Xylogenesis: Coniferous Trees of Temperate Forests Are Listening to the Climate Tale during the Growing Season But Only Remember the Last Words!

Abstract

The complex inner mechanisms that create typical conifer tree-ring structure (i.e. the transition from large, thin-walled earlywood cells to narrow, thick-walled latewood cells) were recently unraveled. However, what physiological or environmental factors drive xylogenesis key processes remain unclear. Here, we aim to quantify the influence of seasonal variations in climatic factors on the spectacular changes in the kinetics of wood cell differentiation and in the resulting treering structure. Wood formation was monitored in three sites over 3 years for three coniferous species (Norway spruce [Picea abies], Scots pine [Pinus sylvestris], and silver fir [Abies alba]). Cell differentiation rates and durations were calculated and related to tracheid final dimensions and corresponding climatic conditions. On the one hand, we found that the kinetics of cell enlargement and the final size of the tracheids were not explained by the seasonal changes in climatic factors. On the other hand, decreasing temperatures strongly constrained cell wall deposition rates during latewood formation. However, the influence of temperature was permanently written into tree-ring structure only for the very last latewood cells, when the collapse of the rate of wall deposition was no longer counterbalanced by the increase of its duration. Our results show that the formation of the typical conifer tree-ring structure, in normal climatic conditions, is only marginally driven by climate, suggesting strong developmental control of xylogenesis. The late breakage of the compensatory mechanism at work in the wall deposition process appears as a clue to understand the capacity of the maximum latewood density to record past temperature conditions.

Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy

“…The compensation observed between rates and durations of tracheid differentiation notably appears as an essential mechanism that allows conifers to cope with environmental change. In addition to its role in dealing with seasonal climatic variations (Cuny & Rathgeber, ) and mitigating the impacts of unusual extreme climatic events such as drought (Balducci et al, ), we show that this rate‐duration compensation preserves the characteristic tree‐ring structure optimized for mechanical stability and water transport across a wide range of thermal conditions. This study thus provides new fundamental insights into tree growth, as well as mechanistic understanding of responses of trees to climate change.…”

“…Concerning the control of the kinetics of cell differentiation processes, the rate and the duration have usually been considered separately. On the one hand, the control of the rate has been associated with a direct influence of temperature on metabolism (Balducci et al, ; Cuny et al, ; Cuny & Rathgeber, ; Mellerowicz et al, ; Proseus, Ortega, & Boyer, ; Proseus, Zhu, & Boyer, ). Cell enlargement implies numerous enzyme reactions (e.g., cutting chemical bonds to loosen the wall, synthesizing, transporting, delivering, and inserting new wall polymers) with high activation energies and thus likely being very sensitive to temperature (Proseus et al, ; Proseus et al, ), whereas the processes involved in wall thickening (e.g., cellulose and lignin biosynthesis, transport, and deposition) are inhibited at temperatures still favourable for photosynthesis (Körner, ; Körner, ; Simard et al, ).…”

“…Indeed, to date, the mechanisms coordinating the durations and rates of cell differentiation processes remain unknown. For wall thickening, a mechanism linking the rate of secondary wall deposition to the date of apoptosis may explain the observed coupling (Cuny & Rathgeber, ; Groover & Jones, ). But why and how this coupling is broken during latewood formation is still unexplained (Cuny et al, ).…”

“…In order to study accurately the mechanisms by which xylogenesis and tree‐ring structure respond to air temperature, the kinetics of tracheid differentiation and the resulting dimensions of xylem cells were compared with the exact thermal conditions prevailing during the process of formation (Figure S2). Air temperature can be considered as a good indicator of cambium temperature (see Cuny & Rathgeber, ). For example, the kinetics of enlargement and the final cross‐sectional area of a cell were compared with the mean air temperature experienced during the enlargement of this cell.…”

“…The elevation gradient corresponds to a range of 8°C in mean annual temperature (Table ). We used a novel modelling approach to associate cell differentiation kinetics and final cell dimensions with the corresponding thermal conditions (Cuny & Rathgeber, ; Figure S2). We establish the following three hypotheses:Hypothesis Lower site temperature is associated with a later start, earlier ending and shorter duration of xylem tissue formation.Hypothesis Due to these adjustments in phenology, the first and last xylem cells formed in the growing season experience similar thermal conditions during their differentiation along the thermal gradient.Hypothesis Consequently, the kinetics (rates and durations) of the cell differentiation processes (cell enlargement and wall thickening), which determine the final dimensions of xylem cells and thus shape the tree‐ring structure, are quite similar despite contrasted thermal environments.…”