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Seasonality in tree cambial activity and xylem formation encompass large variation in environmental conditions. Abiotic stressors such as warming or drought also modulate plant behavior at species and individual level. Despite xylem formation susceptibility to carbon (C) and water availability, it is still unknown which are the key physiological variables that regulate xylogenesis, and to what extent plant performance contributes to further explain the number of cells in the different phases of xylem development. Xylogenesis and physiological behavior was monitored in saplings of Pinus pinaster Aiton, a bimodal growth pattern species, distributed in different irrigation regimes. Xylogenesis and plant physiological behavior were compared between treatments and the relationship between climate, physiology and the number of cells in the cambium, enlargement and cell-wall thickening phases was evaluated. Xylogenesis regulation shifted from physiological to climatic control as cell differentiation advanced to mature tracheids. The number of cells in the cambium increased with assimilation rates and decreased with the water potential gradient through the plant. Enlargement was the most susceptible phase to plant relative water content, whereas no physiological variable contributed to explain the number of cells in the wall thickening phase, which declined as temperatures increased. All treatments showed a bimodal growth pattern with a second growth period starting when primary growth was completed and after plants had experienced the highest summer hydraulic losses. Our study demonstrates the importance of including physiological responses and not only climate to fully understand xylogenesis, with special attention to the enlargement phase. This is critical when studying species with a bimodal growth pattern because the second growth peak responds to internal shifts of C allocation and may strongly depend on plant hydraulic responses and not on a fine tuning of cambial activity with soil water availability.

Recent climate projections predict a more rapid increase of winter temperature than summer and global temperature averages in temperate and cold environments. As there is relatively little experimental knowledge on the effect of winter warming on cambium phenology and stem growth in species growing in cold environments, the setting of manipulative experiments is considered of primary importance, and they can help to decipher the effect of reduced winter chilling and increased forcing temperatures on cambium reactivation, growth and xylem traits. In this study, localized stem heating was applied to investigate the effect of warming from the rest to the growth phase on cambium phenology, intra-annual stem growth dynamics and ring wood features in Picea abies (L.) H.Karst. We hypothesized that reduced winter chilling induces a postponed cambium dormancy release and decrease of stem growth, while high temperature during cell wall lignification determines an enrichment of latewood-like cells. The heating device was designed to maintain a +5 °C temperature delta with respect to air temperature, thus allowing an authentic scenario of warming. Continuous stem heating from the rest (November) to the growing phase determined, at the beginning of radial growth, a reduction of the number of cell layers in the cambium, higher number of cell layers in the wall thickening phase and an asynchronous stem radial growth when comparing heated and ambient saplings. Nevertheless, heating did not induce changes in the number of produced cell layers at the end of the growing season. The analyses of two-photon fluorescence images showed that woody rings formed during heating were enriched with latewood-like cells. Our results showed that an increase of 5 °C of temperature applied to the stem from the rest to growth might not influence, as generally reported, onset of cambial activity, but it could affect xylem morphology of Norway spruce in mountain environments.

Research on wood phenology has mainly focused on reactivation of the cambium in spring. In this study we investigated if summer drought advances cessation of wood formation and if it has any influence on wood structure in late successional forest trees of the temperate zone. The end of xylogenesis was monitored between August and November in stands of European beech and pedunculate oak in Belgium for two consecutive years, 2017 and 2018, with the latter year having experienced an exceptional summer drought. Wood formation in oak was affected by the drought, with oak trees ceasing cambial activity and wood maturation about 3 weeks earlier in 2018 compared with 2017. Beech ceased wood formation before oak, but its wood phenology did not differ between years. Furthermore, between the 2 years, no significant difference was found in ring width, percentage of mature fibers in the late season, vessel size and density. In 2018, beech did show thinner fiber walls, whereas oak showed thicker walls. In this paper, we showed that summer drought can have an important impact on late season wood phenology xylem development. This will help to better understand forest ecosystems and improve forest models.

Interlocked grain occurs when the orientation of xylem fibres oscillates, alternating between left- and right-handed spirals in successive wood layers. The cellular mechanisms giving rise to interlocked grain, thought to involve the slow rotation of fusiform initials within the vascular cambium, remain unclear. We suggest that observations of wood structure at the cellular level, but over large areas, might reveal these mechanisms. We assayed timber from several commercially important tropical angiosperms from the genus Khaya (African mahogany) that exhibit interlocked grain using X-ray computed microtomography followed by orthogonal slicing and image processing in ImageJ. Reconstructed tangential longitudinal sections were processed with the ImageJ directionality plug-in to directly measure fibre orientation and showed grain deviations of more than 10° from vertical in both left- and right-handed directions. Grain changed at locally constant rates, separated by locations where the direction of grain change sharply reversed. Image thresholding and segmentation conducted on reconstructed cross sections allowed the identification of vessels and measurement of their location, with vessel orientations then calculated in Matlab and, independently, in recalculated tangential longitudinal sections with the directionality plug-in. Vessel orientations varied more than fibre orientations, and on average deviated further from vertical than fibres at the locations where the direction of grain change reversed. Moreover, the reversal location for vessels was shifted ~400 μm towards the pith compared with the fibres, despite both cell types arising from the same fusiform initials within the vascular cambium. We propose a simple model to explain these distinct grain patterns. Were an auxin signal to control both the reorientation of cambial initials, as well as coordinating the end-on-end differentiation and linkage of xylem vessel elements, then it would be possible for fibres and vessels to run at subtly different angles, and to show different grain reversal locations.

Knowing more precisely the cambial phenology and wood formation dynamics of trees can lead to a better understanding on how trees react to short-term changes in environmental conditions. Such an understanding could also shed light on the physiological foundation of climate-growth interactions at a regional scale. Although it has been documented that temperature is an important factor determining the cambial phenology in cold and humid climates, there is less agreement on the driver(s) that trigger the onset and end of wood formation in cold and arid climates. Here, the phenological traits of cambial activity and xylem formation were analyzed biweekly along an altitudinal transect ranging from 3580 to 3980 m above sea level, a transect that covers the distribution of Qilian juniper (Juniperus przewalskii Kom.) along a slope of the Tibetan Plateau. Cambial phenology and the duration and rate of wood formation were assessed from anatomical observations during the growing season of the developing xylem obtained from microcores collected from the stem of 10 trees total in 2012 (five at two altitudes each) and 25 trees (five at five altitudes each) in 2013. We found that the onset of wood formation was significantly correlated with altitude in 2013, with onset beginning 8.2 days earlier with every 100 m decrease in elevation. The change in onset with elevation corresponds to a change of 14.1 days °C-1 when adjusted for the monitored altitudinal lapse rate of -0.58 °C per 100 m. The duration of wood formation lasted from mid-May to mid-August, with the length of the 2013 growing season decreasing from 97 to 65 days from low to high elevation. Although the end of growing season appeared minimally related to altitude during both growing seasons, differences in end of wood production and wood formation between the two growing seasons were significant. It appears that summer drought conditions constricted the end of growing season across all elevations along our transect in 2013. Sensitivity analysis found xylem growth was positively correlated with rate and duration of wood production, with the former explaining most variability in growth. Our findings provide new data on the timing and duration of wood formation and help quantify the potential impacts of global warming on tree growth and productivity in cold and arid regions.

In recent decades, anthropogenic activities have increased nitrogen (N) deposition in terrestrial ecosystems. This higher availability of N is expected to impact plant growth. However, the effects of N deposition on tree growth remain inconclusive due to the wide variability of experimental methods used. This study aimed to test the effect of short-term N addition on the intra-annual wood formation of Chinese red pine (Pinus massoniana Lamb.) in a warm-temperate forest of Central China. From 2013, solution containing 25 kg N ha-1 year-1 was applied monthly to the understory of experimental plots from April to December to double the current natural N deposition. Each week from March to December in 2014 and 2015, cambial activity and the timings and dynamics of xylem formation were monitored by collecting microcores from stems. Xylem formation lasted from March to November, producing an average of 19 and 33 cells for all studied trees in 2014 and 2015, respectively. No difference in xylem cell production was observed between control and N-treated trees. Moreover, N-treated trees had similar timings, rates and durations of xylem formation as control trees. These findings indicated that short-term N addition was unable to affect timings and dynamics of xylem formation in Chinese red pine of warm-temperate forest.

China's subtropical forests play a vital role in sequestering global carbon; therefore, it is critical to conduct a precise investigation of intra-annual wood formation in these ecosystems to clarify the mechanisms behind this. Two field experiments were established in Chinese subtropical forests to monitor weekly the intra-annual xylem formation of Pinus massoniana Lamb. from January to December 2015, using the recently developed micro-sampling approach. The effects of climate on wood formation were also assessed using linear or mixed models. Results indicate that there is an inactive period that might be semi-dormancy in subtropical pine ecosystems in January compared with the complete dormancy in temperate and boreal ecosystems and the fully active or short-term dormancy in tropical ecosystems. The duration of xylem formation of Chinese red pine in subtropical China in 2015 was 4-6 months longer than temperate and boreal forests. Moreover, trees were found to grow better during the dry season than the wet season, indicating that the Chinese red pine ecosystem is more strongly regulated by net energy than by environmental factors. Our findings indicate that China's subtropical pine forests may benefit from the expected longer dry seasons, possibly leading to better forest growth and improved carbon sequestration under continued climate warming.

A better understanding and prediction of the impact of changing climate on tree stem growth could greatly benefit from the combination of anatomical and ecophysiological knowledge, yet the majority of studies focus on one research field only. We propose an approach that combines the method of pinning (cambial wounding) to timestamp anatomical X-ray computed microtomography images with continuous measurements of sap flow and stem diameter variations. By pinning the cambium of well-watered and drought-treated young African tropical trees of the species Maesopsis eminii Engl. we could quantify wood formation during a specific period of time and relate it to tree physiology and prevailing microclimate. Integrating continuous plant measurements and high-frequency pinning proved very useful to visualize and quantify the effects on stem growth of drought in M. eminii. Wood formation completely stopped during drought, and was associated with a strong shrinkage in stem diameter. Next, an unexpected increase in stem diameter was observed during drought, probably caused by root pressure, but not accompanied by wood formation. Our proposed approach of combining continuous plant measurements with cambial pinning is very promising to relate ecophysiology to stem anatomy and to understand the mechanisms underlying tree stem growth and bridge the gaps between the two research fields.

Wood represents one of the most important renewable commodities for humanity and plays a crucial role in terrestrial ecosystem carbon-cycling. Wood formation is the result of a multitude of events that require the concerted action of endogenous and exogenous factors under the influence of photoperiod, for instance genes and plant growth regulators. Beyond providing mechanical support and being responsible for the increase in stem radial diameter, woody tissues constitute the vascular system of trees and are capable of reacting to environmental stimuli, and as such are therefore quite plastic and responsive. Despite the ecological and economic importance of wood, not all aspects of its formation have been unveiled. Many gaps in our knowledge are still present, which hinder the maximal exploitation of this precious bioresource. This review aims at surveying the current knowledge of wood formation and the available molecular data addressing the relationship between wood production and environmental factors, which have crucial influences on the rhythmic regulation of cambial activity and exert profound effects on tree stem growth, wood yield and properties. We will here go beyond wood sensu stricto, i.e., secondary xylem, and extend our survey to other tissues, namely vascular cambium, phloem and fibres. The purpose is to provide the reader with an overview of the complexity of the topic and to highlight the importance of progressing in the future towards an integrated knowledge on the subject.

Despite its major economic importance and the vulnerability of Picea abies (L.) H. Karst. to climate change, how its radial growth at intra-annual resolution is influenced by weather conditions in forest stands with a high production capacity has scarcely been explored. Between 2009 and 2011, phenological variation in seasonal cambial cell production (CP) was analysed in adult P. abies trees from three contrasting sites, differing in altitude and latitude. The results indicate that the timing of cambial CP is a highly synchronic process within populations since in all cases the cambium simultaneously started and stopped producing xylem and phloem cells. Our results also demonstrate that the phenology of cambial CP is highly variable and plastic between years, depending on seasonal temperature and precipitation variation. Differences among sites, however, are only partially explained by different environmental (elevation and altitude) and climatic conditions, suggesting that local adaptation may also play a decisive role in the strategy of P. abies for adapting wood and phloem increments to function optimally under local conditions.

Drought tolerance is a key factor for the establishment and survival of tree species in tropical ecosystems. Specific mecha nisms of drought resistance can be grouped into four functional ecotypes based on differences in leaf fall behavior: deciduous, brevi-deciduous, stem succulent and evergreen. To identify the key factors influencing phenology and cambial activity and thus drought tolerance, we tested the stomatal conductance, leaf water potential and stable carbon isotopes in the leaves and wood of 12 species from a tropical dry forest in Costa Rica. With wood anatomical techniques, we further studied seasonal cambial activity and a suite of wood traits related to water transport for each of the functional ecotypes. Using a p rincipal component analysis, we identified two groups of variables that can be related to (i) hydraulic conductivity and (ii) c ontrol of transpiration and water loss. Hydraulic conductivity is controlled by vessel size as the limiting variable, water potential as the driving force and wood density as the stabilizing factor of the anatomical structure of an effective water transport system. Stomatal control plays a major role in terms of water loss or saving and is the dominant factor for differences in phenological behavior. Stem succulent species in particular developed a rarely identified but highly effective strat egy against drought stress, which makes it a successful pioneer species in tropical dry forests.

The timing of wood formation is crucial to determine how environmental factors affect tree growth. The long-lived bristlecone pine (Pinus longaeva D. K. Bailey) is a foundation treeline species in the Great Basin of North America reaching stem ages of about 5000 years. We investigated stem cambial phenology and radial size variability to quantify the relative influence of environmental variables on bristlecone pine growth. Repeated cellular measurements and half-hourly dendrometer records were obtained during 2013 and 2014 for two high-elevation stands included in the Nevada Climate-ecohydrological Assessment Network. Daily time series of stem radial variations showed rehydration and expansion starting in late April-early May, prior to the onset of wood formation at breast height. Formation of new xylem started in June and lasted until mid-September. There were no differences in phenological timing between the two stands, or in the air and soil temperature thresholds for the onset of xylogenesis. A multiple logistic regression model highlighted a separate effect of air and soil temperature on xylogenesis, the relevance of which was modulated by the interaction with vapor pressure and soil water content. While air temperature plays a key role in cambial resumption after winter dormancy, soil thermal conditions coupled with snowpack dynamics also influence the onset of wood formation by regulating plant-soil water exchanges. Our results help build a physiological understanding of climate-growth relationships in P. longaeva, the importance of which for dendroclimatic reconstructions can hardly be overstated. In addition, environmental drivers of xylogenesis at the treeline ecotone, by controlling the growth of dominant species, ultimately determine ecosystem responses to climatic change.

By 2100, climate change is predicted to warm high-latitude summers by 3–8 °C (ACIA 2005, Christensen et al. 2007). High temperatures will become more common in the boreal region and, in the absence of significantly increased precipitation, drought frequency and intensity will increase. Much of the North American boreal consists of forests dominated by black spruce (Picea mariana (Mill.) B.S.P.), a major timber crop that dominates frequently flooded soils, but has shallow roots (

We determined the cambial sensitivity and quantified the anatomical differences in xylem of Abies balsamea (L.) Mill. seedlings subjected to artificial defoliation to simulate spruce budworm feeding. Defoliation was performed by removing two-thirds of needles of all current-year shoots for up to four consecutive growth cycles to account for inter- and intra-annual xylem formation. In Experiment 1, xylem development was studied from May to October 2005 in seedlings defoliated at the end of June. In Experiment 2, anatomical features of the xylem were measured along the tree rings formed in 2005 and 2006 during the four cycles of growth and defoliation. Control and defoliated seedlings showed similar patterns of cambial activity and timing of xylem differentiation, although fewer enlarging cells were observed in August to September in defoliated seedlings. Tree-ring widths were similar in control and defoliated seedlings, with thinner rings produced in the greenhouse in winter. No effect of defoliation on cell lumen area was observed, and effects on radial cell diameter and wall thickness were found only occasionally. The results indicate that the A. balsamea seedlings produced all the resources required to maintain stem growth during the four cycles of defoliation.

After mechanical wounding, callus tissue and tangential rows of traumatic resin ducts (TRDs) are formed in many conifer species. This reaction can be used to date past events of geomorphic processes such as rockfall, debris flow and snow avalanches. However, only few points are known about the tangential spread or the timing of callus tissue and TRD formation after wounding. We analyzed 19 Larix decidua Mill. (European larch) and eight Picea abies (L.) Karst. (Norway spruce) trees that were severely damaged by rockfall activity, resulting in a total of 111 injuries. Callus tissue appeared sparsely on the cross sections and was detected on only 4.2% of the L. decidua samples and 3.6% of the P. abies samples. In contrast, TRDs were present on all cross sections following wounding and were visible on more than one-third (34% in L. decidua and 36.4% in P. abies) of the circumference where the cambium was not destroyed by the rockfall impact. We observe different reactions in the trees depending on the seasonal timing of wounding. The tangential spread of callus tissue and TRDs was more important if the injury occurred during the growth period than during the dormant season, with the difference between seasons being more pronounced for callus tissue formation than for TRD formation. We observed an intra-annual radial migration of TRDs with increasing tangential distance from the wound in 73.2% of the L. decidua samples and 96.6% of the P. abies samples. The persistence of TRD formation in the years following wounding showed that only L. decidua trees produced TRDs 2 years after wounding (10.5%), whereas P. abies trees produced TRDs 5 years after wounding (> 50%).

GH3 genes related to the auxin-inducible Glycine max (L.) Merr. GmGH3 gene encode enzymes that conjugate amino acids to auxin. To investigate the role of GH3 enzymes in stress responses and normal wood development, Populus x canescens (Ait.) was transformed with the promoter-reporter construct GH3::GUS containing a GH3 promoter and the 5' UTR from soybean. beta-Glucuronidase (GUS) activity was present in the vascular tissues of leaves and in developing lateral roots and was inducible in silent tissues by external auxin application. A decrease in GUS activity from the stem apex to the bottom corresponded to decreases in auxin concentrations in these tissues. High auxin concentration and high GH3::GUS activity were present in the pith tissue, which may provide storage for auxin compounds. GH3 reporter was active in ray cells, paratracheal parenchyma cells, maturing vessels and in cells surrounding maturing phloem fibers but not in the cambium and immature phloem, despite high auxin concentrations in the latter tissues. However, the GH3 promoter in these tissues became active when the plants were exposed to abiotic stresses, like bending or salinity, causing changes in wood anatomy. We suggest that adjustment of the internal auxin balance in wood in response to environmental cues involves GH3 auxin conjugate synthases.

The involvement of microfilaments and microtubules in the development of the radial and axial components of secondary xylem (wood) in hybrid aspen (Populus tremula L. x P. tremuloides Michx.) was studied by indirect immunofluorescent localization techniques. In addition to cambial cells, the differentiated cell types considered were early- and late-wood vessel elements, axial parenchyma, normal-wood fibers and gelatinous fibers, and contact and isolation ray cells. Microfilaments were rare in ray cambial cells, but were abundant and axially arranged in their derivatives once cell elongation had begun, and persisted in that orientation in mature ray cells. Microfilaments were axially arranged in fusiform cambial cells and persisted in that orientation in all xylem derivatives of those cells. Microtubules were randomly oriented in ray and fusiform cells of the cambial zone. Dense arrays of parallel-aligned microtubules were oriented near axially in the developing gelatinous fibers, but at a wide range of angles in normal-wood fibers. Ellipses of microfilaments were associated with pit development in fiber cells and isolation ray cells. Rings of co-localized microtubules and microfilaments were associated with developing inter-vessel bordered pits and vessel-contact ray cell contact pits, and, in the case of bordered pits, these rings decreased in diameter as the over-arching pit border increased in size. Although only microtubules were seen at the periphery of the perforation plate of vessel elements, a prominent meshwork of microfilaments overlaid the perforation plate itself. A consensus view of the roles of the cytoskeleton during wood formation in angiosperm trees is presented.

Inferences on climate change effects are reliable only if they are based on a causal relationship rather than simple statistical predictive capacity. To assess for causal links between climate and mature black spruce (Picea mariana (Mills.) BSP) radial growth, we combined the use of wood anatomy, cambium phenology, climate and soil measurements (air temperature and humidity, precipitations, soil temperature and water content, photosynthetically active radiation), and a model selection approach proceeding backwards from a full model. Results show that the number of tracheids is responsible for 88% of the variation in ring width whereas mean tracheid diameter accounts for the remaining 12%. The number of tracheids produced depends on factors related to photosynthesis during tracheid production, i.e., daily light intensity and maximum temperature between the day of initiation and the day of cessation of tracheid production, plus soil temperature during August of the previous year which is an important period for determining the number of new needles produced. It is also important to consider duration of the period for tracheid production. These results imply that short-term climate change should increase black spruce radial growth. They also suggest that the typical use of post-growth ring width sampling individually linked to air temperature and precipitations is not sufficient to infer climate change effects accurately on radial growth where there is no strong single climatic limitation but multiple limitations instead.

Cambial growth was modelled as a function of detailed levelled physiological processes for cell enlargement and water and sugar transport to the cambium. Cambial growth was described at the cell level where local sugar concentration and turgor pressure induce irreversible cell expansion and cell wall synthesis. It was demonstrated how transpiration and photosynthesis rates, metabolic and physiological processes and structural features of a tree mediate their effects directly on the local water and sugar status and influence cambial growth. Large trees were predicted to be less sensitive to changes in the transient water and sugar status, compared with smaller ones, as they have more water and sugar storage and were, therefore, less coupled to short-term changes in the environment. Modelling the cambial dynamics at the individual cell level turned out to be a complex task as the radial short-distance transport of water and sugars and control signals determining cell division and cessation of cell enlargement and cell wall synthesis had to be described simultaneously.

At present, a carbon (C) content of 50% (w/w) in dry wood is widely accepted as a generic value; however, few wood C measurements have been reported. We used elemental analysis to investigate C content per unit of dry matter and observed that it varied both radially and vertically in boles of two old-growth tree species: sugar maple (Acer saccharum Marsh.) and giant sequoia (Sequoiadendron giganteum (Lindl.) Bucholz). In sugar maple there was considerable variation in tree ring widths among four radii for particular annual layers of xylem, revealing that the annual rate of C assimilation differs around the circumference and from the base of each tree to its top, but the observed variation in C content was unrelated to diameter growth rate and strongly related to the calendar year when the wood was formed. Carbon content in sugar maple wood increased in an approximately linear fashion, from50 to 51% from pith to cambium, at both the base and top of the boles. In giant sequoia, C was essentially constant at55% across many hundreds of years of heartwood, but it declined abruptly at the sapwood-heartwood boundary and remained lower in all sapwood samples, an indication that heartwood formation involves anabolic metabolism. Factors that may be responsible for the different C contents and trends with age between sugar maple and sequoia trees are considered. Tree-ring data from this study do not support some of the key assumptions made by dendrochronology.

In 1990, a 2-ha plantation of Eucalyptus nitens (Deane and Maiden) Maiden was established in southeastern Tasmania and subjected to different irrigation regimes. Point dendrometers were installed in March 1995 to monitor radial stem movement every 15 min over several growing seasons. In this study, data from two growing seasons (1996-1998) were considered. From these measurements, daily increments of stem radius were determined. At the end of the second growing season, we extracted 12-mm cores and measured microfibril angles (MFA) of the wood at high resolution. Microfibril angles were rescaled on a time axis and mapped to daily and distance-based elements. Among treatments, irrigated trees in particular formed higher MFA early in the growing season (September-November) and lower MFA later in the growing season. Trees subjected to cyclic droughts showed clear relationships between MFA and soil water deficits, with MFA increasing in response to water stress release. Increases in MFA were preceded by accelerations in daily increment of stem radius. Among treatments, trees subjected to severe drought had the smallest MFA and generally low fluctuations in MFA. Irrigated trees were susceptible to changes in climate, whereas growth of the trees in the other treatments was limited by water availability. Use of path-analysis showed that temperature had an effect on stem radius increment but not on MFA; wind speed was the only factor that influenced MFA directly. Microfibril angle was correlated with stem shrinking and expansion phases; growth period length and growth rates were positively related to MFA.