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1.  A meta-analysis of cambium phenology and growth: linear and non-linear patterns in conifers of the northern hemisphere 
Annals of Botany  2013;112(9):1911-1920.
Background and Aims
Ongoing global warming has been implicated in shifting phenological patterns such as the timing and duration of the growing season across a wide variety of ecosystems. Linear models are routinely used to extrapolate these observed shifts in phenology into the future and to estimate changes in associated ecosystem properties such as net primary productivity. Yet, in nature, linear relationships may be special cases. Biological processes frequently follow more complex, non-linear patterns according to limiting factors that generate shifts and discontinuities, or contain thresholds beyond which responses change abruptly. This study investigates to what extent cambium phenology is associated with xylem growth and differentiation across conifer species of the northern hemisphere.
Xylem cell production is compared with the periods of cambial activity and cell differentiation assessed on a weekly time scale on histological sections of cambium and wood tissue collected from the stems of nine species in Canada and Europe over 1–9 years per site from 1998 to 2011.
Key Results
The dynamics of xylogenesis were surprisingly homogeneous among conifer species, although dispersions from the average were obviously observed. Within the range analysed, the relationships between the phenological timings were linear, with several slopes showing values close to or not statistically different from 1. The relationships between the phenological timings and cell production were distinctly non-linear, and involved an exponential pattern
The trees adjust their phenological timings according to linear patterns. Thus, shifts of one phenological phase are associated with synchronous and comparable shifts of the successive phases. However, small increases in the duration of xylogenesis could correspond to a substantial increase in cell production. The findings suggest that the length of the growing season and the resulting amount of growth could respond differently to changes in environmental conditions.
PMCID: PMC3838565  PMID: 24201138
Cambium; cell differentiation; cell production; climate change; conifers; growth; meristem; phenology; productivity; secondary wall formation; xylogenesis
2.  Climatic influences on wood anatomy and tree-ring features of Great Basin conifers at a new mountain observatory1 
Applications in Plant Sciences  2014;2(10):apps.1400054.
• Premise of the study: A network of mountain observing stations has been installed in the Great Basin of North America. NevCAN (Nevada Climate-ecohydrological Assessment Network), which spans a latitudinal range of 2.5° and two elevation ranges of about 2000 m each, enabled us to investigate tree growth in relation to climate.
• Methods: We analyzed wood anatomy and tree-ring characteristics of four conifer species in response to different levels of water availability by comparing a low- and a high-elevation population. Chronologies of earlywood and latewood widths, as well as cellular parameters, were developed from the year 2000 to 2012.
• Results: At the southern (drier and warmer) sites, Pinus monophylla had smaller cell lumen, tracheid diameter, and cell wall thickness. Pinus monophylla and P. flexilis showed bigger cellular elements at the higher elevations, whereas the opposite pattern was found in Picea engelmannii and Pinus longaeva. When all species and sites were pooled together, stem diameter was positively related with earlywood anatomical parameters.
• Discussion: We have provided a glimpse of the applications that NevCAN, as a new scientific tool, could allow in the general field of botany. In particular, we were able to investigate how differences in water stress related to elevation lead to changes in xylem anatomy.
PMCID: PMC4189497  PMID: 25309838
elevation-latitude gradients; NevCAN; Picea engelmannii; Pinus flexilis; Pinus longaeva; Pinus monophylla; tracheid size
3.  The bud break process and its variation among local populations of boreal black spruce 
Phenology of local populations can exhibit adaptations to the current environmental conditions resulting from a close interaction between climate and genotype. The bud break process and its variations among populations were analyzed in greenhouse by monitoring the growth resumption in black spruce [Picea mariana (Mill.) BSP] seedlings originating from seeds of five stands across the closed boreal forest in Quebec, Canada. Bud break lasted 15 days and occurred earlier and quicker in northern provenances. Provenance explained between 10.2 and 32.3% of the variance in bud break, while the families accounted for a smaller but still significant part of the variance. The late occurrence of one phenological phase corresponded to a delayed occurrence of the others according to linear relationships. A causal model was proposed in the form of a chain of events with each phase of bud break being related to the previous and successive one, while no link was observed between non-adjacent phases. The adaptation of black spruce populations along the latitudinal gradient points toward a strategy based on rapid physiological processes triggered by temperature increase inducing high metabolic activity. The variation observed in bud break reflects an evolutionary trade-off between maximization of security and taking advantage of the short growing season. This work provides evidence of the phenological adaptations of black spruce to its local environmental conditions while retaining sizeable genetic diversity within populations. Because of the multigenic nature of phenology, this diversity should provide some raw material for adaptation to changing local environmental conditions.
PMCID: PMC4211384  PMID: 25389430
adaptation; cold climate; genecology; genetic diversity; phenology; temperature
4.  Duration of xylogenesis in black spruce lengthened between 1950 and 2010 
Annals of Botany  2012;110(6):1099-1108.
Background and Aims
Reconstructions have identified the 20th century as being uniquely warm in the last 1000 years. Changes in the phenology of primary meristems converged toward increases in length of the growing season. Has the phenology of secondary meristem changed during the last century, and to what extent?
Timings of wood formation in black spruce, Picea mariana, were monitored for 9 years on a weekly timescale at four sites in the boreal forest of Quebec, Canada. Models for assessing xylem phenology were defined and applied to reconstruct onset, ending and duration of xylogenesis between 1950 and 2010 using thermal thresholds on chronologies of maximum and minimum temperatures.
Key Results
All sites exhibited increasing trends of both annual and May–September temperatures, with the greatest changes observed at the higher latitudes. Phenological events in spring were more affected than those occurring in autumn, with cambial resumptions occurring 0·5–0·8 d decade−1 earlier. The duration of xylogenesis has lengthened significantly since 1950, although the models supplied wide ranges of variations, between 0·07 and 1·5 d decade−1, respectively.
The estimated changes in past cambial phenology demonstrated the marked effects of the recent increase in temperature on the phenological traits of secondary meristems. In the long run, the advancement of cambial activity could modify the short time window for growth of boreal species and dramatically affect the dynamics and productivity of trees in these temperature-limited ecosystems.
PMCID: PMC3478046  PMID: 23041380
boreal forest; cell differentiation; Picea mariana; threshold temperature; wood formation; xylogenesis
5.  Cambial activity related to tree size in a mature silver-fir plantation 
Annals of Botany  2011;108(3):429-438.
Background and Aims
Our knowledge about the influences of environmental factors on tree growth is principally based on the study of dominant trees. However, tree social status may influence intra-annual dynamics of growth, leading to differential responses to environmental conditions. The aim was to determine whether within-stand differences in stem diameters of trees belonging to different crown classes resulted from variations in the length of the growing period or in the rate of cell production.
Cambial activity was monitored weekly in 2006 for three crown classes in a 40-year-old silver-fir (Abies alba) plantation near Nancy (France). Timings, duration and rate of tracheid production were assessed from anatomical observations of the developing xylem.
Key Results
Cambial activity started earlier, stopped later and lasted longer in dominant trees than in intermediate and suppressed ones. The onset of cambial activity was estimated to have taken 3 weeks to spread to 90 % of the trees in the stand, while the cessation needed 6 weeks. Cambial activity was more intense in dominant trees than in intermediate and suppressed ones. It was estimated that about 75 % of tree-ring width variability was attributable to the rate of cell production and only 25 % to its duration. Moreover, growth duration was correlated to tree height, while growth rate was better correlated to crown area.
These results show that, in a closed conifer forest, stem diameter variations resulted principally from differences in the rate of xylem cell production rather than in its duration. Tree size interacts with environmental factors to control the timings, duration and rate of cambial activity through functional processes involving source–sink relationships principally, but also hormonal controls.
PMCID: PMC3158687  PMID: 21816842
Cambial activity; forest-stand structure; silver fir (Abies alba); tree-ring formation; tree-to-tree competition; social status; wood anatomy; xylem cell differentiation
6.  Causes and correlations in cambium phenology: towards an integrated framework of xylogenesis 
Journal of Experimental Botany  2011;63(5):2117-2126.
Although habitually considered as a whole, xylogenesis is a complex process of division and maturation of a pool of cells where the relationship between the phenological phases generating such a growth pattern remains essentially unknown. This study investigated the causal relationships in cambium phenology of black spruce [Picea mariana (Mill.) BSP] monitored for 8 years on four sites of the boreal forest of Quebec, Canada. The dependency links connecting the timing of xylem cell differentiation and cell production were defined and the resulting causal model was analysed with d-sep tests and generalized mixed models with repeated measurements, and tested with Fisher’s C statistics to determine whether and how causality propagates through the measured variables. The higher correlations were observed between the dates of emergence of the first developing cells and between the ending of the differentiation phases, while the number of cells was significantly correlated with all phenological phases. The model with eight dependency links was statistically valid for explaining the causes and correlations between the dynamics of cambium phenology. Causal modelling suggested that the phenological phases involved in xylogenesis are closely interconnected by complex relationships of cause and effect, with the onset of cell differentiation being the main factor directly or indirectly triggering all successive phases of xylem maturation.
PMCID: PMC3295399  PMID: 22174441
Causal modelling; cell differentiation; cell production; d-sep test; Picea mariana; secondary wall formation; xylogenesis
7.  Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem 
Journal of Experimental Botany  2011;63(2):837-845.
The diameter of vascular conduits increases towards the stem base. It has been suggested that this profile is an efficient anatomical feature for reducing the hydraulic resistance when trees grow taller. However, the mechanism that controls the cell diameter along the plant is not fully understood. The timing of cell differentiation along the stem was investigated. Cambial activity and cell differentiation were investigated in a Picea abies tree (11.5 m in height) collecting microsamples at nine different heights (from 1 to 9 m) along the stem with a 4 d time interval. Wood sections (8–12 μm thick) were stained and observed under a light microscope with polarized light to differentiate the developing xylem cells. Cell wall lignification was detected using cresyl violet acetate. The first enlarging cells appeared almost simultaneously along the tree axis indicating that cambium activation is not height-dependent. A significant increase in the duration of the cell expansion phase was observed towards the tree base: at 9 m from the ground, xylem cells expanded for 7 d, at 6 m for 14 d, and at 3 m for 19 d. The duration of the expansion phase is positively correlated with the lumen area of the tracheids (r2=0.68, P < 0.01) at the same height. By contrast, thickness of the cell wall of the earlywood did not show any trend with height. The lumen area of the conduits down the stem appeared linearly dependent on time during which differentiating cells remained in the expansion phase. However, the inductive signal of such long-distance patterned differentiation remains to be identified.
PMCID: PMC3254684  PMID: 22016427
Auxin; cambium; cell differentiation; conduit tapering; Picea abies polar pattern growth
8.  Dynamics of Depletion and Replenishment of Water Storage in Stem and Roots of Black Spruce Measured by Dendrometers 
In the short term, trees rely on the internal storage of water because it affects their ability to sustain photosynthesis and growth. However, water is not rapidly available for transpiration from all the compartments of the plant and the living tissues of the stem act as a buffer to preclude low water potentials during peaks of transpiration. In this paper, electronic dendrometers were used from mid-June to mid-September 2008 to compare the radius variations in stem and roots of black spruce [Picea mariana (Mill.) B.S.P.] in two sites of the boreal forest of Quebec, Canada, with different soil characteristics and water retention. The duration of the daily cycles was similar between sites and measurement heights but greater amplitudes of contraction and expansion were observed on the stem and in the site with the shallowest soil organic layer. The expansion phase had higher amplitudes and lasted longer than contraction. On average, the contraction phase occurred between 07:00 and 16:30 (legal time), while expansion lasted 14.5 h. The roots in the site with the deepest organic layer showed a wider variation in the onset of contraction, which could be as late as 13:00. The probability of observing the contraction phase depended on precipitation. With a precipitation <0.5 mm h−1, the bivariate posterior probabilities estimated >60% probability of observing contraction between 05:00 and 21:00, decreasing to 20% with precipitation >1.1 mm h−1. These findings demonstrated that the depth of the organic layer plays an important role in maintaining the internal water reserve of trees. The dynamics of water depletion and replenishment can modify the water potential of xylem and cell turgor during the enlargement phase, thus affecting radial growth. Changes in temperature and precipitation regime could influence the dynamics of internal water storage in trees growing on shallower and drier soils.
PMCID: PMC3355585  PMID: 22639583
boreal forest; climate change; stem cycle approach; plant–water relationships; soil depth; water reserves
9.  Cambial Activity and Intra-annual Xylem Formation in Roots and Stems of Abies balsamea and Picea mariana 
Annals of Botany  2008;102(5):667-674.
Background and Aims
Studies on xylogenesis focus essentially on the stem, whereas there is basically no information about the intra-annual growth of other parts of the tree. As roots strongly influence carbon allocation and tree development, knowledge of the dynamics of xylem production and maturation in roots at a short time scale is required for a better understanding of the phenomenon of tree growth. This study compared cambial activity and xylem formation in stem and roots in two conifers of the boreal forest in Canada.
Wood microcores were collected weekly in stem and roots of ten Abies balsamea and ten Picea mariana during the 2004–2006 growing seasons. Cross-sections were cut using a rotary microtome, stained with cresyl violet acetate and observed under visible and polarized light. The number of cells in the cambial zone and in differentiation, plus the number of mature cells, was counted along the developing xylem.
Key Results
Xylem formation lasted from the end of May to the end of September, with no difference between stem and roots in 2004–2005. On the contrary, in 2006 a 1-week earlier beginning of cell differentiation was observed in the stem, with cell wall thickening and lignification in roots ending up to 22 d later than in the stem. Cell production in the stem was concentrated early in the season, in June, while most cell divisions in roots occurred 1 month later.
The intra-annual dynamics of growth observed in stem and roots could be related to the different amount of cells produced by the cambium and the patterns of air and soil temperature occurring in spring.
PMCID: PMC2712372  PMID: 18708643
Abies balsamea; boreal forest; cambium; cell differentiation; cell wall thickening; lignification; Picea mariana; root; stem; xylem
10.  Glucose determination by means of steady-state and time-course UV fluorescence in free or immobilized Glucose Oxidase 
Sensors (Basel, Switzerland)  2007;7(11):2612-2625.
Changes in steady-state UV fluorescence emission from free or immobilized glucose oxidase have been investigated as a function of glucose concentration. Immobilized GOD has been obtained by entrapment into a gelatine membrane. Changes in steady-state UV fluorescence have been quantitatively characterized by means of optokinetic parameters and their values have been compared with those previously obtained for FAD fluorescence in the visible range. The results confirmed that greater calibration ranges are obtained from UV signals both for free and immobilized GOD in respect to those obtained under visible fluorescence excitation. An alternative method to the use UV fluorescence for glucose determination has been investigated by using time course measurements for monitoring the differential fluorescence of the redox forms of the FAD in GOD. Also in this case quantitative analysis have been carried out and a comparison with different experimental configurations has been performed. Time coarse measurements could be particularly useful for glucose monitoring in complex biological fluids in which the intrinsic UV fluorescence of GOD could be not specific by considering the presence of numerous proteins.
PMCID: PMC3965247
Glucose Oxidase; Glucose Concentration Determination; Immobilized enzymes; Emission fluorescence spectra; Biosensors

Results 1-10 (10)