The Widened Pipe Model of plant hydraulic evolution.

Shaping global water and carbon cycles, plants lift water from roots to leaves through xylem conduits. The importance of xylem water conduction makes it crucial to understand how natural selection deploys conduit diameters within and across plants. Wider conduits transport more water but are likely more vulnerable to conduction-blocking gas embolisms and cost more for a plant to build, a tension necessarily shaping xylem conduit diameters along plant stems. We build on this expectation to present the Widened Pipe Model (WPM) of plant hydraulic evolution, testing it against a global dataset. The WPM predicts that xylem conduits should be narrowest at the stem tips, widening quickly before plateauing toward the stem base. This universal profile emerges from Pareto modeling of a trade-off between just two competing vectors of natural selection: one favoring rapid widening of conduits tip to base, minimizing hydraulic resistance, and another favoring slow widening of conduits, minimizing carbon cost and embolism risk. Our data spanning terrestrial plant orders, life forms, habitats, and sizes conform closely to WPM predictions. The WPM highlights carbon economy as a powerful vector of natural selection shaping plant function. It further implies that factors that cause resistance in plant conductive systems, such as conduit pit membrane resistance, should scale in exact harmony with tip-to-base conduit widening. Furthermore, the WPM implies that alterations in the environments of individual plants should lead to changes in plant height, for example, shedding terminal branches and resprouting at lower height under drier climates, thus achieving narrower and potentially more embolism-resistant conduits.

The total path length hydraulic resistance according to known anatomical patterns: What is the shape of the root-to-leaf tension gradient along the plant longitudinal axis?

Xylem conduit diameter widens from leaf tip to stem base and how this widening affects the total hydraulic resistance (RTOT) and the gradient of water potential (Ψxyl) has never been thoroughly investigated. Data of conduit diameter of Acer pseudoplatanus,Fagus sylvatica and Picea abies were used to model the axial variation of RTOT and Ψxyl. The majority of RTOT (from 79 to 98%) was predicted to be confined within the leaf/needle. This means that the xylem conduits of stem and roots, accounting for nearly the total length of the hydraulic path, theoretically provide a nearly negligible contribution to RTOT. Consequently, a steep gradient of water potentials was predicted to develop within the leaf/needle base, whereas lower in the stem water potentials approximate those of rootlets. Our results would suggest that the strong partitioning of RTOT between leaves/needles coupled with basal conduit widening is of key importance for both hydraulic safety against drought-induced embolism formation and efficiency, as it minimizes the exposure of stem xylem to high tensions and makes the total plant's conductance substantially independent of body size.

Axial anatomy of the leaf midrib provides new insights into the hydraulic architecture and cavitation patterns of Acer pseudoplatanus leaves.

The structure of leaf veins is typically described by a hierarchical scheme (e.g. midrib, 1st order, 2nd order), which is used to predict variation in conduit diameter from one order to another whilst overlooking possible variation within the same order. We examined whether xylem conduit diameter changes within the same vein order, with resulting consequences for resistance to embolism. We measured the hydraulic diameter (Dh), and number of vessels (VN) along the midrib and petioles of leaves of Acer pseudoplatanus, and estimated the leaf area supplied (Aleaf-sup) at different points of the midrib and how variation in anatomical traits affected embolism resistance. We found that Dh scales with distance from the midrib tip (path length, L) with a power of 0.42, and that VN scales with Aleaf-sup with a power of 0.66. Total conductive area scales isometrically with Aleaf-sup. Embolism events along the midrib occurred first in the basipetal part and then at the leaf tip where vessels are narrower. The distance from the midrib tip is a good predictor of the variation in vessel diameter along the 1st order veins in A. pseudoplatanus leaves and this anatomical pattern seems to have an effect on hydraulic integrity since wider vessels at the leaf base embolize first.

Tree differences in primary and secondary growth drive convergent scaling in leaf area to sapwood area across Europe.

Trees scale leaf (AL ) and xylem (AX ) areas to couple leaf transpiration and carbon gain with xylem water transport. Some species are known to acclimate in AL  : AX balance in response to climate conditions, but whether trees of different species acclimate in AL  : AX in similar ways over their entire (continental) distributions is unknown. We analyzed the species and climate effects on the scaling of AL vs AX in branches of conifers (Pinus sylvestris, Picea abies) and broadleaved (Betula pendula, Populus tremula) sampled across a continental wide transect in Europe. Along the branch axis, AL and AX change in equal proportion (isometric scaling: b Ëœ 1) as for trees. Branches of similar length converged in the scaling of AL vs AX with an exponent of b = 0.58 across European climates irrespective of species. Branches of slow-growing trees from Northern and Southern regions preferentially allocated into new leaf rather than xylem area, with older xylem rings contributing to maintaining total xylem conductivity. In conclusion, trees in contrasting climates adjust their functional balance between water transport and leaf transpiration by maintaining biomass allocation to leaves, and adjusting their growth rate and xylem production to maintain xylem conductance.

A standardization method to disentangle environmental information from axial trends of xylem anatomical traits.

Anatomical traits such as xylem conduit diameter and vessel connectivity are fundamental characteristics of the hydraulic architecture of vascular plants. Stem xylem conduits are narrow at the stem apex, and this confers resistance to embolisms that might otherwise be induced by large, negative water potentials at the top of tall trees. Below the apex, conduits progressively widen and this characteristic minimizes effects of path length on total hydraulic resistance. While interconnections among xylem vessels have been noted for decades, their role(s) are not fully clarified. For example, we do not know if they allow water to bypass embolized vessels, or increase the risk of spread of embolisms, or how their arrangement varies within a tree. Here we demonstrate the benefit of removing the independent effect of stem length on assessment of effects of external (e.g., climatic) factors on such xylem traits. We measured the hydraulic diameter (Dh) and vessel conductivity index (VCI) along the stem of 21 shrubs/trees of similar height (1.19 < H < 5.45 m) belonging to seven Acacia species, across a wide aridity gradient in Australia. All trees showed similar scaling exponents of Dh (b = 0.33) and VCI (b = 0.53) vs axial distance from the apex (L), thus conforming with general patterns in woody plants. After de-trending for L, neither Dh (P = 0.21) nor VCI (P = 0.109) differed across the aridity gradient. We found that across a wide gradient of aridity, climate had no effect on xylem anatomy of Acacia spp, which was instead dictated by axial distances from stem apices. We argue that the use of standardization procedures to filter out intrinsic patterns of vascular traits is an essential step in assessing climate-driven modifications of xylem architecture.

Allometric Trajectories and "Stress": A Quantitative Approach.

The term "stress" is an important but vague term in plant biology. We show situations in which thinking in terms of "stress" is profitably replaced by quantifying distance from functionally optimal scaling relationships between plant parts. These relationships include, for example, the often-cited one between leaf area and sapwood area, which presumably reflects mutual dependence between sources and sink tissues and which scales positively within individuals and across species. These relationships seem to be so basic to plant functioning that they are favored by selection across nearly all plant lineages. Within a species or population, individuals that are far from the common scaling patterns are thus expected to perform negatively. For instance, "too little" leaf area (e.g., due to herbivory or disease) per unit of active stem mass would be expected to incur to low carbon income per respiratory cost and thus lead to lower growth. We present a framework that allows quantitative study of phenomena traditionally assigned to "stress," without need for recourse to this term. Our approach contrasts with traditional approaches for studying "stress," e.g., revealing that small "stressed" plants likely are in fact well suited to local conditions. We thus offer a quantitative perspective to the study of phenomena often referred to under such terms as "stress," plasticity, adaptation, and acclimation.

Rhizophoraceae Mangrove Saplings Use Hypocotyl and Leaf Water Storage Capacity to Cope with Soil Water Salinity Changes.

Some of the most striking features of Rhizophoraceae mangrove saplings are their voluminous cylinder-shaped hypocotyls and thickened leaves. The hypocotyls are known to serve as floats during seed dispersal (hydrochory) and store nutrients that allow the seedling to root and settle. In this study we investigate to what degree the hypocotyls and leaves can serve as water reservoirs once seedlings have settled, helping the plant to buffer the rapid water potential changes that are typical for the mangrove environment. We exposed saplings of two Rhizophoraceae species to three levels of salinity (15, 30, and 0-5‰, in that sequence) while non-invasively monitoring changes in hypocotyl and leaf water content by means of mobile NMR sensors. As a proxy for water content, changes in hypocotyl diameter and leaf thickness were monitored by means of dendrometers. Hypocotyl diameter variations were also monitored in the field on a Rhizophora species. The saplings were able to buffer rapid rhizosphere salinity changes using water stored in hypocotyls and leaves, but the largest water storage capacity was found in the leaves. We conclude that in Rhizophora and Bruguiera the hypocotyl offers the bulk of water buffering capacity during the dispersal phase and directly after settlement when only few leaves are present. As saplings develop more leaves, the significance of the leaves as a water storage organ becomes larger than that of the hypocotyl.

Osmolality and Non-Structural Carbohydrate Composition in the Secondary Phloem of Trees across a Latitudinal Gradient in Europe.

Phloem osmolality and its components are involved in basic cell metabolism, cell growth, and in various physiological processes including the ability of living cells to withstand drought and frost. Osmolality and sugar composition responses to environmental stresses have been extensively studied for leaves, but less for the secondary phloem of plant stems and branches. Leaf osmotic concentration and the share of pinitol and raffinose among soluble sugars increase with increasing drought or cold stress, and osmotic concentration is adjusted with osmoregulation. We hypothesize that similar responses occur in the secondary phloem of branches. We collected living bark samples from branches of adult Pinus sylvestris, Picea abies, Betula pendula and Populus tremula trees across Europe, from boreal Northern Finland to Mediterranean Portugal. In all studied species, the observed variation in phloem osmolality was mainly driven by variation in phloem water content, while tissue solute content was rather constant across regions. Osmoregulation, in which osmolality is controlled by variable tissue solute content, was stronger for Betula and Populus in comparison to the evergreen conifers. Osmolality was lowest in mid-latitude region, and from there increased by 37% toward northern Europe and 38% toward southern Europe due to low phloem water content in these regions. The ratio of raffinose to all soluble sugars was negligible at mid-latitudes and increased toward north and south, reflecting its role in cold and drought tolerance. For pinitol, another sugar known for contributing to stress tolerance, no such latitudinal pattern was observed. The proportion of sucrose was remarkably low and that of hexoses (i.e., glucose and fructose) high at mid-latitudes. The ratio of starch to all non-structural carbohydrates increased toward the northern latitudes in agreement with the build-up of osmotically inactive C reservoir that can be converted into soluble sugars during winter acclimation in these cold regions. Present results for the secondary phloem of trees suggest that adjustment with tissue water content plays an important role in osmolality dynamics. Furthermore, trees acclimated to dry and cold climate showed high phloem osmolality and raffinose proportion.