Giai Petit

Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates

Angiosperm hydraulic performance is crucially affected by the diameters of vessels, the water conducting conduits in the wood. Hydraulic optimality models suggest that vessels should widen predictably from stem tip to base, buffering hydrodynamic resistance accruing as stems, and therefore conductive path, increase in length. Data from 257 species (609 samples) show that vessels widen as predicted with distance from the stem apex across angiosperm orders, habits and habitats. Standardising for stem length, vessels are only slightly wider in warm/moist climates and in lianas, showing that, rather than climate or habit, plant size is by far the main driver of global variation in mean vessel diameter. Terminal twig vessels become wider as plant height increases, while vessel density decreases slightly less than expected tip to base. These patterns lead to testable predictions regarding evolutionary strategies allowing plants to minimise carbon costs per unit leaf area even as height increases.

Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem

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.

Distilling allometric and environmental information from time series of conduit size: the standardization issue and its relationship to tree hydraulic architecture.

Trees are among the best natural archives of past environmental information. Xylem anatomy preserves information related to tree allometry and ecophysiological performance, which is not available from the more customary ring-width or wood-density proxy parameters. Recent technological advances make tree-ring anatomy very attractive because time frames of many centuries can now be covered. This calls for the proper treatment of time series of xylem anatomical attributes. In this article, we synthesize current knowledge on the biophysical and physiological mechanisms influencing the short- to long-term variation in the most widely used wood-anatomical feature, namely conduit size. We also clarify the strong mechanistic link between conduit-lumen size, tree hydraulic architecture and height growth. Among the key consequences of these biophysical constraints is the pervasive, increasing trend of conduit size during ontogeny. Such knowledge is required to process time series of anatomical parameters correctly in order to obtain the information of interest. An appropriate standardization procedure is fundamental when analysing long tree-ring-related chronologies. When dealing with wood-anatomical parameters, this is even more critical. Only an interdisciplinary approach involving ecophysiology, wood anatomy and dendrochronology will help to distill the valuable information about tree height growth and past environmental variability correctly.

Plant physiology in theory and practice: An analysis of the WBE model for vascular plants

The theoretical model of West, Brown and Enquist (hereafter WBE) proposed the fractal geometry of the transport system as the origin of the allometric scaling laws observed in nature. The WBE model has either been criticized for some restrictive and biologically unrealistic constraints or its reliability debated on the evidence of empirical tests. In this work, we revised the structure of the WBE model for vascular plants, highlighting some critical assumptions and simplifications and discuss them with regard to empirical evidence from plant anatomy and physiology. We conclude that the WBE model had the distinct merit of shedding light on some important features such as conduit tapering. Nonetheless, it is over-simplistic and a revised model would be desirable with an ontogenetic perspective that takes some important phenomena into account, such as the transformation of the inner sapwood into heartwood and the effect of hydraulic constraints in limiting the growth in height.

AXIAL CONDUIT WIDENING IN WOODY SPECIES: A STILL NEGLECTED ANATOMICAL PATTERN

Within a tree the lumen of the xylem conduits varies widely (by at least 1 order of magnitude). Transversally in the stem conduits are smaller close to the pith and larger in the outermost rings. Axially (i.e. from petioles to roots) conduits widen from the stem apex downwards in the same tree ring. This axial variation is proposed as being the most efficient anatomical adjustment for stabilizing hydraulic path-length resistance with the progressive growth in height. The hydrodynamic (i.e. physical) constraint shapes the whole xylem conduits column in a very similar way in different species and environments. Our aim is to provide experimental evidence that the axial conduit widening is an ineluctable feature of the vascular system in plants. If evolution has favoured efficient distribution networks (i.e. total resistance is tree-size independent) the axial conduit widening can be predicted downwards along the stem. Indeed, in order to compensate for the increase in path length with growth in height the conduit size should scale as a power function of tree height with an exponent higher than 0.2. Similarly, this approach could be applied in branches and roots but due to the different lengths of the path roots-leaves the patterns of axial variations of conduit size might slightly deviate from the general widening trend. Finally, we emphasize the importance of sampling standardization with respect to tree height for correctly comparing the anatomical characteristics of different individuals.

Hydraulic constraints limit height growth in trees at high altitude

• Low temperatures limit the fixation of photosynthates and xylogenesis. Here, we hypothesized that reduced longitudinal growth in trees at high altitude is related to the lower hydraulic efficiency of the transport system. • Apical buds of Norway spruce (Picea abies) trees at high and low elevation were heated during 2006 and 2007. At the end of the experiment, trees were felled. Longitudinal increments and tracheid lumen areas were measured along the stem. Apical hydraulic conductivity (k) was estimated from anatomical data. • Before heating, high-altitude trees showed fewer (P = 0.002) and smaller (P = 0.008) apical conduits, and therefore reduced k (P = 0.016) and stem elongation (P < 0.0001), in comparison with trees at low elevation. After 2 yr of heating, k increased at both high (P = 0.014) and low (P = 0.047) elevation. Only high-altitude trees showed increased stem elongation, which reached the same magnitude as that of controls at low elevation (P = 0.735). Heating around the apical shoots did not appear to induce significant changes in conduit dimension along the rest of the stem. • The total number and size of xylem elements at the stem apex are strongly constrained by low temperatures. Trees at high altitude are therefore prevented from building up an efficient transport system, and their reduced longitudinal growth reflects strong hydraulic limitations.

The challenge of tree height in Eucalyptus regnans: when xylem tapering overcomes hydraulic resistance

*Recent research suggests that increasing conduit tapering progressively reduces hydraulic constraints caused by tree height. Here, we tested this hypothesis using the tallest hardwood species, Eucalyptus regnans. *Vertical profiles of conduit dimensions and vessel density were measured for three mature trees of height 47, 51 and 63 m. *Mean hydraulic diameter (Dh) increased rapidly from the tree apex to the point of crown insertion, with the greatest degree of tapering yet reported (b > 0.33). Conduit tapering was such that most of the total resistance was found close to the apex (82-93% within the first 1 m of stem) and the path length effect was reduced by a factor of 2000. Vessel density (VD) declined from the apex to the base of each tree, with scaling parameters being similar for all trees (a = 4.6; b = -0.5). *Eucalyptus regnans has evolved a novel xylem design that ensures a high hydraulic efficiency. This feature enables the species to grow quickly to heights of 50-60 m, beyond the maximum height of most other hardwood trees.

Comparative axial widening of phloem and xylem conduits in small woody plants

Key messageAlong the stem axis phloem’s sieve elements increase in diameter basally at rates comparable to those of xylem conduits and in agreement with principles of hydraulic optimization.AbstractPlant physiology relies on the efficiency of the two long-distance transport systems of xylem and phloem. Xylem architecture comprises conduits of small dimensions towards the stem apex, where transpiration-induced tensions are the highest along the root-to-leaves hydraulic pathway, and widen basally to minimize the path length resistance to water flow. Instead, information on phloem anatomy and allometry is extremely scarce, although potentially relevant for the efficiency of sugar transportation. We measured the hydraulic diameter (Dh) of both xylem conduits and phloem sieve elements in parallel at different heights along the stem of a small tree of Picea abies, Fraxinus excelsior and Salix eleagnos. Dh increased from the stem apex to base in both xylem and phloem, with a higher scaling exponent (b) of sieve elements than that of tracheids in the conifer (0.19 vs. 0.14) and lower than that of vessels in the angiosperms (0.14–0.22 vs. 0.19–0.40). In addition, sieve elements were larger than tracheids in P. abies and narrower than angiosperms vessels at any height along the stem. In conclusion, axial conduit widening would seem to be a key feature of both xylem and phloem long-distance transport architectures.

Divergent climate response on hydraulic-related xylem anatomical traits of Picea abies along a 900-m altitudinal gradient

Climate change can induce substantial modifications in xylem structure and water transport capacity of trees exposed to environmental constraints. To elucidate mechanisms of xylem plasticity in response to climate, we retrospectively analysed different cell anatomical parameters over tree-ring series in Norway spruce (Picea abies L. Karst.). We sampled 24 trees along an altitudinal gradient (1200, 1600 and 2100 m above sea level, a.s.l.) and processed 2335 ± 1809 cells per ring. Time series for median cell lumen area (MCA), cell number (CN), tree-ring width (RW) and tree-ring-specific hydraulic conductivity (Kr) were crossed with daily temperature and precipitation records (1926-2011) to identify climate influence on xylem anatomical traits. Higher Kr at the low elevation site was due to higher MCA and CN. These variables were related to different aspects of intra-seasonal climatic variability under different environmental conditions, with MCA being more sensitive to summer precipitation. Winter precipitation (snow) benefited most parameters in all the sites. Descending the gradient, sensitivity of xylem features to summer climate shifted mostly from temperature to precipitation. In the context of climate change, our results indicate that higher summer temperatures at high elevations will benefit cell production and xylem hydraulic efficiency, whereas reduced water availability at lower elevations could negatively affect tracheids enlargement and thus stem capacity to transport water.

Retrospective Analysis of Wood Anatomical Traits Reveals a Recent Extension in Tree Cambial Activity in Two High-Elevation Conifers

The study of xylogenesis or wood formation is a powerful, yet labor intensive monitoring approach to investigate intra-annual tree growth responses to environmental factors. However, it seldom covers more than a few growing seasons, so is in contrast to the much longer lifespan of woody plants and the time scale of many environmental processes. Here we applied a novel retrospective approach to test the long-term (1926–2012) consistency in the timing of onset and ending of cambial activity, and in the maximum cambial cell division rate in two conifer species, European larch and Norway spruce at high-elevation in the Alps. We correlated daily temperature with time series of cell number and lumen area partitioned into intra-annual sectors. For both species, we found a good correspondence (1–10 days offset) between the periods when anatomical traits had significant correlations with temperature in recent decades (1969–2012) and available xylogenesis data (1996–2005), previously collected at the same site. Yet, results for the 1926–1968 period indicate a later onset and earlier ending of the cambial activity by 6–30 days. Conversely, the peak in the correlation between annual cell number and temperature, which should correspond to the peak in secondary growth rate, was quite stable over time, with just a minor advance of 4–5 days in the recent decades. Our analyses on time series of wood anatomical traits proved useful to infer on past long-term changes in xylogenetic phases. Combined with intensive continuous monitoring, our approach will improve the understanding of tree responses to climate variability in both the short- and long-term context.