Divergent driving mechanisms of community temporal stability in China's drylands.

Climate change and anthropogenic activities are reshaping dryland ecosystems globally at an unprecedented pace, jeopardizing their stability. The stability of these ecosystems is crucial for maintaining ecological balance and supporting local communities. Yet, the mechanisms governing their stability are poorly understood, largely due to the scarcity of comprehensive field data. Here we show the patterns of community temporal stability and its determinants across an aridity spectrum by integrating a transect survey across China's drylands with remote sensing. Our results revealed a U-shaped relationship between community temporal stability and aridity, with a pivotal shift occurring around an aridity level of 0.88. In less arid areas (aridity level below 0.88), enhanced precipitation and biodiversity were associated with increased community productivity and stability. Conversely, in more arid zones (aridity level above 0.88), elevated soil organic carbon and biodiversity were linked to greater fluctuations in community productivity and reduced stability. Our study identifies a critical aridity threshold that precipitates significant changes in community stability in China's drylands, underscoring the importance of distinct mechanisms driving ecosystem stability in varying aridity contexts. These insights are pivotal for developing informed ecosystem management and policy strategies tailored to the unique challenges of dryland conservation.

Drought increases Norway spruce susceptibility to the Eurasian spruce bark beetle and its associated fungi.

Drought affects the complex interactions between Norway spruce, the bark beetle Ips typographus and associated microorganisms. We investigated the interplay of tree water status, defense and carbohydrate reserves with the incidence of bark beetle attack and infection of associated fungi in mature spruce trees. We installed roofs to induce a 2-yr moderate drought in a managed spruce stand to examine a maximum of 10 roof and 10 control trees for resin flow (RF), predawn twig water potentials, terpene, phenolic and carbohydrate bark concentrations, and bark beetle borings in field bioassays before and after inoculation with Endoconidiophora polonica and Grosmannia penicillata. Drought-stressed trees showed more attacks and significantly longer fungal lesions than controls, but maintained terpene resin defenses at predrought levels. Reduced RF and lower mono- and diterpene, but not phenolic concentrations were linked with increased host selection. Bark beetle attack and fungi stimulated chemical defenses, yet G. penicillata reduced phenolic and carbohydrate contents. Chemical defenses did not decrease under mild, prolonged drought in our simulated small-scale biotic infestations. However, during natural mass attacks, reductions in carbon fixation under drought, in combination with fungal consumption of carbohydrates, may deplete tree defenses and facilitate colonization by I. typographus.

The mobilization and transport of newly fixed carbon are driven by plant water use in an experimental rainforest under drought.

Non-structural carbohydrates (NSCs) are building blocks for biomass and fuel metabolic processes. However, it remains unclear how tropical forests mobilize, export, and transport NSCs to cope with extreme droughts. We combined drought manipulation and ecosystem 13CO2 pulse-labeling in an enclosed rainforest at Biosphere 2, assessed changes in NSCs, and traced newly assimilated carbohydrates in plant species with diverse hydraulic traits and canopy positions. We show that drought caused a depletion of leaf starch reserves and slowed export and transport of newly assimilated carbohydrates below ground. Drought effects were more pronounced in conservative canopy trees with limited supply of new photosynthates and relatively constant water status than in those with continual photosynthetic supply and deteriorated water status. We provide experimental evidence that local utilization, export, and transport of newly assimilated carbon are closely coupled with plant water use in canopy trees. We highlight that these processes are critical for understanding and predicting tree resistance and ecosystem fluxes in tropical forest under drought.

Field-work reveals a novel function for MAX2 in a native tobacco's high-light adaptions.

Laboratory studies have revealed that strigolatone (SL) and karrikin (KAR) signalling mediate responses to abiotic and biotic stresses, and reshape branching architecture that could increase reproductive performance and crop yields. To understand the ecological function of SL and KAR signalling, transgenic lines of wild tobacco Nicotiana attenuata, silenced in SL/KAR biosynthesis/signalling were grown in the glasshouse and in two field plots in the Great Basin Desert in Utah over four field seasons. Of the lines silenced in SL and KAR signalling components (irMAX2, irD14, irKAI2 and irD14 × irKAI2 plants), which exhibited the expected increases in shoot branching, only irMAX2 plants showed a strong leaf-bleaching phenotype when grown in the field. In the field, irMAX2 plants had lower sugar and higher leaf amino acid contents, lower lifetime fitness and were more susceptible to herbivore attack compared to wild-type plants. These irMAX2 phenotypes were not observed in glasshouse-grown plants. Transcriptomic analysis revealed dramatic responses to high-light intensity in irMAX2 leaves in the field: lutein contents decreased, and transcriptional responses to high-intensity light, singlet oxygen and hydrogen peroxide increased. PAR and UV-B manipulations in the field revealed that the irMAX2 bleaching phenotype is reversed by decreasing PAR, but not UV-B fluence. We propose that NaMAX2 functions in high-light adaptation and fitness optimisation by regulating high-light responses independently of its roles in the SL and KAR signalling pathways. The work provides another example of the value of studying the function of genes in the complex environments in which plants evolved, namely nature.

Addressing a century-old hypothesis - do pioneer beetles of Ips typographus use volatile cues to find suitable host trees?

Global warming and more frequent climate extremes have caused bark beetle outbreaks of unprecedented scale of these insects in many conifer forests world-wide. Conifers that have been weakened by drought and heat or damaged by storms are highly susceptible to bark beetle infestation. A large proportion of trees with impaired defences provides good conditions for beetle population build-up of beetles, but mechanisms driving host search of pioneer beetles are still uncertain in several species, including the Eurasian spruce bark beetle Ips typographus. Despite a two-century-long history of bark beetle research, we still lack a sufficient understanding of interactions between I. typographus and its host Norway spruce (Picea abies) to forecast future disturbance regimes and forest dynamics. Depending on the scale (habitat or patch) and beetle population state (endemic or epidemic), host selection is likely driven by a combination of pre and postlanding cues, including visual selection or olfactory detection (kairomones). Here, we discuss primary attraction mechanisms and how volatile emission profiles of Norway spruce may provide cues on tree vitality and suitability for attacks by I. typographus, in particular during the endemic phase. We identify several crucial knowledge gaps and provide a research agenda addressing the experimental challenges of such investigations.

Amplifying effects of recurrent drought on the dynamics of tree growth and water use in a subalpine forest.

Despite recent advances in our understanding of drought impacts on tree functioning, we lack knowledge about the dynamic responses of mature trees to recurrent drought stress. At a subalpine forest site, we assessed the effects of three years of recurrent experimental summer drought on tree growth and water relations of Larix decidua Mill. and Picea abies (L. Karst.), two common European conifers representative for contrasting water-use strategies. We combined dendrometer and xylem sap flow measurements with analyses of xylem anatomy and non-structural carbohydrates and their carbon-isotope composition. Recurrent drought increased the effects of soil moisture limitation on growth and xylogenesis, and to a lesser extent on xylem sap flow. P. abies showed stronger growth responses to recurrent drought, reduced starch concentrations in branches and increased water-use efficiency when compared to L. decidua. Despite comparatively larger maximum tree water deficits than in P. abies, xylem formation of L. decidua was less affected by drought, suggesting a stronger capacity of rehydration or lower cambial turgor thresholds for growth. Our study shows that recurrent drought progressively increases impacts on mature trees of both species, which suggests that in a future climate increasing drought frequency could impose strong legacies on carbon and water dynamics of treeline species.

Ecosystem fluxes during drought and recovery in an experimental forest.

Severe droughts endanger ecosystem functioning worldwide. We investigated how drought affects carbon and water fluxes as well as soil-plant-atmosphere interactions by tracing 13CO2 and deep water 2H2O label pulses and volatile organic compounds (VOCs) in an enclosed experimental rainforest. Ecosystem dynamics were driven by different plant functional group responses to drought. Drought-sensitive canopy trees dominated total fluxes but also exhibited the strongest response to topsoil drying. Although all canopy-forming trees had access to deep water, these reserves were spared until late in the drought. Belowground carbon transport was slowed, yet allocation of fresh carbon to VOCs remained high. Atmospheric VOC composition reflected increasing stress responses and dynamic soil-plant-atmosphere interactions, potentially affecting atmospheric chemistry and climate feedbacks. These interactions and distinct functional group strategies thus modulate drought impacts and ecosystem susceptibility to climate change.

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.

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.

Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling.

Drought has promoted large-scale, insect-induced tree mortality in recent years, with severe consequences for ecosystem function, atmospheric processes, sustainable resources and global biogeochemical cycles. However, the physiological linkages among drought, tree defences, and insect outbreaks are still uncertain, hindering our ability to accurately predict tree mortality under on-going climate change. Here we propose an interdisciplinary research agenda for addressing these crucial knowledge gaps. Our framework includes field manipulations, laboratory experiments, and modelling of insect and vegetation dynamics, and focuses on how drought affects interactions between conifer trees and bark beetles. We build upon existing theory and examine several key assumptions: (1) there is a trade-off in tree carbon investment between primary and secondary metabolites (e.g. growth vs defence); (2) secondary metabolites are one of the main component of tree defence against bark beetles and associated microbes; and (3) implementing conifer-bark beetle interactions in current models improves predictions of forest disturbance in a changing climate. Our framework provides guidance for addressing a major shortcoming in current implementations of large-scale vegetation models, the under-representation of insect-induced tree mortality.

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.

New Perspectives on CO2, Temperature, and Light Effects on BVOC Emissions Using Online Measurements by PTR-MS and Cavity Ring-Down Spectroscopy.

Volatile organic compounds (VOC) play important roles in atmospheric chemistry, plant ecology, and physiology, and biogenic VOC (BVOC) emitted by plants is the largest VOC source. Our knowledge about how environmental drivers (e.g., carbon, light, and temperature) may regulate BVOC emissions is limited because they are often not controlled. We combined a greenhouse facility to manipulate atmospheric CO2 ([CO2]) with proton-transfer-reaction mass spectrometry (PTR-MS) and cavity ring-down spectroscopy to investigate the regulation of BVOC in Norway spruce. Our results indicate a direct relationship between [CO2] and methanol and acetone emissions, and their temperature and light dependencies, possibly related to substrate availability. The composition of monoterpenes stored in needles remained constant, but emissions of mono-(linalool) and sesquiterpenes (ß-farnesene) increased at lower [CO2], with the effects being most pronounced at the highest air temperature. Pulse-labeling suggested an immediate incorporation of recently assimilated carbon into acetone, mono- and sesquiterpene emissions even under 50 ppm [CO2]. Our results provide new perspectives on CO2, temperature and light effects on BVOC emissions, in particular how they depend on stored pools and recent photosynthetic products. Future studies using smaller but more seedlings may allow sufficient replication to examine the physiological mechanisms behind the BVOC responses.

Increasing carbon availability stimulates growth and secondary metabolites via modulation of phytohormones in winter wheat.

Phytohormones play important roles in plant acclimation to changes in environmental conditions. However, their role in whole-plant regulation of growth and secondary metabolite production under increasing atmospheric CO2 concentrations ([CO2]) is uncertain but crucially important for understanding plant responses to abiotic stresses. We grew winter wheat (Triticum aestivum) under three [CO2] (170, 390, and 680 ppm) over 10 weeks, and measured gas exchange, relative growth rate (RGR), soluble sugars, secondary metabolites, and phytohormones including abscisic acid (ABA), auxin (IAA), jasmonic acid (JA), and salicylic acid (SA) at the whole-plant level. Our results show that, at the whole-plant level, RGR positively correlated with IAA but not ABA, and secondary metabolites positively correlated with JA and JA-Ile but not SA. Moreover, soluble sugars positively correlated with IAA and JA but not ABA and SA. We conclude that increasing carbon availability stimulates growth and production of secondary metabolites via up-regulation of auxin and jasmonate levels, probably in response to sugar-mediated signalling. Future low [CO2] studies should address the role of reactive oxygen species (ROS) in leaf ABA and SA biosynthesis, and at the transcriptional level should focus on biosynthetic and, in particular, on responsive genes involved in [CO2]-induced hormonal signalling pathways.

Release of resource constraints allows greater carbon allocation to secondary metabolites and storage in winter wheat.

The atmospheric CO2 concentration ([CO2 ]) is rapidly increasing, and this may have substantial impact on how plants allocate metabolic resources. A thorough understanding of allocation priorities can be achieved by modifying [CO2 ] over a large gradient, including low [CO2 ], thereby altering plant carbon (C) availability. Such information is of critical importance for understanding plant responses to global environmental change. We quantified the percentage of daytime whole-plant net assimilation (A) allocated to night-time respiration (R), structural growth (SG), nonstructural carbohydrates (NSC) and secondary metabolites (SMs) during 8 weeks of vegetative growth in winter wheat (Triticum aestivum) growing at low, ambient and elevated [CO2 ] (170, 390 and 680 ppm). R/A remained relatively constant over a large gradient of [CO2 ]. However, with increasing C availability, the fraction of assimilation allocated to biomass (SG + NSC + SMs), in particular NSC and SMs, increased. At low [CO2 ], biomass and NSC increased in leaves but decreased in stems and roots, which may help plants achieve a functional equilibrium, that is, overcome the most severe resource limitation. These results reveal that increasing C availability from rising [CO2 ] releases allocation constraints, thereby allowing greater investment into long-term survival in the form of NSC and SMs.