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1.  A Functional and Structural Mongolian Scots Pine (Pinus sylvestris var. mongolica) Model Integrating Architecture, Biomass and Effects of Precipitation 
PLoS ONE  2012;7(8):e43531.
Mongolian Scots pine (Pinus sylvestris var. mongolica) is one of the principal tree species in the network of Three-North Shelterbelt for windbreak and sand stabilisation in China. The functions of shelterbelts are highly correlated with the architecture and eco-physiological processes of individual tree. Thus, model-assisted analysis of canopy architecture and function dynamic in Mongolian Scots pine is of value for better understanding its role and behaviour within shelterbelt ecosystems in these arid and semiarid regions. We present here a single-tree functional and structural model, derived from the GreenLab model, which is adapted for young Mongolian Scots pines by incorporation of plant biomass production, allocation, allometric rules and soil water dynamics. The model is calibrated and validated based on experimental measurements taken on Mongolian Scots pines in 2007 and 2006 under local meteorological conditions. Measurements include plant biomass, topology and geometry, as well as soil attributes and standard meteorological data. After calibration, the model allows reconstruction of three-dimensional (3D) canopy architecture and biomass dynamics for trees from one- to six-year-old at the same site using meteorological data for the six years from 2001 to 2006. Sensitivity analysis indicates that rainfall variation has more influence on biomass increment than on architecture, and the internode and needle compartments and the aboveground biomass respond linearly to increases in precipitation. Sensitivity analysis also shows that the balance between internode and needle growth varies only slightly within the range of precipitations considered here. The model is expected to be used to investigate the growth of Mongolian Scots pines in other regions with different soils and climates.
PMCID: PMC3425476  PMID: 22927982
2.  Intra-seasonal dynamics in metabolic processes of 13C/12C and 18O/16O in components of Scots pine twigs from southern Siberia interpreted with a conceptual framework based on the Carbon Metabolism Oscillatory Model 
BMC Plant Biology  2012;12:76.
Carbon isotope data from conifer trees play an important role in research on the boreal forest carbon reservoir in the global carbon cycle. Carbon isotopes are routinely used to study interactions between the environment and tree growth. Moreover, carbon isotopes became an essential tool for the evaluation of carbon assimilation and transport from needles into reserve pools, as well as the allocation of stored assimilates within a tree. The successful application and interpretation of carbon isotopes rely on the coherence of isotopic fractionation modeling. This study employs a new Carbon Metabolism Oscillatory Model (CMOM) to interpret the experimental data sets on metabolic seasonal dynamics of 13C/12 C and 18O/16O ratios measured in twig components of Scots pine growing in southern Siberia (Russia).
The dynamics of carbon isotopic variables were studied in components of Pinus sylvestris L. in light and in dark chambers during the vegetation period from 14 June to 28 July 2006. At the beginning of this period water-soluble organic matter, mostly labile sugars (including sucrose as the main component) and newly formed bulk needle material, displayed relatively “light” δ13C values (depletion in 13 C). Then, 13 C content increased again with noticeable “depletion” events in the middle of the growth period. A gradual 13 C accumulation took place in the second half of the vegetation period. Similar effects were observed both in the light and in the dark with some temporal shifts. Environmental factors did not influence the δ13C values. A gradual 12C-depletion effect was noticed in needles of the previous year. The δ13C values of sucrose and proteins from needle biomass altered independently from each other in the light chamber. A distinct negative correlation between δ13C and δ18O values was revealed for all studied variables.
The abrupt 13C depletion recorded by all tested trees for the period from June to July provides clear evidence of the transition from the dominant role of reserve carbohydrate pool (RCP) during the first half of the growth season to the preferable current year carbohydrate pool (CCP) consumption by new needles during its second half. The investigation of the isotopic signatures of Pinus sylvestris L. emphasizes the pivotal role of the intra-seasonal dynamics in carbon metabolism through the transport of assimilates from autotrophic (needles) to heterotrophic (twigs) organs of the studied trees. This provides an explanation for changes of carbon isotopic values observed within the growth season. The CMOM-based results support the hypothesis of the integration of three carbohydrate pools by photosynthesizing cells. The fluctuations of the carbon isotope ratios in different carbohydrate pools underlie various physiological processes in the tree metabolism. The possible mechanisms and pathways of formation of these carbohydrate pools are further discussed. Hence, CMOM provides a reasonable explanation for the absence of the impact of environmental conditions on the needle isotopic variables, the 12C-depletion effects and the use of RCP in needles. The model explains the negative connections between δ13C and δ18O values in all studied variables.
PMCID: PMC3432013  PMID: 22646756
3.  Nine Years of Irrigation Cause Vegetation and Fine Root Shifts in a Water-Limited Pine Forest 
PLoS ONE  2014;9(5):e96321.
Scots pines (Pinus sylvestris L.) in the inner-Alpine dry valleys of Switzerland have suffered from increased mortality during the past decades, which has been caused by longer and more frequent dry periods. In addition, a proceeding replacement of Scots pines by pubescent oaks (Quercus pubescens Willd.) has been observed. In 2003, an irrigation experiment was performed to track changes by reducing drought pressure on the natural pine forest. After nine years of irrigation, we observed major adaptations in the vegetation and shifts in Scots pine fine root abundance and structure. Irrigation permitted new plant species to assemble and promote canopy closure with a subsequent loss of herb and moss coverage. Fine root dry weight increased under irrigation and fine roots had a tendency to elongate. Structural composition of fine roots remained unaffected by irrigation, expressing preserved proportions of cellulose, lignin and phenolic substances. A shift to a more negative δ13C signal in the fine root C indicates an increased photosynthetic activity in irrigated pine trees. Using radiocarbon (14C) measurement, a reduced mean age of the fine roots in irrigated plots was revealed. The reason for this is either an increase in newly produced fine roots, supported by the increase in fine root biomass, or a reduced lifespan of fine roots which corresponds to an enhanced turnover rate. Overall, the responses belowground to irrigation are less conspicuous than the more rapid adaptations aboveground. Lagged and conservative adaptations of tree roots with decadal lifespans are challenging to detect, hence demanding for long-term surveys. Investigations concerning fine root turnover rate and degradation processes under a changing climate are crucial for a complete understanding of C cycling.
PMCID: PMC4011741  PMID: 24802642
4.  Adaptation strategies and referencing trial of Scots and black pine populations subjected to heavy metal pollution 
The impact of industrial heavy metal pollution on Scots pine (Pinus sylvestris L.) and black pine (Pinus nigra Arn.) populations was investigated. Sampled pine stands, which were located in Upper Silesia (southern Poland) in an area strongly polluted by heavy metals, consisted of resistant and sensitive trees. To evaluate the adaptation process, genetic structure and diversity was tested using isozyme analysis. Higher levels of Zn, Pb, Cd and Cu were detected in needles of sensitive trees compared with resistant ones. With respect to morphology, Scots pines were more distinctly impaired than black pines. Although black pines had lower heavy metal concentrations, levels in 1-year-old needles, other than Cu, significantly exceeded “reference plant” values (Markert 1994). In both species, resistant trees demonstrated a lower degree of genetic variation than metal-sensitive trees with respect to some enzyme loci (SHDH A, PGI, PGM, MDH C and DIA). This observation was corroborated in sensitive trees by the smaller number of identified alleles and alleles per locus, absence of private alleles and significant excess of homozygotes in relation to expected Hardy–Weinberg equilibrium values. Assuming that only resistant trees of both species survive under conditions of prolonged soil contamination, the observed genetic structure implies that remaining populations will be depleted of some alleles of unknown adaptive value to future selection pressures. Genetic changes induced by heavy metals suggest an important role for specific enzymes—FEST, SHDH A and B, GOT B and PGI—in the adaptation process. Our results may serve as a basis for selection and propagation of individuals appropriate for re-cultivation of areas chemically degraded by industrial activity.
PMCID: PMC3906555  PMID: 24043503
Genetic variation; Heavy metal; Enzymes; Pinus nigra; Pinus sylvestris; Reference plant
5.  Secret lifestyles of Neurospora crassa 
Scientific Reports  2014;4:5135.
Neurospora crassa has a long history as an excellent model for genetic, cellular, and biochemical research. Although this fungus is known as a saprotroph, it normally appears on burned vegetations or trees after forest fires. However, due to a lack of experimental evidence, the nature of its association with living plants remains enigmatic. Here we report that Scots pine (Pinus sylvestris) is a host plant for N. crassa. The endophytic lifestyle of N. crassa was found in its interaction with Scots pine. Moreover, the fungus can switch to a pathogenic state when its balanced interaction with the host is disrupted. Our data reveal previously unknown lifestyles of N. crassa, which are likely controlled by both environmental and host factors. Switching among the endophytic, pathogenic, and saprotrophic lifestyles confers upon fungi phenotypic plasticity in adapting to changing environments and drives the evolution of fungi and associated plants.
PMCID: PMC4038807  PMID: 24875794
6.  Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor 
At the last glacial maximum, Fennoscandia was covered by an ice sheet while the tundra occupied most of the rest of northern Eurasia. More or less disjunct refugial populations of plants were dispersed in southern Europe, often trapped between mountain ranges and seas. Genetic and paleobotanical evidences indicate that these populations have contributed much to Holocene recolonization of more northern latitudes. Less supportive evidence has been found for the existence of glacial populations located closer to the ice margin. Scots pine (Pinus sylvestris L.) is a nordic conifer with a wide natural range covering much of Eurasia. Fractures in its extant genetic structure might be indicative of glacial vicariance and how different refugia contributed to the current distribution at the continental level. The population structure of Scots pine was investigated on much of its Eurasian natural range using maternally inherited mitochondrial DNA polymorphisms.
A novel polymorphic region of the Scots pine mitochondrial genome has been identified, the intron 1 of nad7, with three variants caused by insertions-deletions. From 986 trees distributed among 54 populations, four distinct multi-locus mitochondrial haplotypes (mitotypes) were detected based on the three nad7 intron 1 haplotypes and two previously reported size variants for nad1 intron B/C. Population differentiation was high (GST = 0.657) and the distribution of the mitotypes was geographically highly structured, suggesting at least four genetically distinct ancestral lineages. A cosmopolitan lineage was widely distributed in much of Europe throughout eastern Asia. A previously reported lineage limited to the Iberian Peninsula was confirmed. A new geographically restricted lineage was found confined to Asia Minor. A new lineage was restricted to more northern latitudes in northeastern Europe and the Baltic region.
The contribution of the various ancestral lineages to the current distribution of Scots pine was asymmetric and extant endemism reflected the presence of large geographic barriers to migration. The results suggest a complex biogeographical history with glacial refugia shared with temperate plant species in southern European Peninsulas and Asia Minor, and a genetically distinct glacial population located more North. These results confirm recent observations for cold tolerant species about the possible existence of refugial populations at mid-northern latitudes contributing significantly to the recolonization of northern Europe. Thus, Eurasian populations of nordic plant species might not be as genetically homogenous as assumed by simply considering them as offsets of glacial populations located in southern peninsulas. As such, they might have evolved distinctive genetic adaptations during glacial vicariance, worth evaluating and considering for conservation.
PMCID: PMC2222255  PMID: 18034901
7.  Novel Lignan and Stilbenoid Mixture Shows Anticarcinogenic Efficacy in Preclinical PC-3M-luc2 Prostate Cancer Model 
PLoS ONE  2014;9(4):e93764.
Prostate cancer is the most common cancer of men in the Western world, and novel approaches for prostate cancer risk reduction are needed. Plant-derived phenolic compounds attenuate prostate cancer growth in preclinical models by several mechanisms, which is in line with epidemiological findings suggesting that consumption of plant-based diets is associated with low risk of prostate cancer. The objective of this study was to assess the effects of a novel lignan-stilbenoid mixture in PC-3M-luc2 human prostate cancer cells in vitro and in orthotopic xenografts. Lignan and stilbenoid –rich extract was obtained from Scots pine (Pinus sylvestris) knots. Pine knot extract as well as stilbenoids (methyl pinosylvin and pinosylvin), and lignans (matairesinol and nortrachelogenin) present in pine knot extract showed antiproliferative and proapoptotic efficacy at ≥40 μM concentration in vitro. Furthermore, pine knot extract derived stilbenoids enhanced tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induced apoptosis already at ≥10 μM concentrations. In orthotopic PC-3M-luc2 xenograft bearing immunocompromized mice, three-week peroral exposure to pine knot extract (52 mg of lignans and stilbenoids per kg of body weight) was well tolerated and showed anti-tumorigenic efficacy, demonstrated by multivariate analysis combining essential markers of tumor growth (i.e. tumor volume, vascularization, and cell proliferation). Methyl pinosylvin, pinosylvin, matairesinol, nortrachelogenin, as well as resveratrol, a metabolite of pinosylvin, were detected in serum at total concentration of 7−73 μM, confirming the bioavailability of pine knot extract derived lignans and stilbenoids. In summary, our data indicates that pine knot extract is a novel and cost-effective source of resveratrol, methyl pinosylvin and other bioactive lignans and stilbenoids. Pine knot extract shows anticarcinogenic efficacy in preclinical prostate cancer model, and our in vitro data suggests that compounds derived from the extract may have potential as novel chemosensitizers to TRAIL. These findings promote further research on health-related applications of wood biochemicals.
PMCID: PMC3974786  PMID: 24699425
8.  The oxygen isotope enrichment of leaf-exported assimilates – does it always reflect lamina leaf water enrichment? 
The New Phytologist  2013;200(1):144-157.
The oxygen stable isotope composition of plant organic matter (OM) (particularly of wood and cellulose in the tree ring archive) is valuable in studies of plant–climate interaction, but there is a lack of information on the transfer of the isotope signal from the leaf to heterotrophic tissues.We studied the oxygen isotopic composition and its enrichment above source water of leaf water over diel courses in five tree species covering a broad range of life forms. We tracked the transfer of the isotopic signal to leaf water-soluble OM and further to phloem-transported OM.Observed leaf water evaporative enrichment was consistent with values predicted from mechanistic models taking into account nonsteady-state conditions. While leaf water-soluble OM showed the expected 18O enrichment in all species, phloem sugars were less enriched than expected from leaf water enrichment in Scots pine (Pinus sylvestris), European larch (Larix decidua) and Alpine ash (Eucalyptus delegatensis).Oxygen atom exchange with nonenriched water during phloem loading and transport, as well as a significant contribution of assimilates from bark photosynthesis, can explain these phloem 18O enrichment patterns. Our results indicate species-specific uncoupling between the leaf water and the OM oxygen isotope signal, which is important for the interpretation of tree ring data.
PMCID: PMC3902987  PMID: 23763637
broadleaf; conifer; diel course; oxygen atom exchange; phloem transport
9.  Effects of male fecundity, interindividual distance and anisotropic pollen dispersal on mating success in a Scots pine (Pinus sylvestris) seed orchard 
Heredity  2011;108(3):312-321.
Quantifying the effect of pollen dispersal and flowering traits on mating success is essential for understanding evolutionary responses to changing environments and establishing strategies for forest tree breeding. This study examined, quantitatively, the effects of male fecundity, interindividual distance and anisotropic pollen dispersal on the mating success of Scots pine (Pinus sylvestris), utilizing a well-mapped Scots pine seed orchard. Paternity analysis of 1021 seeds sampled from 87 trees representing 28 clones showed that 53% of the seeds had at least one potential pollen parent within the orchard. Pronounced variation in paternal contribution was observed among clones. Variations in pollen production explained up to 78% of the variation in mating success, which was 11.2 times greater for clones producing the largest amount of pollen than for clones producing the least pollen. Mating success also varied with intertree distance and direction, which explained up to 28% of the variance. Fertilization between neighboring trees 2.3 m apart was 2.4 times more frequent than between trees 4.6 m apart, and up to 12.4 times higher for trees downwind of the presumed prevailing wind direction than for upwind trees. The effective number of pollen donors recorded in the seed orchard (12.2) was smaller than the theoretical expectation (19.7). Based on the empirical observations, a mating model that best describes the gene dispersal pattern in clonal seed orchards was constructed.
PMCID: PMC3282400  PMID: 21897440
anisotropic pollen dispersal; male fecundity; distance effect; mating model; paternity assignment
10.  Tree rings of Scots pine (Pinus sylvestris L.) as a source of information about past climate in northern Poland 
Scots pine (Pinus sylvestris) is a very common tree in Polish forests, and therefore was widely used as timber. A relatively large amount of available wood allowed a long-term chronology to be built up and used as a source of information about past climate. The analysis of reconstructed indexed values of mean temperature in 51-year moving intervals allowed the recognition of the coldest periods in the years 1207–1346, 1383–1425, 1455–1482, 1533–1574, 1627–1646, and 1694–1785. The analysis of extreme wide and narrow rings forms a complementary method of examining climatic data within tree rings. The tree ring widths, early wood and late wood widths of 16 samples were assessed during the period 1581–1676. The most apparent effect is noted in the dry summer of 1616. According to previous research and our findings, temperature from February to March seems to be one of the most stable climatic factors which influenced pine growth in Poland. Correlation coefficients in the calibration and validation procedure gave promising results for temperature reconstruction from the pine chronology.
PMCID: PMC3245383  PMID: 21174127
Dendrochronology; Dendroclimatology; Climate reconstruction; Scots pine
11.  Simultaneous estimation of multiple quantitative trait loci and growth curve parameters through hierarchical Bayesian modeling 
Heredity  2011;108(2):134-146.
A novel hierarchical quantitative trait locus (QTL) mapping method using a polynomial growth function and a multiple-QTL model (with no dependence in time) in a multitrait framework is presented. The method considers a population-based sample where individuals have been phenotyped (over time) with respect to some dynamic trait and genotyped at a given set of loci. A specific feature of the proposed approach is that, instead of an average functional curve, each individual has its own functional curve. Moreover, each QTL can modify the dynamic characteristics of the trait value of an individual through its influence on one or more growth curve parameters. Apparent advantages of the approach include: (1) assumption of time-independent QTL and environmental effects, (2) alleviating the necessity for an autoregressive covariance structure for residuals and (3) the flexibility to use variable selection methods. As a by-product of the method, heritabilities and genetic correlations can also be estimated for individual growth curve parameters, which are considered as latent traits. For selecting trait-associated loci in the model, we use a modified version of the well-known Bayesian adaptive shrinkage technique. We illustrate our approach by analysing a sub sample of 500 individuals from the simulated QTLMAS 2009 data set, as well as simulation replicates and a real Scots pine (Pinus sylvestris) data set, using temporal measurements of height as dynamic trait of interest.
PMCID: PMC3262873  PMID: 21792229
functional mapping; scots pine; QTL; multitrait; Bayesian model; MCMC
12.  Parameter Optimization and Field Validation of the Functional–Structural Model GREENLAB for Maize 
Annals of Botany  2006;97(2):217-230.
• Background and Aims There are three reasons for the increasing demand for crop models that build the plant on the basis of architectural principles and organogenetic processes: (1) realistic concepts for developing new crops need to be guided by such models; (2) there is an increasing interest in crop phenotypic plasticity, based on variable architecture and morphology; and (3) engineering of mechanized cropping systems requires information on crop architecture. The functional–structural model GREENLAB was recently presented that simulates resource-dependent plasticity of plant architecture. This study introduces a new methodology for crop parameter optimization against measured data called multi-fitting, validates the calibrated model for maize with independent field data, and describes a technique for 3D visualization of outputs.
• Methods Maize was grown near Beijing during the 2000, 2001 and 2003 (two sowing dates) summer seasons in a block design with four to five replications. Detailed morphological and topological observations were made on the plant architecture throughout the development of the four crops. Data obtained in 2000 was used to establish target files for parameter optimization using the generalized least square method, and parameter accuracy was evaluated by coefficient of variance. In situ plant digitization was used to establish 3D symbol files for organs that were then used to translate model outputs directly into 3D representations for each time step of model execution.
•Key Results and Conclusions Multi-fitting against several target files obtained at different growth stages gave better parameter accuracy than single fitting at maturity only, and permitted extracting generic organ expansion kinetics from the static observations. The 2000 model gave excellent predictions of plant architecture and vegetative growth for the other three seasons having different temperature regimes, but predictions of inter-seasonal variability of biomass partitioning during grain filling were less accurate. This was probably due to insufficient consideration of processes governing cob sink size and terminal leaf senescence. Further perspectives for model improvement are discussed.
PMCID: PMC2803369  PMID: 16390847
Plant architecture; competition among sinks; source–sink relationships; functional–structural models; Zea mays; model parameterization
13.  Measuring and Simulating Crown Respiration of Scots Pine with Increased Temperature and Carbon Dioxide Enrichment 
Annals of Botany  2002;90(3):325-335.
Acclimation to elevated atmospheric carbon dioxide concentration and temperature of respiration by the foliage in the crown of Scots pine (Pinus sylvestris) trees is measured and modelled. Starting in 1996, individual 20‐year‐old trees were enclosed in chambers and exposed to either normal ambient conditions (CON), elevated CO2 concentration (EC), elevated temperature (ET) or a combination of EC and ET (ECT). Respiration of individual leaves within the crown was measured in 2000. To extrapolate the response of respiration of individual leaves to the whole crown, a multi‐layer model was developed and used to predict daily and annual crown respiration, in which the crown structure and corresponding microclimate data were used as input. Respiration measurements showed that EC led to higher Q10 values (4·6 %) relative to CON, but lower basal respiration rates at 20 °C [Rl.d(20)] (–7·1 %) during the main growth season (days 120–240), whereas ET and ECT both reduced Q10 (–12·0 and –9·8 %, respectively) throughout the year but increased Rl.d(20) (27·2 and 21·6 %, respectively) during the period of no‐growth, and slightly reduced Rl.d(20) (–1·7 and –2·8 %, respectively) during the main growth season. Model computations showed that annual crown respiration increased: (1) by 16 % in EC, with 92 % of this increase attributable to the increase in foliage area; (2) by 35 % in ET, with 66 % related to the increase in foliage area and 17 % to the rise in ambient temperature; and (3) by 27 % in the case of ECT, with 43 % attributable to the increase in foliage area and 29 % to the rise in ambient temperature. Changed respiration parameters for individual leaves, induced by treatments, made only a small contribution to the annual crown respiration compared with the increased foliage area. The effects of changes in crown architecture and nitrogen distribution, caused by treatments, on the daily and annual course of crown respiration are discussed.
PMCID: PMC4240391  PMID: 12234144
Environment‐controlled chambers; CO2 and temperature elevation; crown respiration; simulation; Scots pine
14.  Fluorescence measurements show stronger cold inhibition of photosynthetic light reactions in Scots pine compared to Norway spruce as well as during spring compared to autumn 
We studied the photosynthetic activity of Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies [L.] Karst) in relation to air temperature changes from March 2013 to February 2014. We measured the chlorophyll fluorescence of approximately 50 trees of each species growing in southern Finland. Fluorescence was measured 1–3 times per week. We began by measuring shoots present in late winter (i.e., March 2013) before including new shoots once they started to elongate in spring. By July, when the spring shoots had achieved similar fluorescence levels to the older ones, we proceeded to measure the new shoots only. We analyzed the data by fitting a sigmoidal model containing four parameters to link sliding averages of temperature and fluorescence. A parameter defining the temperature range over which predicted fluorescence increased most rapidly was the most informative with in describing temperature dependence of fluorescence. The model generated similar fluorescence patterns for both species, but differences were observed for critical temperature and needle age. Down regulation of the light reaction was stronger in spring than in autumn. Pine showed more conservative control of the photosynthetic light reactions, which were activated later in spring and more readily attenuated in autumn. Under the assumption of a close correlation of fluorescence and photosynthesis, spruce should therefore benefit more than pine from the increased photosynthetic potential during warmer springs, but be more likely to suffer frost damage with a sudden cooling following a warm period. The winter of 2013–2014 was unusually mild and similar to future conditions predicted by global climate models. During the mild winter, the activity of photosynthetic light reactions of both conifers, especially spruce, remained high. Because light levels during winter are too low for photosynthesis, this activity may translate to a net carbon loss due to respiration.
PMCID: PMC4055857  PMID: 24982664
Scots pine; Norway spruce; photosynthesis; phenology; cold inhibition; climate change; frost tolerance
15.  No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress 
The physiological mechanisms leading to Scots pine (Pinus sylvestris L.) decline in the dry inner Alpine valleys are still unknown. Testing the carbon starvation hypothesis, we analysed the seasonal course of mobile carbohydrate pools (NSC) of Scots pine growing at a xeric and a dry-mesic site within an inner Alpine dry valley (750 m a.s.l., Tyrol, Austria) during the year 2009, which was characterized by exceptional soil dryness. Although, soil moisture content dropped to c. 10% at both sites during the growing season, NSC concentrations were rising in all tissues (branch, stem, root) till end of July, except in needles where maxima were reached around bud break. NSC concentrations were not significantly different in the analysed tissues at the xeric and the dry-mesic site. At the dry-mesic site NSC concentrations in the above ground tree biomass were significantly higher during the period of radial growth. An accumulation of NSC in roots at the end of July indicates a change in carbon allocation after an early cessation in above ground growth, possibly due to elevated below ground carbon demand. In conclusion our results revealed that extensive soil dryness during the growing season did not lead to carbon depletion. However, even though C-reserves were not exhausted, a sequestration of carbohydrate pools during drought periods might lead to deficits in carbon supply that weaken tree vigour and drive tree mortality.
PMCID: PMC3427021  PMID: 21974742
non-structural carbohydrates; Scots pine; drought; dry inner Alpine valley; carbon starvation; tree mortality
16.  Survival and Infectivity of Bursaphelenchus xylophilus in Wood Chip-Soil Mixtures 
Journal of Nematology  1992;24(4):495-503.
To determine the effect of soil environment on the life stages and total numbers of Bursaphelenchus xylophilus, nematode-infested wood chips alone and mixed with soil were incubated at 12 and 20 C. Nematodes were extracted at 2-week intervals for 12 weeks. Numbers of nematodes and percentage of third-stage dispersal larvae were greater at 12 C and in chips without soil. Percentage of juveniles of the propagative cycle was greater at 20 C and in chips with soil. Although B. xylophilus survived in chips with soil for 12 weeks, nematode numbers and life stage percentages changed little over time. To determine if B. xylophilus was capable of infecting wounded roots, infested and uninfested chips were mixed with soil in pots with white and Scots pine seedlings. Trees were maintained at 20 and 30 C and harvested at mortality or after 12 weeks. Only seedlings treated with infested chips contained nematodes. In field experiments, planted seedlings were mulched with infested chips to determine if nematodes would invade basal stem wounds. Among these trees, Scots pine was more susceptible than white or red pines to infection and mortality.
PMCID: PMC2619303  PMID: 19283027
Bursaphelenchus xylophilus; nematode; pine; pinewood nematode; Pinus strobus; P. sylvestris; root; soil; temperature; wood chip
17.  Changes in soil bacterial community triggered by drought-induced gap succession preceded changes in soil C stocks and quality 
Ecology and Evolution  2012;2(12):3016-3031.
The aim of this study was to understand how drought-induced tree mortality and subsequent secondary succession would affect soil bacterial taxonomic composition as well as soil organic matter (SOM) quantity and quality in a mixed Mediterranean forest where the Scots pine (Pinus sylvestris) population, affected by climatic drought-induced die-off, is being replaced by Holm-oaks (HO; Quercus ilex). We apply a high throughput DNA pyrosequencing technique and 13C solid-state Nuclear Magnetic Resonance (CP-MAS 13C NMR) to soils within areas of influence (defined as an surface with 2-m radius around the trunk) of different trees: healthy and affected (defoliated) pines, pines that died a decade ago and healthy HOs. Soil respiration was also measured in the same spots during a spring campaign using a static close-chamber method (soda lime). A decade after death, and before aerial colonization by the more competitive HOs have even taken place, we could not find changes in soil C pools (quantity and/or quality) associated with tree mortality and secondary succession. Unlike C pools, bacterial diversity and community structure were strongly determined by tree mortality. Convergence between the most abundant taxa of soil bacterial communities under dead pines and colonizer trees (HOs) further suggests that physical gap colonization was occurring below-ground before above-ground colonization was taken place. Significantly higher soil respiration rates under dead trees, together with higher bacterial diversity and anomalously high representation of bacteria commonly associated with copiotrophic environments (r-strategic bacteria) further gives indications of how drought-induced tree mortality and secondary succession were influencing the structure of microbial communities and the metabolic activity of soils.
PMCID: PMC3538997  PMID: 23301169
Climate change; drought; ecosystem functioning; forest dieback; gap colonization; microbial diversity; nutrient cycling; pyrosequencing; tree mortality
18.  Duration of shoot elongation in Scots pine varies within the crown and between years 
Annals of Botany  2013;112(6):1181-1191.
Background and Aims
Shoot elongation in boreal and temperate trees typically follows a sigmoid pattern where the onset and cessation of growth are related to accumulated effective temperature (thermal time). Previous studies on leader shoots suggest that while the maximum daily growth rate depends on the availability of resources to the shoot, the duration of the growth period may be an adaptation to long-term temperature conditions. However, other results indicate that the growth period may be longer in faster growing lateral shoots with higher availability of resources. This study investigates the interactions between the rate of elongation and the duration of the growth period in units of thermal time in lateral shoots of Scots pine (Pinus sylvestris).
Length development of 202 lateral shoots were measured approximately three times per week during seven growing seasons in 2–5 trees per year in a mature stand and in three trees during one growing season in a sapling stand. A dynamic shoot growth model was adapted for the analysis to determine (1) the maximum growth rate and (2) the thermal time reached at growth completion. The relationship between those two parameters and its variation between trees and years was analysed using linear mixed models.
Key Results
The shoots with higher maximum growth rate within a crown continued to grow for a longer period in any one year. Higher July–August temperature of the previous summer implied a higher requirement of thermal time for growth completion.
The results provide evidence that the requirement of thermal time for completion of lateral shoot extension in Scots pine may interact with resource availability to the shoot both from year to year and among shoots in a crown each year. If growing season temperatures rise in the future, this will affect not only the rate of shoot growth but its duration also.
PMCID: PMC3783244  PMID: 23985987
Annual course of growth; daily variation in growth; Scots pine; Pinus sylvestris; thermal growth requirement; thermal time; dynamic model; phenology
19.  Seasonal and Annual Stem Respiration of Scots Pine Trees under Boreal Conditions 
Annals of Botany  2004;94(6):889-896.
• Background and Aims Stem respiration of trees is a major, but poorly assessed component of the carbon balance of forests, and important for geo-chemistry. Measurements are required under naturally changing seasonal conditions in different years. Therefore, intra- and inter-annual carbon fluxes of stems in forests were measured continuously from April to November in three consecutive years.
• Methods Stem respiratory CO2 fluxes of 50-year-old Scots pine (Pinus sylvestris) trees were continuously measured with a CO2 analyser, and, concomitantly, stem circumference, stem and air temperature and other environmental factors and photosynthesis, were also measured automatically.
• Key Results There were diurnal, seasonal and inter-annual changes in stem respiration, which peaked at 1600 h during the day and was highest in July. The temperature coefficient of stem respiration (Q10) was greater during the growing season than when growth was slow or had stopped, and more sensitive to temperature in the growing season. The annual Q10 remained relatively constant at about 2 over the three years, while respiration at a reference temperature of 15 °C (R15) was higher in the growing than in the non-growing season (1·09 compared with 0·78 µmol m−2 stem surface s−1), but was similar between the years. Maintenance respiration was 76 %, 82 % and 80 % of the total respiration of 17·46, 17·26 and 19·35 mol m2 stem surface in 2001, 2002 and 2003, respectively. The annual total stem respiration of the stand per unit ground area was 75·97 gC m−2 in 2001 and 74·28 gC m−2 in 2002.
• Conclusions Stem respiration is an important component in the annual carbon balance of a Scots pine stand, contributing 9 % to total carbon loss from the ecosystem and consuming about 8 % of the carbon of the ecosystem gross primary production. Stem (or air) temperature was the most important predictor of stem carbon flux. The magnitude of stem respiration is modified by photosynthesis and tree growth. Solar radiation indirectly affects stem respiration through its effect on photosynthesis.
PMCID: PMC4242285  PMID: 15469943
Stem respiration; Pinus sylvestris; intra- and inter-annual change; Q10; growth respiration; maintenance respiration; carbon balance
20.  Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes? 
A central issue in our understanding of the evolution of the diversity of plant secondary metabolites (PSMs) is whether or not compounds are functional, conferring an advantage to the plant, or non-functional. We examine the hypothesis that the diversity of monoterpene PSMs within a plant species (Scots pine Pinus sylvestris) may be explained by different compounds acting as defences against high-impact herbivores operating at different life stages. We also hypothesize that pairwise coevolution, with uncorrelated interactions, is more likely to result in greater PSM diversity, than diffuse coevolution. We tested whether up to 13 different monoterpenes in Scots pine were inhibitory to herbivory by slugs (Arion ater), bank voles (Clethrionomys glareolus), red deer (Cervus elaphus) and capercaillie (Tetrao urogallus), each of which attack trees at a different life stage. Plants containing more α-pinene were avoided by both slugs and capercaillie, which may act as reinforcing selective agents for this dominant defensive compound. Herbivory by red deer and capercaillie were, respectively, weakly negatively associated with δ3-carene, and strongly negatively correlated with the minor compound β-ocimene. Three of the four herbivores are probably contributory selective agents on some of the terpenes, and thus maintain some, but by no means all, of the phytochemical diversity in the species. The correlated defensive function of α-pinene against slugs and capercaillie is consistent with diffuse coevolutionary processes.
PMCID: PMC3081569  PMID: 21444308
coevolution; diversity; plant secondary metabolites; selection
21.  Nitrogen and Carbon Reallocation in Fungal Mycelia during Decomposition of Boreal Forest Litter 
PLoS ONE  2014;9(3):e92897.
Boreal forests are characterized by spatially heterogeneous soils with low N availability. The decomposition of coniferous litter in these systems is primarily performed by basidiomycete fungi, which often form large mycelia with a well-developed capacity to reallocate resources spatially- an advantageous trait in heterogeneous environments. In axenic microcosm systems we tested whether fungi increase their biomass production by reallocating N between Pinus sylvestris (Scots pine) needles at different stages of decomposition. We estimated fungal biomass production by analysing the accumulation of the fungal cell wall compound chitin. Monospecific systems were compared with systems with interspecific interactions. We found that the fungi reallocated assimilated N and mycelial growth away from well-degraded litter towards fresh litter components. This redistribution was accompanied by reduced decomposition of older litter. Interconnection of substrates increased over-all fungal C use efficiency (i.e. the allocation of assimilated C to biomass rather than respiration), presumably by enabling fungal translocation of growth-limiting N to litter with higher C quality. Fungal connection between different substrates also restricted N-mineralization and production of dissolved organic N, suggesting that litter saprotrophs in boreal forest ecosystems primarily act to redistribute rather than release N. This spatial integration of different resource qualities was hindered by interspecific interactions, in which litters of contrasting quality were colonised by two different basidiomycete species. The experiments provide a detailed picture of how resource reallocation in two decomposer fungi leads to a more efficient utilisation of spatially separated resources under N-limitation. From an ecosystem point of view, such economic fungal behaviour could potentially contribute to organic matter accumulation in the litter layers of boreal forests.
PMCID: PMC3961408  PMID: 24651625
22.  Direct and Indirect Effects of Climate on Demography and Early Growth of Pinus sylvestris at the Rear Edge: Changing Roles of Biotic and Abiotic Factors 
PLoS ONE  2013;8(3):e59824.
Global change triggers shifts in forest composition, with warming and aridification being particularly threatening for the populations located at the rear edge of the species distributions. This is the case of Scots pine (Pinus sylvestris) in the Mediterranean Basin where uncertainties in relation to its dynamics under these changing scenarios are still high. We analysed the relative effect of climate on the recruitment patterns of Scots pine and its interactions with local biotic and abiotic variables at different spatial scales. Number of seedlings and saplings was surveyed, and their annual shoot growth measured in 96 plots located across altitudinal gradients in three different regions in the Iberian Peninsula. We found a significant influence of climate on demography and performance of recruits, with a non-linear effect of temperature on the presence of juveniles, and a positive effect of precipitation on their survival. Abundance of juveniles of P. sylvestris that underwent their first summer drought was skewed towards higher altitudes than the altitudinal mean range of the conspecific adults and the optimum elevation for seedlings' emergence. At local level, light availability did not influence juveniles' density, but it enhanced their growth. Biotic interactions were found between juveniles and the herb cover (competition) and between the number of newly emerged seedlings and shrubs (facilitation). Results also highlighted the indirect effect that climate exerts over the local factors, modulating the interactions with the pre-existing vegetation that were more evident at more stressful sites. This multiscale approach improves our understanding of the dynamics of these marginal populations and some management criteria can be inferred to boost their conservation under the current global warming.
PMCID: PMC3608533  PMID: 23555794
23.  Analysis, pretreatment and enzymatic saccharification of different fractions of Scots pine 
BMC Biotechnology  2014;14:20.
Forestry residues consisting of softwood are a major lignocellulosic resource for production of liquid biofuels. Scots pine, a commercially important forest tree, was fractionated into seven fractions of chips: juvenile heartwood, mature heartwood, juvenile sapwood, mature sapwood, bark, top parts, and knotwood. The different fractions were characterized analytically with regard to chemical composition and susceptibility to dilute-acid pretreatment and enzymatic saccharification.
All fractions were characterized by a high glucan content (38-43%) and a high content of other carbohydrates (11-14% mannan, 2-4% galactan) that generate easily convertible hexose sugars, and by a low content of inorganic material (0.2-0.9% ash). The lignin content was relatively uniform (27-32%) and the syringyl-guaiacyl ratio of the different fractions were within the range 0.021-0.025. The knotwood had a high content of extractives (9%) compared to the other fractions. The effects of pretreatment and enzymatic saccharification were relatively similar, but without pretreatment the bark fraction was considerably more susceptible to enzymatic saccharification.
Since sawn timber is a main product from softwood species such as Scots pine, it is an important issue whether different parts of the tree are equally suitable for bioconversion processes. The investigation shows that bioconversion of Scots pine is facilitated by that most of the different fractions exhibit relatively similar properties with regard to chemical composition and susceptibility to techniques used for bioconversion of woody biomass.
PMCID: PMC3984014  PMID: 24641769
Scots pine; Chemical composition; Dilute-acid pretreatment; Enzymatic saccharification
24.  Odor, gaseous and PM10 emissions from small scale combustion of wood types indigenous to Central Europe 
In this study, we investigated the emissions, including odor, from log wood stoves, burning wood types indigenous to mid-European countries such as Austria, Czech Republic, Hungary, Slovak Republic, Slovenia, Switzerland, as well as Baden-Württemberg and Bavaria (Germany) and South Tyrol (Italy). The investigations were performed with a modern, certified, 8 kW, manually fired log wood stove, and the results were compared to emissions from a modern 9 kW pellet stove. The examined wood types were deciduous species: black locust, black poplar, European hornbeam, European beech, pedunculate oak (also known as “common oak”), sessile oak, turkey oak and conifers: Austrian black pine, European larch, Norway spruce, Scots pine, silver fir, as well as hardwood briquettes. In addition, “garden biomass” such as pine cones, pine needles and dry leaves were burnt in the log wood stove. The pellet stove was fired with softwood pellets.
The composite average emission rates for log wood and briquettes were 2030 mg MJ−1 for CO; 89 mg MJ−1 for NOx, 311 mg MJ−1 for CxHy, 67 mg MJ−1 for particulate matter PM10 and average odor concentration was at 2430 OU m−3. CO, CxHy and PM10 emissions from pellets combustion were lower by factors of 10, 13 and 3, while considering NOx – comparable to the log wood emissions. Odor from pellets combustion was not detectable. CxHy and PM10 emissions from garden biomass (needles and leaves) burning were 10 times higher than for log wood, while CO and NOx rise only slightly. Odor levels ranged from not detectable (pellets) to around 19,000 OU m−3 (dry leaves). The odor concentration correlated with CO, CxHy and PM10. For log wood combustion average odor ranged from 536 OU m−3 for hornbeam to 5217 OU m−3 for fir, indicating a considerable influence of the wood type on odor concentration.
► Study reports emissions from burning of 12 wood types and pellets in modern stoves. ► We examine CO, hydrocarbons (CxHy), PM10 and odor. ► Emissions show high inter-species variability. ► Odor from wood burning is PM10 and CxHy related and is formed mostly during smoldering. ► Pellets burning in an automatically operated stove does not cause odor.
PMCID: PMC3587413  PMID: 23471123
Wood smoke; Odor; Biomass combustion; Particulate emissions; Pellet stove; Log wood stove
25.  Decline and Death of Pinus spp. in Delaware Caused by Bursaphelenchus xylophilus 
Journal of Nematology  1982;14(3):382-385.
Etiological studies to determine the cause of decline and death of Pinus spp. in Delaware were initiated in 1980. The pinewood nematode, Bursaphelenchus xylophilus, was found to be the major canse of mortality in Japanese black pine (Pinus thunbergii). When inoculated into healthy 5-yr-old Japanese black pines, B. xylophilus produced typical decline symptoms observed in the field. The xylophilous fungi most often associated with declining trees, Rhizosphaera pini, Fusarium spp., and Pestalotia funerea, were not pathogenic to Japanese black pine in greenhouse tests. Mineral analyses of soil and foliage showed no significant differences between healthy and infested trees. B. xylolyhilus was also found on loblolly pine (P. taeda), scrub pine (P. virginiana), Scots pine (P. sylvestris), red pine (P. resinosa), Eastern white pine (P. strobus), and pitch pine (P. rigida).
PMCID: PMC2618183  PMID: 19295726
pinewood nematode; Japanese black pine

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