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1.  Impact of warming and drought on carbon balance related to wood formation in black spruce 
Annals of Botany  2014;114(2):335-345.
Background and Aims
Wood formation in trees represents a carbon sink that can be modified in the case of stress. The way carbon metabolism constrains growth during stress periods (high temperature and water deficit) is now under debate. In this study, the amounts of non-structural carbohydrates (NSCs) for xylogenesis in black spruce, Picea mariana, saplings were assessed under high temperature and drought in order to determine the role of sugar mobilization for osmotic purposes and its consequences for secondary growth.
Four-year-old saplings of black spruce in a greenhouse were subjected to different thermal conditions with respect to the outside air temperature (T0) in 2010 (2 and 5 °C higher than T0) and 2011 (6 °C warmer than T0 during the day or night) with a dry period of about 1 month in June of each year. Wood formation together with starch, NSCs and leaf parameters (water potential and photosynthesis) were monitored from May to September.
Key Results
With the exception of raffinose, the amounts of soluble sugars were not modified in the cambium even if gas exchange and photosynthesis were greatly reduced during drought. Raffinose increased more than pinitol under a pre-dawn water potential of less than –1 Mpa, presumably because this compound is better suited than polyol for replacing water and capturing free radicals, and its degradation into simple sugar is easier. Warming decreased the starch storage in the xylem as well the available hexose pool in the cambium and the xylem, probably because of an increase in respiration.
Radial stem growth was reduced during drought due to the mobilization of NSCs for osmotic purposes and due to the lack of cell turgor. Thus plant water status during wood formation can influence the NSCs available for growth in the cambium and xylem.
PMCID: PMC4111389  PMID: 24950772
Cambium; black spruce; Picea mariana; drought; non-structural carbohydrate; soluble sugars; raffinose; starch; global warming; climate change; wood formation; xylogenesis
2.  Carbon allocation during defoliation: testing a defense-growth trade-off in balsam fir 
During repetitive defoliation events, carbon can become limiting for trees. To maintain growth and survival, the resources have to be shared more efficiently, which could result in a trade-off between the different physiological processes of a plant. The objective of this study was to assess the effect of defoliation in carbon allocation of balsam fir [Abies balsamea (L.) Mill.] to test the presence of a trade-off between allocation to growth, carbon storage, and defense. Three defoliation intensities [control (C-trees, 0% defoliation), moderately (M-trees, 41–60%), and heavily (H-trees, 61–80%) defoliated] were selected in order to monitor several variables related to stem growth (wood formation in xylem), carbon storage in stem and needle (non-structural soluble sugars and starch), and defense components in needles (terpenoids compound) from May to October 2011. The concentration of starch was drastically reduced in both wood and leaves of H-trees with a quasi-absence of carbon partitioning to storage in early summer. Fewer kinds of monoterpenes and sesquiterpenes were formed with an increasing level of defoliation indicating a lower carbon allocation for the production of defense. The carbon allocation to wood formation gradually reduced at increasing defoliation intensities, with a lower growth rate and fewer tracheids resulting in a reduced carbon sequestration in cell walls. The hypothesis of a trade-off between the allocations to defense components and to non-structural (NCS) and structural (growth) carbon was rejected as most of the measured variables decreased with increasing defoliation. The starch amount was highly indicative of the tree carbon status at different defoliation intensity and future research should focus on the mechanism of starch utilization for survival and growth following an outbreak.
PMCID: PMC4429555  PMID: 26029235
spruce budworm outbreak; terpenoids; carbon allocation; starch; trade-off; wood formation
3.  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
4.  How do drought and warming influence survival and wood traits of Picea mariana saplings? 
Journal of Experimental Botany  2014;66(1):377-389.
Night and day warming combined with drought affect wood anatomy and survival, reflecting the importance of carbon–water relations for the survival process in Picea mariana saplings.
Warming and drought will occur with increased frequency and intensity at high latitudes in the future. How heat and water stress can influence tree mortality is incompletely understood. The aim of this study was to evaluate how carbon resources, stem hydraulics, and wood anatomy and density determine the ability of black spruce saplings to survive daytime or night-time warming (+ 6 °C in comparison with control) in combination with a drought period. Plant water relations, the dynamics of non-structural carbohydrates and starch, mortality rate, and wood anatomy and density of saplings were monitored. Warming, in conjunction with 25 d of water deficit, increased sapling mortality (10% and 20% in night-time and daytime warming, respectively) compared with the control conditions (0.8%). Drought substantially decreased gas exchange, and also pre-dawn and mid-day leaf water potential to values close to –3MPa which probably induced xylem embolism (xylem air entry point, P 12, being on average around –3MPa for this species). In addition, the recovery of gas exchange never reached the initial pre-stress levels, suggesting a possible loss of xylem hydraulic conductivity associated with cavitation. Consequently, mortality may be due to xylem hydraulic failure. Warmer temperatures limited the replenishment of starch reserves after their seasonal minimum. Lighter wood was formed during the drought period, reflecting a lower carbon allocation to cell wall formation, preventing the adaptation of the hydraulic system to drought. Saplings of black spruce experienced difficulty in adapting under climate change conditions, which might compromise their survival in the future.
PMCID: PMC4265170  PMID: 25371502
Carbon balance; climate change; drought; survival; warming; wood anatomy; wood density.
5.  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
6.  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
7.  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
8.  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
9.  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

Results 1-9 (9)