Modelling the spatial crosstalk between two biochemical signals explains wood formation dynamics and tree-ring structure.

In conifers, xylogenesis during a growing season produces a very characteristic tree-ring structure: large, thin-walled earlywood cells followed by narrow, thick-walled latewood cells. Although many factors influence the dynamics of differentiation and the final dimensions of xylem cells, the associated patterns of variation remain very stable from one year to the next. While radial growth is characterized by an S-shaped curve, the widths of xylem differentiation zones exhibit characteristic skewed bell-shaped curves. These elements suggest a strong internal control of xylogenesis. It has long been hypothesized that much of this regulation relies on a morphogenetic gradient of auxin. However, recent modelling studies have shown that while this hypothesis could account for the dynamics of stem radial growth and the zonation of the developing xylem, it failed to reproduce the characteristic tree-ring structure. Here, we investigated the hypothesis of regulation by a crosstalk between auxin and a second biochemical signal, by using computational morphodynamics. We found that, in conifers, such a crosstalk is sufficient to simulate the characteristic features of wood formation dynamics, as well as the resulting tree-ring structure. In this model, auxin controls cell enlargement rates while another signal (e.g. cytokinin, tracheary element differentiation inhibitory factor) drives cell division and auxin polar transport.

Biomechanical control of beech pole verticality (Fagus sylvatica) before and after thinning: theoretical modelling and ground-truth data using terrestrial LiDAR.

PREMISE OF THE STUDY: Thinning is a frequent disturbance in managed forests, especially to increase radial growth. Due to buckling and bending risk associated with height and mass growth, tree verticality is strongly constrained in slender trees growing in dense forests and poor light conditions. Tree verticality is controlled by uprighting movements implemented from local curvatures induced by wood maturation stresses and/or eccentric radial growth. This study presents the first attempt to compare the real uprighting movements in mature trees using a theoretical model of posture control. METHODS: Stem lean and curvature were measured by Terrestrial LiDAR Scanner (TLS) technology before and 6 years after thinning and compared to unthinned control poles. Measures for several tree and wood traits were pooled together to implement a widely used biomechanical model of tree posture control. Changes in observed stem lean were then compared with the model predictions, and discrepancies were reviewed. KEY RESULTS: Even under a highly constrained environment, most control poles were able to counterbalance gravitational curvature and avoid sagging. Thinning stimulated uprighting movements. The theoretical uprighting curvature rate increased just after thinning, then slowed after 2 years, likely due to the stem diameter increase. The biomechanical model overestimated the magnitude of uprighting. CONCLUSIONS: Most suppressed beech poles maintain a constant lean angle, and uprighting movements occur after thinning, indicating that stem lean is plastic in response to light conditions. Acclimation of posture control to other changes in growth condition should be investigated, and lean angles should be measured in forest inventories as an indicator of future wood quality.

Forest trees filter chronic wind-signals to acclimate to high winds.

Controlled experiments have shown that trees acclimate thigmomorphogenetically to wind-loads by sensing their deformation (strain). However, the strain regime in nature is exposed to a full spectrum of winds. We hypothesized that trees avoid overreacting by responding only to winds which bring information on local climate and/or wind exposure. Additionally, competition for light dependent on tree social status also likely affects thigmomorphogenesis. We monitored and manipulated quantitatively the strain regimes of 15 pairs of beech (Fagus sylvatica) trees of contrasting social status in an acclimated stand, and quantified the effects of these regimes on the radial growth over a vegetative season. Trees exposed to artificial bending, the intensity of which corresponds to the strongest wind-induced strains, enhanced their secondary growth by at least 80%. Surprisingly, this reaction was even greater - relatively - for suppressed trees than for dominant ones. Acclimated trees did not sense the different types of wind events in the same way. Daily wind speed peaks due to thermal winds were filtered out. Thigmomorphogenesis was therefore driven by intense storms. Thigmomorphogenesis is also likely to be involved in determining social status.

Kinetics of tracheid development explain conifer tree-ring structure.

Conifer tree rings are generally composed of large, thin-walled cells of light earlywood followed by narrow, thick-walled cells of dense latewood. Yet, how wood formation processes and the associated kinetics create this typical pattern remains poorly understood. We monitored tree-ring formation weekly over 3 yr in 45 trees of three conifer species in France. Data were used to model cell development kinetics, and to attribute the relative importance of the duration and rate of cell enlargement and cell wall deposition on tree-ring structure. Cell enlargement duration contributed to 75% of changes in cell diameter along the tree rings. Remarkably, the amount of wall material per cell was quite constant along the rings. Consequently, and in contrast with widespread belief, changes in cell wall thickness were not principally attributed to the duration and rate of wall deposition (33%), but rather to the changes in cell size (67%). Cell enlargement duration, as the main driver of cell size and wall thickness, contributed to 56% of wood density variation along the rings. This mechanistic framework now forms the basis for unraveling how environmental stresses trigger deviations (e.g. false rings) from the normal tree-ring structure.

Generalized additive models reveal the intrinsic complexity of wood formation dynamics.

The intra-annual dynamics of wood formation, which involves the passage of newly produced cells through three successive differentiation phases (division, enlargement, and wall thickening) to reach the final functional mature state, has traditionally been described in conifers as three delayed bell-shaped curves followed by an S-shaped curve. Here the classical view represented by the 'Gompertz function (GF) approach' was challenged using two novel approaches based on parametric generalized linear models (GLMs) and 'data-driven' generalized additive models (GAMs). These three approaches (GFs, GLMs, and GAMs) were used to describe seasonal changes in cell numbers in each of the xylem differentiation phases and to calculate the timing of cell development in three conifer species [Picea abies (L.), Pinus sylvestris L., and Abies alba Mill.]. GAMs outperformed GFs and GLMs in describing intra-annual wood formation dynamics, showing two left-skewed bell-shaped curves for division and enlargement, and a right-skewed bimodal curve for thickening. Cell residence times progressively decreased through the season for enlargement, whilst increasing late but rapidly for thickening. These patterns match changes in cell anatomical features within a tree ring, which allows the separation of earlywood and latewood into two distinct cell populations. A novel statistical approach is presented which renews our understanding of xylogenesis, a dynamic biological process in which the rate of cell production interplays with cell residence times in each developmental phase to create complex seasonal patterns.

Effect of tree size and competition on tension wood production over time in beech plantations and assessing relative gravitropic response with a biomechanical model.

PREMISE OF THE STUDY: Gravitropic movements are unexpected mechanical processes that could disturb tree design allometries derived from the physics of nonliving bodies. We investigated whether the scaling law of gravitropic performance (power of -2 of stem diameter) derived from integrative biomechanical modeling is disturbed by ontogeny or environment, then discuss the silvicultural and dendroecological consequences. METHODS: In a beech (Fagus sylvatica) plantation, four plots with different initial planting densities evolved without any intervention for 26 yr. Regular tree inventories and a silvicultural model were used to monitor competition over time in each plot. The radial production of tension wood was quantified using a cross-section of the stems at 1.30-m height, and an integrative biomechanical model computed the tree gravitropic performance over time. KEY RESULTS: All trees developed tension wood over the whole period, with higher amounts at the youngest age, resulting in theoretical lean corrections of ca. 20-30° on the first 4 m of the stem over the whole period. The scaling law of gravitropic performance is slightly larger than the power of -2 of stem diameter. CONCLUSIONS: Gravitropic performance in forest ecosystems is mainly limited by size (diameter). Ontogenic acclimation of tension wood formation allows the youngest trees to be more reactive. No additional effect of spacing was found. However, silviculture influences size and, therefore, tree reactivity at a given age. Such results will be helpful for dendroecological approaches that use wood as a marker of environmental disturbances or a trait linked to plant strategies.

Growth and posture control strategies in Fagus sylvatica and Acer pseudoplatanus saplings in response to canopy disturbance.

BACKGROUND AND AIMS: Forest tree saplings that grow in the understorey undergo frequent changes in their light environment to which they must adapt to ensure their survival and growth. Crown architecture, which plays a critical role in light capture and mechanical stability, is a major component of sapling adaptation to canopy disturbance. Shade-adapted saplings typically have plagiotropic stems and branches. After canopy opening, they need to develop more erect shoots in order to exploit the new light conditions. The objective of this study was to test whether changes in sapling stem inclination occur after canopy opening, and to analyse the morphological changes associated with stem reorientation. METHODS: A 4-year canopy-opening field experiment with naturally regenerated Fagus sylvatica and Acer pseudoplatanus saplings was conducted. The appearance of new stem axes, stem basal diameter and inclination along the stem were recorded every year after canopy opening. KEY RESULTS: Both species showed considerable stem reorientation resulting primarily from uprighting (more erect) shoot movements in Fagus, and from uprighting movements, shoot elongation and formation of relay shoots in Acer. In both species, the magnitude of shoot uprighting movements was primarily related to initial stem inclination. Both the basal part and the apical part of the stem contributed to uprighting movements. Stem movements did not appear to be limited by stem size or by stem growth. CONCLUSIONS: Stem uprighting movements in shade-adapted Fagus and Acer saplings following canopy disturbance were considerable and rapid, suggesting that stem reorientation processes play a significant role in the growth strategy of the species.

The power and control of gravitropic movements in plants: a biomechanical and systems biology view.

The study of gravitropic movements in plants has enjoyed a long history of research going back to the pioneering works of the 19th century and the famous book entitled 'The power of movement in plants' by Charles and Francis Darwin. Over the last few decades, the emphasis has shifted towards the cellular and molecular biology of gravisensing and the onset of auxin gradients across the organs. However, our understanding of plant movement cannot be completed before quantifying spatio-temporal changes in curvature and how they are produced through the motor process of active bending and controlled by gravisensing. This review sets out to show how combining approaches borrowed from continuum mechanics (kinematic imaging, structural modelling) with approaches from physiology and modern molecular biology has made it possible to generate integrative biomechanical models of the processes involved in gravitropism at several levels. The physiological and biomechanical bases are reviewed and two of the most complete integrative models of the gravireaction organ available are then compared, highlighting how the comparison between movements driven by differential growth and movements driven by reaction wood formation in woody organs has provided highly informative key insights. The advantages of these models as tools for analysing genetic control through quantitative process-based phenotyping as well as for identifying target traits for ecological studies are discussed. It is argued that such models are tools for a systems biology approach to gravitropic movement that has the potential to resolve at least some of the research questions raised 150 years ago.

Functional diversity in gravitropic reaction among tropical seedlings in relation to ecological and developmental traits.

Gravitropism is necessary for plants to control the orientation of their axes while they grow in height. In woody plants, stem re-orientations are costly because they are achieved through diameter growth. The functional diversity of gravitropism was studied to check if the mechanisms involved and their efficiency may contribute to the differentiation of height growth strategies between forest tree species at the seedling stage. Seedlings of eight tropical species were grown tilted in a greenhouse, and their up-righting movement and diameter growth were measured over three months. Morphological, anatomical, and biomechanical traits were measured at the end of the survey. Curvature analysis was used to analyse the up-righting response along the stems. Variations in stem curvature depend on diameter growth, size effects, the increase in self-weight, and the efficiency of the gravitropic reaction. A biomechanical model was used to separate these contributions. Results showed that (i) gravitropic movements were based on a common mechanism associated to similar dynamic patterns, (ii) clear differences in efficiency (defined as the change in curvature achieved during an elementary diameter increment for a given stem diameter) existed between species, (iii) the equilibrium angle of the stem and the anatomical characters associated with the efficiency of the reaction also differed between species, and (iv) the differences in gravitropic reaction were related to the light requirements: heliophilic species, compared to more shade-tolerant species, had a larger efficiency and an equilibrium angle closer to vertical. This suggests that traits determining the gravitropic reaction are related to the strategy of light interception and may contribute to the differentiation of ecological strategies promoting the maintenance of biodiversity in tropical rainforests.

Changes in hydraulic conductivity, mechanical properties, and density reflecting the fall in strain along the lateral roots of two species of tropical trees.

Roots have been described as having larger vessels and so greater hydraulic efficiency than the stem. Differences in the strength and stiffness of the tissue within the root system itself are thought to be an adaptation to the loading conditions experienced by the roots and to be related to differences in density. It is not known how potential mechanical adaptations may affect the hydraulic properties of the roots. The change in strength, stiffness, conductivity, density, sapwood area, and second moment of area distally along the lateral roots of two tropical tree species in which the strain is known to decrease rapidly was studied and the values were compared with those of the trunk. It was found that as the strain fell distally along the roots, so did the strength and stiffness of the tissue, whereas the conductivity increased exponentially. These changes appeared to be related to differences in density. In contrast to the distal-most roots, the tissue of the proximal roots had a lower conductivity and higher strength than that of the trunk. This suggests that mechanical requirements on the structure rather than the water potential gradient from roots to branches are responsible for the general pattern that roots have larger vessels than the stem. In spite of their increased transectional area, the buttressed proximal roots were subjected to higher levels of stress and had a lower total conductivity than the rest of the root system.

Wind loads and competition for light sculpt trees into self-similar structures.

Trees are self-similar structures: their branch lengths and diameters vary allometrically within the tree architecture, with longer and thicker branches near the ground. These tree allometries are often attributed to optimisation of hydraulic sap transport and safety against elastic buckling. Here, we show that these allometries also emerge from a model that includes competition for light, wind biomechanics and no hydraulics. We have developed MECHATREE, a numerical model of trees growing and evolving on a virtual island. With this model, we identify the fittest growth strategy when trees compete for light and allocate their photosynthates to grow seeds, create new branches or reinforce existing ones in response to wind-induced loads. Strikingly, we find that selected trees species are self-similar and follow allometric scalings similar to those observed on dicots and conifers. This result suggests that resistance to wind and competition for light play an essential role in determining tree allometries.

Comment on "Critical wind speed at which trees break".

Virot et al. [E. Virot et al., Phys. Rev. E 93, 023001 (2016)10.1103/PhysRevE.93.023001] assert that the critical wind speed at which ⩾50% of all trees in a population break is ≈42 m/s, regardless of tree characteristics. We show that empirical data do not support this assertion, and that the assumptions underlying the theory used by Virot et al. are inconsistent with the biomechanics of trees.

Woody biomass production lags stem-girth increase by over one month in coniferous forests.

Wood is the main terrestrial biotic reservoir for long-term carbon sequestration(1), and its formation in trees consumes around 15% of anthropogenic carbon dioxide emissions each year(2). However, the seasonal dynamics of woody biomass production cannot be quantified from eddy covariance or satellite observations. As such, our understanding of this key carbon cycle component, and its sensitivity to climate, remains limited. Here, we present high-resolution cellular based measurements of wood formation dynamics in three coniferous forest sites in northeastern France, performed over a period of 3 years. We show that stem woody biomass production lags behind stem-girth increase by over 1 month. We also analyse more general phenological observations of xylem tissue formation in Northern Hemisphere forests and find similar time lags in boreal, temperate, subalpine and Mediterranean forests. These time lags question the extension of the equivalence between stem size increase and woody biomass production to intra-annual time scales(3, 4, 5, 6). They also suggest that these two growth processes exhibit differential sensitivities to local environmental conditions. Indeed, in the well-watered French sites the seasonal dynamics of stem-girth increase matched the photoperiod cycle, whereas those of woody biomass production closely followed the seasonal course of temperature. We suggest that forecasted changes in the annual cycle of climatic factors(7) may shift the phase timing of stem size increase and woody biomass production in the future.

Life strategies in intra-annual dynamics of wood formation: example of three conifer species in a temperate forest in north-east France.

We investigated whether timing and rate of growth are related to the life strategies and fitness of three conifer species. Intra-annual dynamics of wood formation, shoot elongation and needle phenology were monitored over 3 years in five Norway spruces (Picea abies (L.) Karst.), five Scots pines (Pinus sylvestris L.) and five silver firs (Abies alba Mill.) grown intermixed. For the three species, the growing season (delimited by cambial activity onset and cessation) lasted about 4 months, while the whole process of wood formation lasted 5-6 months. Needle unfolding and shoot elongation followed the onset of cambial activity and lasted only one-third of the season. Pines exhibited an 'extensive strategy' of cambial activity, with long durations but low growth rates, while firs and spruces adopted an 'intensive strategy' with shorter durations but higher growth rates. We estimated that about 75% of the annual radial increment variability was attributable to the rate of cell production, and only 25% to its duration. Cambial activity rates culminated at the same time for the three species, whereas shoot elongation reached its maximal rate earlier in pines. Results show that species-specific life strategies are recognizable through functional traits of intra-annual growth dynamics. The opposition between Scots pine extensive strategy and silver fir and Norway spruce intensive strategy supports the theory that pioneer species are greater resource expenders and develop riskier life strategies to capture resources, while shade-tolerant species utilize resources more efficiently and develop safer life strategies. Despite different strategies, synchronicity of the maximal rates of cambial activity suggests a strong functional convergence between co-existing conifer species, resulting in head-on competition for resources.

Interrelations between hydraulic and mechanical stress adaptations in woody plants.

The fields of plant water relations and plant biomechanics have traditionally been studied separately even though often the same tissues are responsible for water transport and mechanical support. There is now increasing evidence that hydraulic and mechanical adaptations may influence one another. We studied the changes in the hydraulic and mechanical properties of the wood along lateral roots of two species of buttressed trees. In these roots, the mechanical contstraints quantified by strain measurements are known to decrease distally. Further, we investigated the effect of mechanical loading on the vessel anatomy in these and four other species of tropical trees. We found that as the strain decreased, the wood became progressively less stiff and strong but the conductivity increased exponentially. This was reflected in that adaptations towards re-enforcing mechanically loaded areas resulted in xylem with fewer and smaller vessels. In addition a controlled growth experiment on three tree species showed that drought adaptation may results in plants with stronger and stiffer tissue. Our results indicate that hydraulic and mechanical stress adaptations may be interrelated, and so support recent studied suggesting that physiological responses are complex balances rather than pure optimisations.

The gravitropic response of poplar trunks: key roles of prestressed wood regulation and the relative kinetics of cambial growth versus wood maturation.

In tree trunks, the motor of gravitropism involves radial growth and differentiation of reaction wood (Archer, 1986). The first aim of this study was to quantify the kinematics of gravitropic response in young poplar (Populus nigra x Populus deltoides, 'I4551') by measuring the kinematics of curvature fields along trunks. Three phases were identified, including latency, upward curving, and an anticipative autotropic decurving, which has been overlooked in research on trees. The biological and mechanical bases of these processes were investigated by assessing the biomechanical model of Fournier et al. (1994). Its application at two different time spans of integration made it possible to test hypotheses on maturation, separating the effects of radial growth and cross section size from those of wood prestressing. A significant correlation between trunk curvature and Fournier's model integrated over the growing season was found, but only explained 32% of the total variance. Moreover, over a week's time period, the model failed due to a clear out phasing of the kinetics of radial growth and curvature that the model does not take into account. This demonstrates a key role of the relative kinetics of radial growth and the maturation process during gravitropism. Moreover, the degree of maturation strains appears to differ in the tension woods produced during the upward curving and decurving phases. Cell wall maturation seems to be regulated to achieve control over the degree of prestressing of tension wood, providing effective control of trunk shape.

How to determine sapling buckling risk with only a few measurements.

Tree buckling risk (actual height/critical buckling height) is an important biomechanical trait of plant growth strategies, and one that contributes to species coexistence. To estimate the diversity of this trait among wide samples, a method that minimizes damage to the plants is necessary. On the basis of the rarely used, complete version of Greenhill's model (1881, Proceedings of the Cambridge Philosophical Society 4(2): 65-73), we precisely measured all the necessary parameters on a sample of 236 saplings of 16 species. Then, using sensitivity (variance) analysis, regressions between successive models for risk factors and species ranks and the use of these models on samples of self- and nonself-supporting saplings, we tested different degrees of simplification up to the most simple and widely used formula that assumes that the tree is a cylindrical homogeneous pole. The size factor had the greatest effect on buckling risk, followed by the form factor and the modulus of elasticity of the wood. Therefore, estimates of buckling risk must consider not only the wood properties but especially the form factor. Finally, we proposed a simple but accurate method of assessing tree buckling risk that is applicable to a wide range of samples and that requires mostly nondestructive measurements.

Changes in vessel anatomy in response to mechanical loading in six species of tropical trees.

It is well known that trees adapt their supportive tissues to changes in loading conditions, yet little is known about how the vascular anatomy is modified in this process. We investigated this by comparing more and less mechanically loaded sections in six species of tropical trees with two different rooting morphologies. We measured the strain, vessel size, frequency and area fraction and from this calculated the specific conductivity, then measured the conductivity, modulus of elasticity and yield stress. The smallest vessels and the lowest vessel frequency were found in the parts of the trees subjected to the greatest stresses or strains. The specific conductivity varied up to two orders of magnitude between mechanically loaded and mechanically unimportant parts of the root system. A trade-off between conductivity and stiffness or strength was revealed, which suggests that anatomical alterations occur in response to mechanical strain. By contrast, between-tree comparisons showed that average anatomical features for the whole tree seemed more closely related to their ecological strategy.

Biomechanics of buttressed trees: bending strains and stresses.

The different hypotheses about buttress function and formation mainly involve mechanical theory. Forces were applied to two trees of Sloanea spp., a tropical genus that develops typical thin buttresses, and the three-dimensional strains were measured at different parts of the trunk base. Risks of failure were greater on the buttress sides, where shear and tangential stresses are greater, not on the ridges, in spite of high longitudinal (parallel to the grain) stresses. A simple beam model, computed from the second moment of area of digitized cross sections, is consistent with longitudinal strain variations but cannot predict accurately variations with height. Patterns of longitudinal strain variation along ridges are very different in the two individuals, owing to a pronounced lateral curvature in one specimen. The constant stress hypothesis is discussed based on these results. Without chronological data during the development of the tree, it cannot be proved that buttress formation is activated by stress or strain.