Storage of carbon reserves in spruce trees is prioritized over growth in the face of carbon limitation

Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.DATA AVAILABITY : All study data are included in the article and/or supporting information. Transcriptome data have been deposited in the NCBI database under BioProject accession no. PRJNA751264.Max Planck Society.https://www.pnas.orghj2022BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant Patholog

Eyes on the future – evidence for trade‐offs between growth, storage and defense in Norway spruce

Carbon (C) allocation plays a central role in tree responses to environmental changes. Yet, fundamental questions remain about how trees allocate C to different sinks, for example, growth vs storage and defense. In order to elucidate allocation priorities, we manipulated the whole‐tree C balance by modifying atmospheric CO2 concentrations [CO2] to create two distinct gradients of declining C availability, and compared how C was allocated among fluxes (respiration and volatile monoterpenes) and biomass C pools (total biomass, nonstructural carbohydrates (NSC) and secondary metabolites (SM)) in well‐watered Norway spruce (Picea abies) saplings. Continuous isotope labelling was used to trace the fate of newly‐assimilated C. Reducing [CO2] to 120 ppm caused an aboveground C compensation point (i.e. net C balance was zero) and resulted in decreases in growth and respiration. By contrast, soluble sugars and SM remained relatively constant in aboveground young organs and were partially maintained with a constant allocation of newly‐assimilated C, even at expense of root death from C exhaustion. We conclude that spruce trees have a conservative allocation strategy under source limitation: growth and respiration can be downregulated to maintain ‘operational’ concentrations of NSC while investing newly‐assimilated C into future survival by producing SM.Supplementary material: Fig. S1 Concentrations of soluble sugars, starch and NSC (soluble sugars + starch) expressed as percentage of control (400 ppm [CO2]) at the whole‐tree level. Fig. S2 Concentrations of soluble sugars, starch and NSC (soluble sugars + starch) at the whole‐tree level. Fig. S3 Concentrations of phenolic compounds, monoterpenes and total secondary metabolites expressed as percentage of control (400 ppm [CO2]) at the whole‐tree level. Fig. S4 Concentrations of phenolic compounds, monoterpenes and total secondary metabolites (phenolic compounds + monoterpenes) at the whole‐tree level. Fig. S5 δ13C (‰) of bulk tissue, water soluble C and phenolic compounds at the whole‐tree level. Methods S1 TD‐GC‐MS conditions for BVOC analysis. Table S1 Internal standards, weight‐based response factors and methods used for the measurements of secondary metabolites. Table S2 A rough estimation of allocation of newly‐assimilated carbon.JH was funded by the Chinese Scholarship Council and Max Planck Institute for Biogeochemistry, and acknowledges support from the International Max Planck Research School for Global Biogeochemical Cycles.http://www.newphytologist.com2020-04-01hj2019Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Analysis of mitochondrial haemoglobin in Parkinson's disease brain

Mitochondrial dysfunction is an early feature of neurodegeneration. We have shown there are mitochondrial haemoglobin changes with age and neurodegeneration. We hypothesised that altered physiological processes are associated with recruitment and localisation of haemoglobin to these organelles. To confirm a dynamic localisation of haemoglobin we exposed Drosophila melanogaster to cyclical hypoxia with recovery. With a single cycle of hypoxia and recovery we found a relative accumulation of haemoglobin in the mitochondria compared with the cytosol. An additional cycle of hypoxia and recovery led to a significant increase of mitochondrial haemoglobin (p b 0.05). We quantified ratios of human mitochondrial haemoglobin in 30 Parkinson's and matched control human post-mortem brains. Relative mitochondrial/cytosolic quantities of haemoglobin were obtained for the cortical region, substantia nigra and cerebellum. In age matched postmortem brain mitochondrial haemoglobin ratios change, decreasing with disease duration in female cerebellum samples (n = 7). The change is less discernible in male cerebellum (n = 18). In cerebellar mitochondria, haemoglobin localisation in males with long disease duration shifts from the intermembrane space to the outer membrane of the organelle. These new data illustrate dynamic localisation of mitochondrial haemoglobin within the cell. Mitochondrial haemoglobin should be considered in the context of gender differences characterised in Parkinson's disease. It has been postulated that cerebellar circuitry may be activated to play a protective role in individuals with Parkinson's. The changing localisation of intracellular haemoglobin in response to hypoxia presents a novel pathway to delineate the role of the cerebellum in Parkinson's disease

Plant diversity increases soil microbial activity and soil carbon storage

Plant diversity strongly influences ecosystem functions and services, such as soil carbon storage. However, the mechanisms underlying the positive plant diversity effects on soil carbon storage are poorly understood. We explored this relationship using long-term data from a grassland biodiversity experiment (The Jena Experiment) and radiocarbon (14C) modelling. Here we show that higher plant diversity increases rhizosphere carbon inputs into the microbial community resulting in both increased microbial activity and carbon storage. Increases in soil carbon were related to the enhanced accumulation of recently fixed carbon in high-diversity plots, while plant diversity had less pronounced effects on the decomposition rate of existing carbon. The present study shows that elevated carbon storage at high plant diversity is a direct function of the soil microbial community, indicating that the increase in carbon storage is mainly limited by the integration of new carbon into soil and less by the decomposition of existing soil carbon

Production of constitutive and induced secondary metabolites is coordinated with growth and storage in Norway spruce saplings.

A mechanistic understanding of how trees balance the trade-offs between growth, storage and defense is limited but crucial for predicting tree responses to abiotic and biotic stresses. Here we investigated how trees allocate storage of non-structural carbohydrates (NSC) to growth and constitutive and induced secondary metabolites (SM). We exposed Norway spruce (Picea abies) saplings to 5 weeks of complete darkness to induce light and/or carbon limitation and then applied methyl jasmonate (MeJA) to simulate biotic attack. We measured changes in biomass, NSC (sum of soluble sugars and starches), and constitutive and induced SM (sum of phenolic compounds and terpenoids) in current-year developing and previous-year mature needles and branches, as well as volatiles emitted from the canopy. Under darkness, NSC storage was preferentially used for constitutive biosynthesis of monoterpenes rather than biosynthesis of stilbenes and growth of developing organs, while SM stored in mature organs cannot be remobilized and recycled. Furthermore, MeJA-induced production of SM was constrained by low NSC availability in developing organs but not in mature organs grown in the dark. Emissions of volatiles were suppressed in the dark but after 1 h of re-illumination, emissions of both constitutive and induced monoterpene hydrocarbons recovered rapidly, whereas emissions of linalool and sesquiterpene produced via de novo synthesis did not recover. Our results highlight that light and/or carbon limitation may constrain constitutive and JA-induced biosynthesis of SM in coordination with growth, NSC storage and mobilization

Altered carbon turnover processes and microbiomes in soils under long-term extremely high CO2 exposure.

There is only limited understanding of the impact of high p(CO2) on soil biomes. We have studied a floodplain wetland where long-term emanations of temperate volcanic CO2 (mofettes) are associated with accumulation of carbon from the Earth's mantle. With an integrated approach using isotope geochemistry, soil activity measurements and multi-omics analyses, we demonstrate that high (nearly pure) CO2 concentrations have strongly affected pathways of carbon production and decomposition and therefore carbon turnover. In particular, a promotion of dark CO2 fixation significantly increased the input of geogenic carbon in the mofette when compared to a reference wetland soil exposed to normal levels of CO2. Radiocarbon analysis revealed that high quantities of mofette soil carbon originated from the assimilation of geogenic CO2 (up to 67%) via plant primary production and subsurface CO2 fixation. However, the preservation and accumulation of almost undegraded organic material appeared to be facilitated by the permanent exclusion of meso- to macroscopic eukaryotes and associated physical and/or ecological traits rather than an impaired biochemical potential for soil organic matter decomposition. Our study shows how CO2-induced changes in diversity and functions of the soil community can foster an unusual biogeochemical profile

An optimal defense strategy for phenolic glycoside production in Populus trichocarpa--isotope labeling demonstrates secondary metabolite production in growing leaves.

Large amounts of carbon are required for plant growth, but young, growing tissues often also have high concentrations of defensive secondary metabolites. Plants' capacity to allocate resources to growth and defense is addressed by the growth-differentiation balance hypothesis and the optimal defense hypothesis, which make contrasting predictions. Isotope labeling can demonstrate whether defense compounds are synthesized from stored or newly fixed carbon, allowing a detailed examination of these hypotheses. Populus trichocarpa saplings were pulse-labeled with 13CO2 at the beginning and end of a growing season, and the 13C signatures of phenolic glycosides (salicinoids), sugars, bulk tissue, and respired CO2 were traced over time. Half of the saplings were also subjected to mechanical damage. Populus trichocarpa followed an optimal defense strategy, investing 13C in salicinoids in expanding leaves directly after labeling. Salicinoids turned over quickly, and their production continued throughout the season. Salicin was induced by early-season damage, further demonstrating optimal defense. Salicinoids appear to be of great value to P. trichocarpa, as they command new C both early and late in the growing season, but their fitness benefits require further study. Export of salicinoids between tissues and biochemical pathways enabling induction also needs research. Nonetheless, the investigation of defense production afforded by isotope labeling lends new insights into plants' ability to grow and defend simultaneously

14C-Free Carbon Is a Major Contributor to Cellular Biomass in Geochemically Distinct Groundwater of Shallow Sedimentary Bedrock Aquifers.

Despite the global significance of the subsurface biosphere, the degree to which it depends on surface organic carbon (OC) is still poorly understood. Here, we compare stable and radiogenic carbon isotope compositions of microbial phospholipid fatty acids (PLFAs) with those of in situ potential microbial C sources to assess the major C sources for subsurface microorganisms in biogeochemical distinct shallow aquifers (Critical Zone Exploratory, Thuringia Germany). Despite the presence of younger OC, the microbes assimilated 14C-free OC to varying degrees; ~31% in groundwater within the oxic zone, ~47% in an iron reduction zone, and ~70% in a sulfate reduction/anammox zone. The persistence of trace amounts of mature and partially biodegraded hydrocarbons suggested that autochthonous petroleum-derived hydrocarbons were a potential 14C-free C source for heterotrophs in the oxic zone. In this zone, Δ14C values of dissolved inorganic carbon (-366 ± 18‰) and 11MeC16:0 (-283 ± 32‰), an important component in autotrophic nitrite oxidizers, were similar enough to indicate that autotrophy is an important additional C fixation pathway. In anoxic zones, methane as an important C source was unlikely since the 13C-fractionations between the PLFAs and CH4 were inconsistent with kinetic isotope effects associated with methanotrophy. In the sulfate reduction/anammox zone, the strong 14C-depletion of 10MeC16:0 (-942 ± 22‰), a PLFA common in sulfate reducers, indicated that those bacteria were likely to play a critical part in 14C-free sedimentary OC cycling. Results indicated that the 14C-content of microbial biomass in shallow sedimentary aquifers results from complex interactions between abundance and bioavailability of naturally occurring OC, hydrogeology, and specific microbial metabolisms