Exploratory workshop on – The significance of xylem hydraulic plasticity to reconstruct past environments, Kippel, Switzerland, May 2012, supported by the European Science Foundation
Climate plays a crucial role in determining the geographic distribution of plant species and communities (Garzon et al., 2011). The close relationship between climate and plants is reflected in functional adaptations and a large morphological and taxonomic diversity. One important functional trait represents water transport capacity through the xylem tissue, which is closely connected with a plant’s water use strategy and net primary productivity in a given environment. In fact, the xylem structure reflects the functional balance between efficient water transport to achieve optimal growth, minimum investment of construction costs to secure the xylem plumbing system, mechanical support of the assimilating leaves, and storage of water and nonstructural carbohydrates for defence and resistance to stress (von Arx et al., 2012). Although water conducting cells are dead when fully developed and functional, woody plants are able to acclimate their developing xylem to the changing environment before cell death, which is particularly relevant in perennial plants with a long generation cycle. Since these structural features remain permanently fixed and chronologically archived in wood, tree-ring anatomy offers the opportunity to add a ‘time component’ to functional mechanisms of xylem plasticity, and thus to reconstruct dynamics in ecological conditions (Eilmann et al., 2010; Fonti et al., 2010).
A European Science Foundation workshop brought together more than 30 experts to discuss current understanding of xylem plasticity and to explore limitations and future challenges in how a plant’s hydraulic system may respond to climate. The discussions were stimulated by seven scientific talks, short data set presentations on anatomical features measured along series of conifer tree rings from a nearby valley of Valais (Switzerland), and a half-day excursion to local projects of the WSL Institute (Birmensdorf, Switzerland). The participants, with expertise in fields such as xylem formation, wood anatomy, dendrochronology, and ecophysiology, recognized the additional value of an inter-disciplinary approach to identify research priorities. Here we present the major issues discussed.
Linking xylem anatomy to hydraulics
A first fundamental step towards the interpretation of xylem related signals is to assign the appropriate functional significance to anatomical structures. It is well known that characteristics of the xylem hydraulic architecture, such as the arrangement of conduits, their frequency, length, diameter, wall thickness, and pit characteristics, not only regulate hydraulic resistance (Christman & Sperry, 2010; Jansen et al., 2011), but also affect safety against hydraulic failure (Hoffmann et al., 2011; Lens et al., 2011). Recent efforts have been made in linking anatomical features with hydraulic traits such as resistance to cavitation (Mayr & Cochard, 2003; Lens et al., 2011). Despite recent progress, most of our insights are based on studies at the inter-specific level, comparing taxa from contrasting environmental sites or along environmental gradients. There is a lack of studies at the intra-specific level (Martínez-Vilalta et al., 2009; Schreiber et al., 2011), long-term modifications of xylem over the full life-span of trees, and variability along axial and radial profiles (Schulte, 2012).
‘Models are thus essential to integrate tree functioning with internal and external factors, offering huge benefits for climate reconstruction from xylem related signals, and prediction of plant distribution in response to climate change.’
Many questions raised at the workshop concerned the connectivity between conduits (Jansen et al., 2011; Lens et al., 2011), and hydraulic interactions across growth rings and between xylem and phloem (De Schepper & Steppe, 2010). Hydraulic measurements across growth rings and at the individual cell level should be explored more adequately (Mayr & Cochard, 2003; Christman & Sperry, 2010), and would provide a promising approach to link hydraulic parameters with micromorphological dimensions of tree rings, conduits and bordered pits. Such an approach would also be ideal to investigate functional and structural scaling between bordered pit size, pit frequency, and conduit dimensions (Schulte, 2012).
At a larger scale, more attention should be paid to hydraulic segmentation and isolation, which may be caused by variation in embolism resistance along the whole-plant hydraulic pathway, the role of conduit tapering in determining privileged pathways for water transport, and the hydraulic role of parenchyma as buffer tissue for water and nonstructural carbohydrate reserves. Techniques such as X-ray computed tomography, high throughput X-ray density, near-infrared spectroscopy (NIRS), magnetic resonance imaging (MRI), and cavitron offer promising possibilities to obtain detailed hydraulic parameters for a large number of samples.
Understanding xylogenesis to link carbon allocation with water transport
Another fundamental question is which environmental and/or internal signals trigger xylem formation and structure. The cambium is at the intersection between a plant’s water economy and carbon balance, with a tight connection to phloem and xylem (Fig. 1). It is therefore fundamental to understand the dynamic coupling of cambial activity with the carbon and water budget of a plant, as well as functional properties of cambial derivatives (Deslauriers et al., 2009). Recent progress has been made in defining the environmental signals that actually drive cambial division and xylogenesis, and in quantifying the relationships between cambial activity, phenology, conduit development, and climate (Rathgeber et al., 2011; Rossi et al., 2012). Interestingly, an increase in the duration of cell expansion from the stem apex to the base is found to play a key role in determining the lumen tapering of early-wood tracheids in Picea abies (Anfodillo et al., 2012).
There is a clear need to identify the impact of xylem structure and ecophysiology on cambial activity, especially considering the necessary time-lag and carry-over effects. In this context, there is special interest in conducting experiments on phloem and xylem development, and in applying stable isotope techniques, which may add a valuable short-term time component to our understanding of how trees are able to fine-tune their water–carbon balance (Eilmann et al., 2010; Wingate et al., 2010). Ideally, developmental data should be used to develop ‘time-explicit’ models of cambial activity, following statistical, structure–function, or process-based approaches.
Modelling hydraulic plasticity
A modelling approach is necessary to simplify the complexity of the xylem–phloem system, and to build up a mechanistic understanding of the carbon–water balance. There is a clear need to combine process-based models of whole-tree functioning with high resolution measurements such as sap flow, stem diameter fluctuations (De Schepper & Steppe, 2010), and oxygen or carbon isotopic data (Ogee et al., 2009) to examine the degree to which tree carbon and water relations are recorded in annual tree-ring structure (e.g. cell dimensions) and composition (e.g. isotopes). Well-designed process-based models not only integrate such mechanistic knowledge, but are also crucial for an in-depth understanding of tree functioning and an unambiguous interpretation of dendroclimatic signals. Models are thus essential to integrate tree functioning with internal and external factors, offering huge benefits for climate reconstruction from xylem related signals, and prediction of plant distribution in response to climate change (Fig. 1).
Key conclusions and future challenges
Understanding basic questions about xylem plasticity in trees is of special importance given current concerns about drought-induced tree mortality across the globe (Hoffmann et al., 2011). Major questions include the underlying evolutionary and genetic mechanisms (e.g. long-term adaptation via selective pressure; continuous, functional acclimation to local conditions), constraints, and potential ‘costs’ associated with xylem plasticity over a tree’s lifespan (Magnani, 2009). Even if direct effects of drought may not directly result in mortality due to hydraulic failure, increase in temperature and aridity may have an influence on the interconnected carbon cycle (von Arx et al., 2012). Current evidence suggests that there is little genetic diversity in cavitation resistance across populations, suggesting canalization as a result of uniform selection or homeostasis of water transport, although data available do not warrant generalizations yet (Lamy et al., 2011; Wortemann et al., 2011).
A huge database made available by dendrochronologists, including profiles of tree ring-width, wood density, stable isotopes, and anatomical features, is waiting to be decrypted. To fully exploit this potential, there is the need to re-visit and further explore structure–function relationships behind the plasticity of various features and parameters, from the individual cell level to whole-plant level, and from individual plants to populations. Collaboration between wood anatomists, plant ecophysiologists and modellers, combined with a standardization in protocols and sampling strategies across sites and within a tree are prerequisites that the scientific community should consider when aiming at a breakthrough in this field. A mechanistic understanding of the determinants and functioning of the plant hydraulic system requires integration across temporal and spatial scales, from studies at the intra-annual level to millennia, and from the individual tree to intra-specific variability across populations and forest communities. An opportunity to implement some of these future goals will be offered by the COST Action STReESS (FP1106), in which various participants of the European Science Foundation (ESF) workshop will be involved.
The authors thank the European Science Foundation for financial support to organize the workshop, and all participants for valuable discussions and helpful comments.