Allometric Trajectories and \u201cStress\u201d: A Quantitative Approach

The term \u201cstress\u201d is an important but vague term in plant biology. We show situations in which thinking in terms of \u201cstress\u201d 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 source 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, \u201ctoo little\u201d 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 \u201cstress,\u201d without need for recourse to this term. Our approach contrasts with traditional approaches for studying \u201cstress,\u201d e.g. revealing that small \u201cstressed\u201d 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 \u201cstress,\u201d plasticity, adaptation, and acclimation

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 with a hierarchical scheme (e.g. midrib, 1st order, 2nd order), that is used to predict variation in conduit diameter from one order to another overlooking possible variation within the same order. We tested whether xylem conduit diameter changes within the same vein order, with consequences on resistance to embolism. We measured the hydraulic diameter (Dh), and number of vessels (VNo) along the midrib and petioles of Acer pseudoplatanus leaves. We estimated the leaf area supplied (LAsup) at different points of the midrib and how variation in anatomical traits affected embolism resistance. Our results showed that Dh scales with distance from the midrib tip (L) with a power of 0.42, and that VNo scales with LAsup with a power of 0.66. Total conductive area scales isometrically with the LAsup. Embolism events along the midrib occurred first in the basipetal part and afterwards at the leaf tip where vessels are narrower. The distance from the midrib tip well predicts the variations in vessels diameter along the 1st order vein in sycamore maple leaves and this anatomical pattern seems to have an effect on hydraulic safety since wider vessels at the leaf base embolize first

The hydraulic architecture of the plants: study of the allometric relations in stem and leaves

The xylem in plants is formed by interconnected dead cells that allow the flow of water from the roots to the leaves. The ascent of sap is mainly passive and it is driven by water evaporation from the mesophyll cell walls in the leaf. The water evaporation generates capillary suction on the menisci at the micro-porous of cell walls, causing negative hydrostatic pressure that propagates down the water column in the xylem. Due to plants grow in height the length of the hydraulic path increases progressively posing the question whether the hydraulic resistance increases accordingly. There is evidence that plants have evolved xylem structures that compensate the possible increase of the hydraulic resistance imposed by path length, namely the tip-to-base conduits widening. Conduits widening has been reported in several species, both angiosperms and conifers, showing that the degree of widening from tip to the base of the stem is very similar among species, or in other words, that plants converge towards a universal xylem structure. Nevertheless, several points on the hydraulic architecture of plants remain to be elucidated. A largely debated point is whether xylem anatomical traits (e.g. the absolute cell size) change with climatic conditions. Moreover, whether and how the conduits widening in the stem may affect the xylem anatomy of the leaf is still not fully understood. This PhD project aims to widen our understanding of the allometric relations of leaves and stem xylem, considering how the environmental conditions and the height of the plant affect the hydraulic architecture of the water transport system. A methodological study (Study 1) has been performed on the xylem tissue of stems of Acacia trees grown in different water availability conditions. The main result was that, once the anatomical data were standardized for the tree height, the hydraulic architecture of the xylem did not change in relation to the environmental conditions. Two studies have been performed on the hydraulic architecture of leaves. The main focus was on the anatomical traits of the xylem conduits in relation to the leaf dimensions and/or the position in the tree crown (height from the base of the stem). The main results were that the xylem traits scaled with the leaf area independently by the position in the crown (Study 2). A fine analysis of the leaf midrib (i.e. major leaf vein) has shown a rigid hydraulic architecture and tissues coordination (Study 3) that was well predicted by the distance from the leaf tip. Both studies showed that the dimensions of the terminal veins were conserved among leaves and within leaf suggesting that the hydraulic architecture of the xylem in the leaf evolved in a way to guarantee an equal distribution of the hydraulic resistances (and thus of the water) among leaves and within the leaf lamina. Finally, we implemented the anatomical data of both stem and leaf into a hydraulic model to assess the distribution of resistances along the hydraulic path to evaluate how the anatomy of the transport system affects the physiology of the entire tree (Study 4). This thesis has highlighted that the path length (i.e. the height of the plant and the dimensions of the leaf) is the main factor affecting the hydraulic architecture of the tree. The conduit dimension in both stem and leaf are determined by the distance from the terminal parts, stem apex or leaf tip respectively. Climatic conditions resulted to have marginal (non-significant) effect on the stem anatomical traits. In the leaf, the dimensions of the xylem conduits are statistically invariant with changes in plant size. This rigid hydraulic architecture of the tree, from the stem to the leaf, allows minimizing the effect of the path length on the hydraulic resistance, confining nearly the whole gradient of water potential within the leaves.Lo xilema nelle piante è formato da cellule morte interconnesse che consentono il flusso di acqua dalle radici alle foglie. L'ascesa della linfa è principalmente passiva ed è guidata dall'evaporazione dell'acqua dalle pareti cellulari del mesofillo nella foglia. L'evaporazione dell'acqua genera un'aspirazione capillare sui menischi a livello dei micro-pori delle pareti cellulari, causando una pressione idrostatica negativa che si propaga lungo la colonna d'acqua nello xilema. A causa dell’aumento in altezza delle piante, la lunghezza del percorso idrico aumenta progressivamente ponendo la domanda se la resistenza idraulica aumenta di conseguenza. Vi è evidenza che le piante hanno evoluto strutture xilematiche che compensano il possibile aumento della resistenza idraulica imposta dall'aumento della lunghezza del percorso, come ad esempio l'allargamento dei condotti dalla punta alla base. L’allargamento dei condotti è stato osservato in diverse specie, sia angiosperme sia conifere, dimostrando che il grado di allargamento dalla punta alla base dello stelo è molto simile tra le specie, o in altre parole, che le piante convergono verso una struttura xilema universale. Tuttavia, restano da chiarire diversi punti sull'architettura idraulica delle piante. Un punto largamente dibattuto è se tratti anatomici dello xilema (ad esempio la dimensione assoluta delle cellule) cambiano con le condizioni climatiche. Inoltre, se e come i condotti che si allargano nello stelo possano influenzare l'anatomia dello xilema della foglia non è ancora completamente compreso. Il progetto di questo dottorato mira ad ampliare la nostra comprensione delle relazioni allometriche nello xilema delle foglie e del fusto, considerando come le condizioni ambientali e l'altezza della pianta possano influenzare l'architettura idraulica del sistema di trasporto dell'acqua. Uno studio metodologico (Studio 1) è stato eseguito sul tessuto xilematico di fusti di alberi di acacia cresciuti in diverse condizioni di disponibilità idrica. Il risultato principale è stato che, una volta che i dati anatomici sono stati standardizzati per l'altezza dell'albero, l'architettura idraulica dello xilema non è cambiata in relazione alle condizioni ambientali. Sono stati eseguiti due studi sull'architettura idraulica delle foglie. L'obiettivo principale degli studi riguardava i tratti anatomici dei condotti dello xilema in relazione alle dimensioni della foglia e / o alla posizione nella chioma dell'albero (altezza dalla base del fusto). Dai risultati si evince che i tratti dello xilema si ridimensionano in base all'area fogliare indipendentemente dalla posizione nella chioma (Studio 2). Un'analisi fine della nervatura principale della foglia ha mostrato una rigida architettura idraulica e la coordinazione dei tessuti (Studio 3), ben predetta dalla distanza dalla punta della foglia. Entrambi gli studi hanno dimostrato che le dimensioni delle vene terminali sono conservate tra le foglie e all'interno della stessa foglia, suggerendo che l'architettura idraulica dello xilema si è evoluta in modo da garantire distribuzione omogenea delle resistenze idrauliche (e quindi dell'acqua) tra le foglie e lungo la lamina fogliare. Infine, abbiamo implementato i dati anatomici di fusto e foglia in un modello idraulico per stimare la distribuzione delle resistenze lungo il percorso idraulico per valutare in che modo l'anatomia del sistema di trasporto influisca sulla fisiologia dell'intero albero (Studio 4). Questa tesi ha evidenziato che la lunghezza del percorso (vale a dire l'altezza della pianta e le dimensioni della foglia) è il fattore principale che influenza l'architettura idraulica dell'albero. La dimensione del condotto sia nel fusto che nella foglia è determinata dalla distanza dalle parti terminali, rispettivamente l'apice del fusto o la punta della foglia. Le condizioni climatiche risultano avere un effetto marginale (non significativo) sui tratti anatomici del fusto e nella foglia, le dimensioni dei condotti dello xilema sono statisticamente indipendenti rispetto alle variazioni nelle dimensioni della pianta. Questa rigida architettura idraulica dell'albero, dal fusto alla foglia, consente di minimizzare l'effetto della lunghezza del percorso sulla resistenza idraulica, confinando quasi l'intero gradiente del potenziale idrico all'interno delle foglie

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

Functional balance between leaf and xylem tissues is maintained under different soil water availability in Pinus sylvestris and Picea abies

Plants are composed by tight connected different tissues and organs that work in synchrony among each other guiding all physiological processes. The functionality of the entire organism depends on the resources allocation for the different organs that have to balance the cost and the benefit of the plant. The ratio between leaf biomass and xylem biomass is an extremely important plant trait since it links photosynthesis to transpiration efficiency and to respiratory costs. Resource availability have been reported to significantly affect the growth of trees. In limited resource environment trees present smaller leaves and shorter braches than plants grown in non-limiting conditions. The aim of this work is to evaluate if the resource allocation is maintained constant during ontogeny and if the ratio between leaf and xylem is preserved in different environmental conditions to guarantee the functionality of the system. We sampled branches of Pinus sylvestris and Picea abies grown on arid and mesic soils. For each the branch we measured the xylem volume and the leaf biomass produced each year and how they cumulate from the branch apex to the base. Our results showed that the cumulated leaf biomass and xylem volume scale linearly with the distance from the branch apex and the branches from the wet site, especially P. sylvestris\u2019 s, had more leaf biomass and xylem volume. This confirms that carbon allocation is conserved during the ontogeny and that the trees grown in non-limiting conditions have higher production. Moreover, the relation among leaf biomass and xylem volume showed a conserved allocation pattern in the two species with no effect of the environmental conditions. This demonstrates that these two traits are highly correlated and dependent on each other and that their functional balance is highly preserved to sustain the functionality of the tree independently by the resource availability

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

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