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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.
doi:10.1371/journal.pone.0043531
PMCID: PMC3425476  PMID: 22927982
2.  Activation of defence pathways in Scots pine bark after feeding by pine weevil (Hylobius abietis) 
BMC Genomics  2015;16(1):352.
Background
During their lifetime, conifer trees are exposed to numerous herbivorous insects. To protect themselves against pests, trees have developed a broad repertoire of protective mechanisms. Many of the plant’s defence reactions are activated upon an insect attack, and the underlying regulatory mechanisms are not entirely understood yet, in particular in conifer trees. Here, we present the results of our studies on the transcriptional response and the volatile compounds production of Scots pine (Pinus sylvestris) upon the large pine weevil (Hylobius abietis) feeding.
Results
Transcriptional response of Scots pine to the weevil attack was investigated using a novel customised 36.4 K Pinus taeda microarray. The weevil feeding caused large-scale changes in the pine transcriptome. In total, 774 genes were significantly up-regulated more than 4-fold (p ≤ 0.05), whereas 64 genes were significantly down-regulated more than 4-fold. Among the up-regulated genes, we could identify genes involved in signal perception, signalling pathways, transcriptional regulation, plant hormone homeostasis, secondary metabolism and defence responses. The weevil feeding on stem bark of pine significantly increased the total emission of volatile organic compounds from the undamaged stem bark area. The emission levels of monoterpenes and sesquiterpenes were also increased. Interestingly, we could not observe any correlation between the increased production of the terpenoid compounds and expression levels of the terpene synthase-encoding genes.
Conclusions
The obtained data provide an important insight into the transcriptional response of conifer trees to insect herbivory and illustrate the massive changes in the host transcriptome upon insect attacks. Moreover, many of the induced pathways are common between conifers and angiosperms. The presented results are the first ones obtained by the use of a microarray platform with an extended coverage of pine transcriptome (36.4 K cDNA elements). The platform will further facilitate the identification of resistance markers with the direct relevance for conifer tree breeding.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1546-9) contains supplementary material, which is available to authorized users.
doi:10.1186/s12864-015-1546-9
PMCID: PMC4422480  PMID: 25943104
Herbivory; VOC emission; Transcriptomics; Phenylpropanoid pathway; Terpenoid pathway; Protease inhibitors; PR proteins
3.  Limited Growth Recovery after Drought-Induced Forest Dieback in Very Defoliated Trees of Two Pine Species 
Mediterranean pine forests display high resilience after extreme climatic events such as severe droughts. However, recent dry spells causing growth decline and triggering forest dieback challenge the capacity of some forests to recover following major disturbances. To describe how resilient the responses of forests to drought can be, we quantified growth dynamics in plantations of two pine species (Scots pine, black pine) located in south-eastern Spain and showing drought-triggered dieback. Radial growth was characterized at inter- (tree-ring width) and intra-annual (xylogenesis) scales in three defoliation levels. It was assumed that the higher defoliation the more negative the impact of drought on tree growth. Tree-ring width chronologies were built and xylogenesis was characterized 3 years after the last severe drought occurred. Annual growth data and the number of tracheids produced in different stages of xylem formation were related to climate data at several time scales. Drought negatively impacted growth of the most defoliated trees in both pine species. In Scots pine, xylem formation started earlier in the non-defoliated than in the most defoliated trees. Defoliated trees presented the shortest duration of the radial-enlargement phase in both species. On average the most defoliated trees formed 60% of the number of mature tracheids formed by the non-defoliated trees in both species. Since radial enlargement is the xylogenesis phase most tightly related to final growth, this explains why the most defoliated trees grew the least due to their altered xylogenesis phases. Our findings indicate a very limited resilience capacity of drought-defoliated Scots and black pines. Moreover, droughts produce legacy effects on xylogenesis of highly defoliated trees which could not recover previous growth rates and are thus more prone to die.
doi:10.3389/fpls.2016.00418
PMCID: PMC4817349  PMID: 27066053
dendroecology; die-off; extreme climate event; forest resilience; Pinus nigra; Pinus sylvestris; xylem; xylogenesis
4.  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.
Background
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).
Results
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.
Conclusions
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.
doi:10.1186/1471-2229-12-76
PMCID: PMC3432013  PMID: 22646756
5.  Selectivity of Pinus sylvestris extract and essential oil to estrogen-insensitive breast cancer cells Pinus sylvestris against cancer cells 
Pharmacognosy Magazine  2015;11(Suppl 2):S290-S295.
Background:
So far, the anticancer action of pine tree extracts has mainly been shown for the species distributed widely around the Asian countries.
Objective:
Therefore, this study was performed to examine the potential cytotoxicity of Scots pine (Pinus sylvestris L.) native also to the European region and growing widely in Estonia.
Materials and Methods:
The cytotoxic activity of methanol extract and essential oil of Scots pine needles was determined by sulforhodamine B assay in different human cancer cell lines.
Results:
This needle extract was found to suppress the viability of several human cancer cell lines showing some selectivity to estrogen receptor negative breast cancer cells, MDA-MB-231(half maximal inhibitory concentration [IC50] 35 μg/ml) in comparison with estrogen receptor-positive breast cancer cells, MCF-7 (IC50 86 μg/ml). It is the strongest cytotoxic effect at all measured, thus far for the needles and leaves extracts derived from various pine species, and is also the first study comparing the anticancer effects of pine tree extracts on molecularly different human breast cancer cells. The essential oil showed the stronger cytotoxic effect to both negative and positive breast cancer cell lines (both IC50 29 μg/ml) than pine extract (IC50 42 and 80 μg/ml, respectively).
Conclusion:
The data from this report indicate that Scots pine needles extract and essential oil exhibits some potential as chemopreventive or chemotherapeutic agent for mammary tumors unresponsive to endocrine treatment.
doi:10.4103/0973-1296.166052
PMCID: PMC4653339  PMID: 26664017
Anticancer effect; mammary adenocarcinoma; pine extract; pine oil; Pinus sylvestris
6.  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.
doi:10.1371/journal.pone.0096321
PMCID: PMC4011741  PMID: 24802642
7.  Quantitative characterization of clumping in Scots pine crowns 
Annals of Botany  2014;114(4):689-694.
Background and Aims
Proper characterization of the clumped structure of forests is needed for calculation of the absorbed radiation and photosynthetic production by a canopy. This study examined the dependency of crown-level clumping on tree size and growth conditions in Scots pine (Pinus sylvestris), and determined the ability of statistical canopy radiation models to quantify the degree of self-shading within crowns as a result of the clumping effect.
Methods
Twelve 3-D Scots pine trees were generated using an application of the LIGNUM model, and the crown-level clumping as quantified by the crown silhouette to total needle area ratio (STARcrown) was calculated. The results were compared with those produced by the stochastic approach of modelling tree crowns as geometric shapes filled with a random medium.
Key Results
Crown clumping was independent of tree height, needle area and growth conditions. The results supported the capability of the stochastic approach in characterizing clumping in crowns given that the outer shell of the tree crown is well represented.
Conclusions
Variation in the whole-stand clumping index is induced by differences in the spatial pattern of trees as a function of, for example, stand age rather than by changes in the degree of self-shading within individual crowns as they grow bigger.
doi:10.1093/aob/mct310
PMCID: PMC4156115  PMID: 24431344
Functional–structural modelling; Pinus sylvestris; radiation; clumping; STAR; crown shape; crown structure
8.  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.
doi:10.1007/s11356-013-2081-3
PMCID: PMC3906555  PMID: 24043503
Genetic variation; Heavy metal; Enzymes; Pinus nigra; Pinus sylvestris; Reference plant
9.  Bursts of CO2 released during freezing offer a new perspective on avoidance of winter embolism in trees 
Annals of Botany  2014;114(8):1711-1718.
Background and Aims
Woody plants can suffer from winter embolism as gas bubbles are formed in the water-conducting conduits when freezing occurs: gases are not soluble in ice, and the bubbles may expand and fill the conduits with air during thawing. A major assumption usually made in studies of winter embolism formation is that all of the gas dissolved in the xylem sap is trapped within the conduits and forms bubbles during freezing. The current study tested whether this assumption is actually valid, or whether efflux of gases from the stem during freezing reduces the occurrence of embolism.
Methods
CO2 efflux measurements were conducted during freezing experiments for saplings of three Scots pine (Pinus sylvestris) and three Norway spruce (Picea abies) trees under laboratory conditions, and the magnitudes of the freezing-related bursts of CO2 released from the stems were analysed using a previously published mechanistic model of CO2 production, storage, diffusion and efflux from a tree stem. The freezing-related bursts of CO2 released from a mature Scots pine tree growing in field conditions were also measured and analysed.
Key Results
Substantial freezing-related bursts of CO2 released from the stem were found to occur during both the laboratory experiments and under field conditions. In the laboratory, the fraction of CO2 released from the stem ranged between 27 and 96 % of the total CO2 content within the stem.
Conclusions
All gases dissolved in the xylem sap are not trapped within the ice in the stem during freezing, as has previously been assumed, thus adding a new dimension to the understanding of winter embolism formation. The conduit water volume not only determines the volume of bubbles formed during freezing, but also the efficiency of gas efflux out of the conduit during the freezing process.
doi:10.1093/aob/mcu190
PMCID: PMC4649691  PMID: 25252688
Bubble formation; cavitation; CO2 efflux; freezing propagation; Norway spruce; Picea abies; Pinus sylvestris; Scots pine; winter embolism; wood respiration
10.  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.
doi:10.1038/srep05135
PMCID: PMC4038807  PMID: 24875794
11.  Dynamics of leaf gas exchange, xylem and phloem transport, water potential and carbohydrate concentration in a realistic 3-D model tree crown 
Annals of Botany  2014;114(4):653-666.
Background and Aims
Tree models simulate productivity using general gas exchange responses and structural relationships, but they rarely check whether leaf gas exchange and resulting water and assimilate transport and driving pressure gradients remain within acceptable physical boundaries. This study presents an implementation of the cohesion–tension theory of xylem transport and the Münch hypothesis of phloem transport in a realistic 3-D tree structure and assesses the gas exchange and transport dynamics.
Methods
A mechanistic model of xylem and phloem transport was used, together with a tested leaf assimilation and transpiration model in a realistic tree architecture to simulate leaf gas exchange and water and carbohydrate transport within an 8-year-old Scots pine tree. The model solved the dynamics of the amounts of water and sucrose solute in the xylem, cambium and phloem using a fine-grained mesh with a system of coupled ordinary differential equations.
Key Results
The simulations predicted the observed patterns of pressure gradients and sugar concentration. Diurnal variation of environmental conditions influenced tree-level gradients in turgor pressure and sugar concentration, which are important drivers of carbon allocation. The results and between-shoot variation were sensitive to structural and functional parameters such as tree-level scaling of conduit size and phloem unloading.
Conclusions
Linking whole-tree-level water and assimilate transport, gas exchange and sink activity opens a new avenue for plant studies, as features that are difficult to measure can be studied dynamically with the model. Tree-level responses to local and external conditions can be tested, thus making the approach described here a good test-bench for studies of whole-tree physiology.
doi:10.1093/aob/mcu068
PMCID: PMC4156122  PMID: 24854169
Functional–structural plant modelling; functional–structural plant models; Scots pine; Pinus sylvestris; long-distance transport; turgor; xylem tension; unloading; structure; LIGNUM; phloem transport; 3-D model; tree crown; canopy gas exchange
12.  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 
Background
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.
Results
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.
Conclusion
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.
doi:10.1186/1471-2148-7-233
PMCID: PMC2222255  PMID: 18034901
13.  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.
doi:10.1007/s00484-010-0390-5
PMCID: PMC3245383  PMID: 21174127
Dendrochronology; Dendroclimatology; Climate reconstruction; Scots pine
14.  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.
doi:10.1371/journal.pone.0093764
PMCID: PMC3974786  PMID: 24699425
15.  Assessing Conifer Ray Parenchyma for Ecological Studies: Pitfalls and Guidelines 
Ray parenchyma is an essential tissue for tree functioning and survival. This living tissue plays a major role for storage and transport of water, nutrients, and non-structural carbohydrates (NSC), thus regulating xylem hydraulics and growth. However, despite the importance of rays for tree carbon and water relations, methodological challenges hamper knowledge about ray intra- and inter-tree variability and its ecological meaning. In this study we provide a methodological toolbox for soundly quantifying spatial and temporal variability of different ray features. Anatomical ray features were surveyed in different cutting planes (cross-sectional, tangential, and radial) using quantitative image analysis on stem-wood micro-sections sampled from 41 mature Scots pines (Pinus sylvestris). The percentage of ray surface (PERPAR), a proxy for ray volume, was compared among cutting planes and between early- and latewood to assess measurement-induced variability. Different tangential ray metrics were correlated to assess their similarities. The accuracy of cross-sectional and tangential measurements for PERPAR estimates as a function of number of samples and the measured wood surface was assessed using bootstrapping statistical technique. Tangential sections offered the best 3D insight of ray integration into the xylem and provided the most accurate estimates of PERPAR, with 10 samples of 4 mm2 showing an estimate within ±6.0% of the true mean PERPAR (relative 95% confidence interval, CI95), and 20 samples of 4 mm2 showing a CI95 of ±4.3%. Cross-sections were most efficient for establishment of time series, and facilitated comparisons with other widely used xylem anatomical features. Earlywood had significantly lower PERPAR (5.77 vs. 6.18%) and marginally fewer initiating rays than latewood. In comparison to tangential sections, PERPAR was systematically overestimated (6.50 vs. 4.92%) and required approximately twice the sample area for similar accuracy. Radial cuttings provided the least accurate PERPAR estimates. This evaluation of ray parenchyma in conifers and the presented guidelines regarding data accuracy as a function of measured wood surface and number of samples represent an important methodological reference for ray quantification, which will ultimately improve the understanding of the fundamental role of ray parenchyma tissue for the performance and survival of trees growing in stressed environments.
doi:10.3389/fpls.2015.01016
PMCID: PMC4649045  PMID: 26635842
cutting plane; measured wood surface; measurement accuracy; non-structural carbohydrates (NSC); number of samples; ray density; ray dimensions; ray volume
16.  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.
doi:10.1111/nph.12359
PMCID: PMC3902987  PMID: 23763637
broadleaf; conifer; diel course; oxygen atom exchange; phloem transport
17.  Impregnation of Scots pine and beech with tannin solutions: effect of viscosity and wood anatomy in wood infiltration 
Wood Science and Technology  2013;47(3):615-626.
The impregnation process of Scots pine and beech samples with tannin solutions was investigated. The two materials involved in the process (impregnation solution and wood samples) are studied in depth. Viscosity of mimosa tannin solutions and the anatomical aspect of beech and Scots pine were analysed and correlated. The viscosity of tannin solutions presents a non-newtonian behaviour when its pH level increases, and in the case of addition of hexamine as a hardener, the crosslinking of the flavonoids turns out to be of great importance. During the impregnation of Scots pine (Pinus sylvestris L.) and beech (Fagus sylvatica L.), the liquid and solid uptakes were monitored while taking into consideration the different conditions of the impregnation process. This method allowed to identify the best conditions needed in order to get a successful preservative uptake for each wooden substrate. The penetration mechanism within the wood of both species was revealed with the aid of a microscopic analysis. Scots pine is impregnated through the tracheids in the longitudinal direction and through parenchyma rays in the radial direction, whereas in beech, the penetration occurs almost completely through longitudinal vessels.
doi:10.1007/s00226-012-0524-5
PMCID: PMC4560084  PMID: 26366019
18.  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.
doi:10.1038/hdy.2011.76
PMCID: PMC3282400  PMID: 21897440
anisotropic pollen dispersal; male fecundity; distance effect; mating model; paternity assignment
19.  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.
doi:10.1002/ece3.409
PMCID: PMC3538997  PMID: 23301169
Climate change; drought; ecosystem functioning; forest dieback; gap colonization; microbial diversity; nutrient cycling; pyrosequencing; tree mortality
20.  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).
Methods
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.
Conclusions
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.
doi:10.1093/aob/mct180
PMCID: PMC3783244  PMID: 23985987
Annual course of growth; daily variation in growth; Scots pine; Pinus sylvestris; thermal growth requirement; thermal time; dynamic model; phenology
21.  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.
doi:10.1093/aob/mch218
PMCID: PMC4242285  PMID: 15469943
Stem respiration; Pinus sylvestris; intra- and inter-annual change; Q10; growth respiration; maintenance respiration; carbon balance
22.  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.
doi:10.1093/aob/mcj033
PMCID: PMC2803369  PMID: 16390847
Plant architecture; competition among sinks; source–sink relationships; functional–structural models; Zea mays; model parameterization
23.  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.
doi:10.1038/hdy.2011.56
PMCID: PMC3262873  PMID: 21792229
functional mapping; scots pine; QTL; multitrait; Bayesian model; MCMC
24.  SCoT: a Python toolbox for EEG source connectivity 
Analysis of brain connectivity has become an important research tool in neuroscience. Connectivity can be estimated between cortical sources reconstructed from the electroencephalogram (EEG). Such analysis often relies on trial averaging to obtain reliable results. However, some applications such as brain-computer interfaces (BCIs) require single-trial estimation methods. In this paper, we present SCoT—a source connectivity toolbox for Python. This toolbox implements routines for blind source decomposition and connectivity estimation with the MVARICA approach. Additionally, a novel extension called CSPVARICA is available for labeled data. SCoT estimates connectivity from various spectral measures relying on vector autoregressive (VAR) models. Optionally, these VAR models can be regularized to facilitate ill posed applications such as single-trial fitting. We demonstrate basic usage of SCoT on motor imagery (MI) data. Furthermore, we show simulation results of utilizing SCoT for feature extraction in a BCI application. These results indicate that CSPVARICA and correct regularization can significantly improve MI classification. While SCoT was mainly designed for application in BCIs, it contains useful tools for other areas of neuroscience. SCoT is a software package that (1) brings combined source decomposition and connectivtiy estimation to the open Python platform, and (2) offers tools for single-trial connectivity estimation. The source code is released under the MIT license and is available online at github.com/SCoT-dev/SCoT.
doi:10.3389/fninf.2014.00022
PMCID: PMC3949292  PMID: 24653694
electroencephalogram; connectivity; Python; single-trial; brain-computer interface
25.  Short Delay in Timing of Emergence Determines Establishment Success in Pinus sylvestris across Microhabitats 
Annals of Botany  2006;98(6):1233-1240.
• Background and Aims The date of emergence may have far-reaching implications for seedling performance. Seedlings emerging early in the growing season often have a greater rate of survival or grow better if early emergence provides advantages with respect to an environmental cue. As a result, the benefits of early emergence may be lost if the environmental stress creating the differences among cohorts disappears. The experimental manipulation under field conditions of the factors that constitute the main sources of stress for seedling establishment is thus a straightforward method to evaluate the impact of date of emergence on seedling establishment under realistic conditions.
• Methods Two field experiments were performed to analyse the effect of emergence date on survival and first-year growth of Scots pine seedlings in natural mountain forests in south-east Spain. Two main environmental factors that determine seedling success in these mountains were considered: (1) microhabitat type (monitoring the effect of date of emergence in the three most common microhabitats where seedlings recruit); (2) summer drought (monitored by an irrigation treatment with control and watered sampling points).
• Key Results Overall, early emergence resulted in a higher probability of survival and better growth in the two experiments and across microhabitats. However, the reduction in summer drought did not diminish the differences observed among cohorts: all cohorts increased their survival and growth, but early cohorts still had a clear advantage.
• Conclusions Date of emergence determines establishment success of Pinus sylvestris seedlings, even if cohorts are separated by only a few days, irrespective of the intensity of summer drought. The experimental design, covering a gradient of light intensity and soil moisture that simulates conditions of the regeneration niche of Scots pine across its geographical range, allows the results to be extrapolated to other areas of the species. Date of emergence is thus likely to have a large impact on the demography of Scots pine across its geographical range.
doi:10.1093/aob/mcl208
PMCID: PMC2803580  PMID: 17056614
Cohort effects; cohort of emergence; date of emergence; delayed emergence; irrigation experiments; Pinus sylvestris; seedling establishment; Sierra Nevada National Park; summer drought

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