P starvation\" was enriched with phosphoenolpyruvate carboxylase kinases, phosphatases and pyrophosphatases as well as regulatory domains such as SPX, but no phosphate transporters. The P-related module was also enriched in genes of the functional category \"galactolipid synthesis\". Galactolipids substitute phospholipids in membranes under P limitation. Two modules, one correlated with C and N and the other with biomass, S and Mg, were connected with the P-related module by co-expression. In these modules GO terms indicating \"DNA modification\" and \"cell division\" as well as \"defense\" and \"RNA modification\" and \"signaling\" were enriched; they contained phosphate transporters. Bark storage proteins were among the most strongly upregulated genes in the growth-related module suggesting that N, which could not be used for growth, accumulated in typical storage compounds. In conclusion, weighted gene coexpression network analysis revealed a hierarchical structure of gene clusters, which separated phosphate starvation responses correlated with P tissue concentrations from other gene modules, which most likely represented transcriptional adjustments related to down-stream nutritional changes and stress.