Matthias Arend

A Molecular Timetable for Apical Bud Formation and Dormancy Induction in Poplar

The growth of perennial plants in the temperate zone alternates with periods of dormancy that are typically initiated during bud development in autumn. In a systems biology approach to unravel the underlying molecular program of apical bud development in poplar (Populus tremula × Populus alba), combined transcript and metabolite profiling were applied to a high-resolution time course from short-day induction to complete dormancy. Metabolite and gene expression dynamics were used to reconstruct the temporal sequence of events during bud development. Importantly, bud development could be dissected into bud formation, acclimation to dehydration and cold, and dormancy. To each of these processes, specific sets of regulatory and marker genes and metabolites are associated and provide a reference frame for future functional studies. Light, ethylene, and abscisic acid signal transduction pathways consecutively control bud development by setting, modifying, or terminating these processes. Ethylene signal transduction is positioned temporally between light and abscisic acid signals and is putatively activated by transiently low hexose pools. The timing and place of cell proliferation arrest (related to dormancy) and of the accumulation of storage compounds (related to acclimation processes) were established within the bud by electron microscopy. Finally, the identification of a large set of genes commonly expressed during the growth-to-dormancy transitions in poplar apical buds, cambium, or Arabidopsis thaliana seeds suggests parallels in the underlying molecular mechanisms in different plant organs.

How tree roots respond to drought

The ongoing climate change is characterized by increased temperatures and altered precipitation patterns. In addition, there has been an increase in both the frequency and intensity of extreme climatic events such as drought. Episodes of drought induce a series of interconnected effects, all of which have the potential to alter the carbon balance of forest ecosystems profoundly at different scales of plant organization and ecosystem functioning. During recent years, considerable progress has been made in the understanding of how aboveground parts of trees respond to drought and how these responses affect carbon assimilation. In contrast, processes of belowground parts are relatively underrepresented in research on climate change. In this review, we describe current knowledge about responses of tree roots to drought. Tree roots are capable of responding to drought through a variety of strategies that enable them to avoid and tolerate stress. Responses include root biomass adjustments, anatomical alterations, and physiological acclimations. The molecular mechanisms underlying these responses are characterized to some extent, and involve stress signaling and the induction of numerous genes, leading to the activation of tolerance pathways. In addition, mycorrhizas seem to play important protective roles. The current knowledge compiled in this review supports the view that tree roots are well equipped to withstand drought situations and maintain morphological and physiological functions as long as possible. Further, the reviewed literature demonstrates the important role of tree roots in the functioning of forest ecosystems and highlights the need for more research in this emerging field.

Provenance-specific growth responses to drought and air warming in three European oak species (Quercus robur, Q. petraea and Q. pubescens)

Provenance-specific growth responses to experimentally applied drought and air warming were studied in saplings of three European oak species: Quercus robur, Quercus petraea and Quercus pubescens. Four provenances of each species were grown in large open-top chambers and subjected to four climates: control, periodic drought, air warming or their combination in 3 subsequent years. Overall growth responses were found among species and provenances, with drought reducing shoot height growth and stem diameter growth and air warming stimulating shoot height growth but reducing stem diameter growth and root length growth. Differential growth responses in shoots, stems and roots resulted in altered allometric growth relations. Root length growth to shoot height growth increased in response to drought but decreased in response to air warming. Stem diameter growth to shoot height growth decreased in response to air warming. The growth responses in shoots and stems were highly variable among provenances indicating provenance-specific sensitivity to drought and air warming, but this response variability did not reflect local adaptation to climate conditions of provenance origin. Shoot height growth was found to be more sensitive to drought in provenances from northern latitudes than in provenances from southern latitudes, suggesting that genetic factors related to the postglacial immigration history of European oaks might have interfered with selective pressure at provenance origins.

Expression of the Arabidopsis Mutant abi1 Gene Alters Abscisic Acid Sensitivity, Stomatal Development, and Growth Morphology in Gray Poplars

The consequences of altered abscisic acid (ABA) sensitivity in gray poplar (Populus × canescens [Ait.] Sm.) development were examined by ectopic expression of the Arabidopsis (Arabidopsis thaliana) mutant abi1 (for abscisic acid insensitive1) gene. The expression resulted in an ABA-insensitive phenotype revealed by a strong tendency of abi1 poplars to wilt, impaired responsiveness of their stomata to ABA, and an ABA-resistant bud outgrowth. These plants therefore required cultivation under very humid conditions to prevent drought stress symptoms. Morphological alterations became evident when comparing abi1 poplars with poplars expressing Arabidopsis nonmutant ABI1 or wild-type plants. abi1 poplars showed increased stomatal size, enhanced shoot growth, and retarded leaf and root development. The increased stomatal size and its reversion to the size of wild-type plants by exogenous ABA indicate a role for ABA in regulating stomatal development. Enhanced shoot growth and retarded leaf and root development support the hypothesis that ABA acts independently from drought stress as a negative regulator of growth in shoots and as a positive regulator of growth in leaves and roots. In shoots, we observed an interaction of ABA with ethylene: abi1 poplars exhibited elevated ethylene production, and the ethylene perception inhibitor Ag+ antagonized the enhanced shoot growth. Thus, we provide evidence that ABA acts as negative regulator of shoot growth in nonstressed poplars by restricting ethylene production. Furthermore, we show that ABA has a role in regulating shoot branching by inhibiting lateral bud outgrowth.

Water regime and growth of young oak stands subjected to air‐warming and drought on two different forest soils in a model ecosystem experiment

Global climate change is expected to increase annual temperatures and decrease summer precipitation in Central Europe. Little is known of how forests respond to the interaction of these climate factors and if their responses depend on soil conditions. In a 3-year lysimeter experiment, we investigated the growth response of young mixed oak stands, on either acidic or calcareous soil, to soil water regime, air-warming and drought treatments corresponding to an intermediate climate change scenario. The air-warming and drought treatments were applied separately as well as in combination. The air-warming treatment had no effect on soil water availability, evapotranspiration or stand biomass. Decreased evapotranspiration from the drought-exposed stands led to significantly higher air and soil temperatures, which were attributed to impaired transpirational cooling. Water limitation significantly reduced the stand foliage, shoot and root biomass as droughts were severe, as shown in low leaf water potentials. Additional air warming did not enhance the drought effects on evapotranspiration and biomass, although more negative leaf water potentials were observed. After re-watering, evapotranspiration increased within a few days to pre-drought levels. Stands not subjected to the drought treatment produced significantly less biomass on the calcareous soil than on the acidic soil, probably due to P or Mn limitation. There was no difference in biomass and water regime between the two soils under drought conditions, indicating that nutrient availability was governed by water availability under these conditions. The results demonstrate that young oak stands can cope with severe drought and therefore can be considered for future forestry.

Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum

The most frequently encountered symbiont on tree roots is the ascomycete Cenococcum geophilum, the only mycorrhizal species within the largest fungal class Dothideomycetes, a class known for devastating plant pathogens. Here we show that the symbiotic genomic idiosyncrasies of ectomycorrhizal basidiomycetes are also present in C. geophilum with symbiosis-induced, taxon-specific genes of unknown function and reduced numbers of plant cell wall-degrading enzymes. C. geophilum still holds a significant set of genes in categories known to be involved in pathogenesis and shows an increased genome size due to transposable elements proliferation. Transcript profiling revealed a striking upregulation of membrane transporters, including aquaporin water channels and sugar transporters, and mycorrhiza-induced small secreted proteins (MiSSPs) in ectomycorrhiza compared with free-living mycelium. The frequency with which this symbiont is found on tree roots and its possible role in water and nutrient transport in symbiosis calls for further studies on mechanisms of host and environmental adaptation.

Seasonal Changes of Plasma Membrane H+-ATPase and Endogenous Ion Current during Cambial Growth in Poplar Plants

The plasma membrane H+-ATPase (PM H+-ATPase), potassium ions, and endogenous ion currents might play a fundamental role in the physiology of cambial growth. Seasonal changes of these parameters were studied in twigs ofPopulus nigra and Populus trichocarpa. Monoclonal and polyclonal antibodies against the PM H+-ATPase, x-ray analysis for K+ localization and a vibrating electrode for measurement of endogenous ion currents were used as probes. In dormant plants during autumn and winter, only a slight immunoreactivity against the PM H+-ATPase was found in cross sections and tissue homogenates, K+ was distributed evenly, and the density of endogenous current was low. In spring during cambial growth, strong immunoreactivity against a PM H+-ATPase was observed in cambial cells and expanding xylem cells using the monoclonal antibody 46 E5 B11 F6 for fluorescence microscopy and transmission electron microscopy. At the same time, K+ accumulated in cells of the cambial region, and strong endogenous current was measured in the cambial and immature xylem zone. Addition of auxin to dormant twigs induced the formation of this PM H+-ATPase in the dormant cambial region within a few days and an increase in density of endogenous current in shoot cuttings within a few hours. The increase in PM H+-ATPase abundance and in current density by auxin indicates that auxin mediates a rise in number and activity of an H+-ATPase in the plasma membrane of cambial cells and their derivatives. This PM H+-ATPase generates the necessary H+-gradient (proton-motive force) for the uptake of K+ and nutrients into cambial and expanding xylem cells.

Concomitant dendrometer and leaf patch pressure probe measurements reveal the effect of microclimate and soil moisture on diurnal stem water and leaf turgor variations in young oak trees

Tree water relations and their dependence on microclimate and soil moisture were studied over several months in young oaks (Quercus robur L.) subjected in large lysimeter-based open top chambers to environments with a controlled soil water supply. Automated single point dendrometers and the recently developed leaf patch clamp pressure (LPCP) probe were used for monitoring water-related stem radius variations (ΔW) and turgor-dependent leaf patch pressures (Pp). Both parameters showed distinct diurnal patterns with sharp negative and positive peaking of ΔW and Pp, respectively, after solar noon and recovery to initial levels in the evening. During the day, varying solar radiation was responsible for short time fluctuations of Pp in the range of minutes to hours reflecting feedback regulation of leaf turgor by sunlight driven stomatal movements. At longer timescales, i.e. days to months, atmospheric vapour pressure deficit (VPD) and soil water content (SWC) were the main determinants of ΔW and Pp. Daily minimum and maximum values of ΔW and Pp decreased and increased, respectively, with increasing VPD or decreasing SWC and recovery of ΔW and Pp in the evening was impeded by low SWC. In well-watered oaks, daily positive peaking of Pp preceded daily negative peaking of ΔW; these time lags gradually increased with increasing soil drought, suggesting hydraulic uncoupling of stem and leaves.

A phenological timetable of oak growth under experimental drought and air warming

Climate change is expected to increase temperature and decrease summer precipitation in Central Europe. Little is known about how warming and drought will affect phenological patterns of oaks, which are considered to possess excellent adaptability to these climatic changes. Here, we investigated bud burst and intra-annual shoot growth of Quercus robur, Q. petraea and Q. pubescens grown on two different forest soils and exposed to air warming and drought. Phenological development was assessed over the course of three growing seasons. Warming advanced bud burst by 1–3 days °C−1 and led to an earlier start of intra-annual shoot growth. Despite this phenological shift, total time span of annual growth and shoot biomass were not affected. Drought changed the frequency and intensity of intra-annual shoot growth and advanced bud burst in the subsequent spring of a severe summer drought by 1–2 days. After re-wetting, shoot growth recovered within a few days, demonstrating the superior drought tolerance of this tree genus. Our findings show that phenological patterns of oaks are modified by warming and drought but also suggest that ontogenetic factors and/or limitations of water and nutrients counteract warming effects on the biomass and the entire span of annual shoot growth.

Root growth of different oak provenances in two soils under drought stress and air warming conditions

Background and aimsOaks are considered to be drought- and thermo-tolerant tree species. Nevertheless, species and provenances may differ in their ecological requirements. We hypothesised that (i) provenances from xeric sites are better adapted to drought than those from more humid sites, (ii) oaks direct root growth towards resource-rich layers, and (iii) air-warming promotes root growth.MethodsTo test different provenances of Quercus robur, Q. petraea and Q. pubescens, we conducted a model ecosystem experiment with young trees, grown on acidic and calcareous soil, subjected to drought, air warming, the combination of warming and drought, and a control.ResultsThe results were only in partial agreement with the first hypothesis. As expected the provenances originating from drier sites produced more biomass than those from more humid sites under drought conditions. Surprisingly, however, they reacted more sensitive to water limiting conditions, as they produced also substantially more biomass under well-watered conditions. The drought treatment reduced root mass substantially in the upper soil. In agreement with the second hypothesis this led to a shift in the centre of root mass to lower depth, where water was still more available than closer to the soil surface. In contrast to the third hypothesis, the air-warming treatment, which was very mild however compared to climate change scenarios, had no significant effects on root growth.ConclusionsGiven that the provenances from drier sites showed more biomass loss at water limiting conditions than provenances from more humid sites, it remains questionable whether provenances from drier sites are better suited for a future climate.