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.

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.

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.

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.

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.

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.