Beyond efficiency: The multi-scale architecture of robust water transport in plants

Our understanding of physical and physiological mechanisms depends on the development of advanced technologies and tools to prove or re-evaluate established theories, and test new hypotheses. Water flow in land plants is a fascinating phenomenon, a vital component of the water cycle, and essential for life on Earth. The cohesion-tension theory (CTT), formulated more than a century ago and based on the physical properties of water, laid the foundation for our understanding of water transport in vascular plants. Numerous experimental tools have since been developed to evaluate various aspects of the CTT, such as the existence of negative hydrostatic pressure. This review focuses on the evolution of the experimental methods used to study water transport in plants, and summarizes the different ways to investigate the diversity of the xylem network structure and sap flow dynamics in various species. As water transport is documented at different scales, from the level of single conduits to entire plants, it is critical that new results be subjected to systematic cross-validation and that findings based on different organs be integrated at the whole-plant level. We also discuss the functional trade-offs between optimizing hydraulic efficiency and maintaining the safety of the entire transport system. Furthermore, we evaluate future directions in sap flow research and highlight the importance of integrating the combined effects of various levels of hydraulic regulation.

In this review, we discuss the evolution of xylem structure in the context of our current understanding of the biophysics of water transport in plants. Water transport in land plants occurs while water is under negative pressure and is thus in a metastable state. Vessels filled with metastable water are prone to dysfunction by cavitation whenever gas-filled voids appear in the vessel lumen. Cavitated vessels fill with air and are incapable of water transport until air bubbles dissolve. We know much more about how cavitations occur and the conditions under which air bubbles (embolisms) dissolve. This gives us an improved understanding of the relations hip between xylem structure and function.

Although the study of plants (botany) is one of the oldest sciences, relatively detailed quantitative theories of water transport in plant tissue have lagged behind those describing water transport in soils and other geologic materials which constitute the saturated and unsaturated zones. Many existing texts deal with various aspects of water transport in these earth materials, but little or nothing is devoted to the analogous transport of water in plant roots and tissue at a similar quantitative level. Yet the soil‐root‐stem water pathway is a major component of the subsurface hydrologic system. Evidently there is a need for both engineering and agricultural hydrologists to further develop their quantitative understanding of water movement in plant and soil‐plant systems. Modern quantitative theories of water transport in plants can be traced to concepts developed and disseminated effectively in landmark papers by Gradmann and van den Honert in 1928 and 1948 respectively. The material reviewed in this paper, while more advanced, is based on these concepts. Emphasis is placed on water movement in soil containing roots and on a general approach to water transport in living plant tissue. Detailed quantitative studies of water extraction by plant roots date back to studies by Gardner published in 1960. Many contemporary models are built around extraction functions in the Darcy‐Richards equation. Several such functions are listed in a table, and their applications, relative advantages, and limitations are discussed in the text. In a series of papers published in 1958, Philip developed the first detailed quantitative description of water transport in plant tissue. His approach resulted in a diffusion equation which could be written with water potential as the dependent variable. Philip's derivation assumed that water movement was primarily from vacuole to vacuole. Subsequent workers have refined and extended Philip's development to include water movement in cell walls and plasmodesmata. The development, interpretation, and application of these models over the past decade is presented in some detail. It can be argued that contemporary models of water transport in plant tissue are oversimplified. However, they have been subjected to some successful testing and they provide a framework within which to devise experiments. Moreover, the recent development of sophisticated experimental techniques should result in more detailed model testing during the 1980's.

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The pattern of water transport in plants is an important part in ecology study and is the theoretical basis of water conservation of plants, which have gotten more attention worldwide. The paper reviews the past studies of the computer simulation of water transport in plants and discusses the simulation models of water uptake of plant root systems, water transport within plants and canopy transpiration in plants. Based on the review and discussion, several areas most concerned about studies of the computer simulation of plants water transport are pointed out: (1) The study shall pay more attention to the microcosmic mechanism of water transport within plants. (2) The fact of growth of plants should be considered while the water transport model of plants is established. And the water transport models of plants and the growth models of plants should be interconnected and matched simultaneously in space and time. (3) Combined with soil-plant-atmosphere continuum, the mutual interaction of plant growth and plant water transport in different areas should be considered to study plant water transport.

Water transport in plants occurs along various paths and is driven by gradients in its free energy. It is generally considered that the mode of transport, being either diffusion or bulk flow, is a passive process, although energy may be required to sustain the forces driving water flow. This review aims at putting water flow at the various organisational levels (cell, organ, plant) in the context of the energy that is required to maintain these flows. In addition, the question is addressed (1) whether water can be transported against a difference in its chemical free energy, 'water potential' (Ψ), through, directly or indirectly, active processes; and (2) whether the energy released when water is flowing down a gradient in its energy, for example during day-time transpiration and cell expansive growth, is significant compared to the energy budget of plant and cell. The overall aim of review is not so much to provide a definite 'Yes' and 'No' to these questions, but rather to stimulate discussion and raise awareness that water transport in plants has its real, associated, energy costs and potential energy gains.

Holbrook and Zwieniecki reply: Terry Goldman is correct in suggesting that providing plants with higher carbon dioxide concentrations can result in both water conservation and enhanced photosynthesis. Indeed, CO2 fertilization is already used by many commercial growers. However, enclosed growing systems have huge energy costs associated with cooling and are thus unsuited for large-scale agricultural production.On the planetary scale, we are currently conducting such an experiment, albeit in an uncontrolled fashion. Increased atmospheric CO2 due to human activities such as fossil-fuel combustion and land clearing is estimated to have increased terrestrial photosynthetic output. However, at the same time, rising temperatures due to higher greenhouse gas concentrations increase the water demands placed on plants and are predicted to alter the frequency and intensity of precipitation events. Thus, although elevated CO2 can improve the efficiency of photosynthesis, there appears to be no free lunch.Jean Roy’s letter suggests that our Quick Study on water transport in trees should “teach the controversy,” so to speak. However, there is no scientific controversy regarding the cohesion-tension theory of water transport in plants. In the early 1990s, there was a short-term challenge to the theory due to discrepancies observed by Ulrich Zimmermann using a pressure probe. Subsequent refinements of that measurement technique by Zimmermann and others eliminated those concerns. 1 1. P. J. Melcher, F. C. Meinzer, D. E. Yount, G. Goldstein, U. Zimmermann, J. Exp. Bot. 49, 1757 (1998). https://doi.org/10.1093/jxb/49.327.1757 Since then no xylem water transport data have been found to be inconsistent with the cohesion-tension theory. Nor has any alternative mechanism been proposed that can explain the transport of water in plants. Publication of the reference Roy cites prompted 45 prominent plant biologists to protest. 2 2. G. Angeles et al. , New Phytol. 163, 451 (2004). https://doi.org/10.1111/j.1469-8137.2004.01142.x The editor’s response was that the paper by Zimmermann and coauthors should be perceived as representing the “views and opinions” of the authors and not as a review of the current state of knowledge appropriate for newcomers to the field. 3 3. I. Woodward, New Phytol. 163, 453 (2004). https://doi.org/10.1111/j.1469-8137.2004.01141.x Finally, we stand by our citation of W. F. Pickard’s 1981 work as an outstanding treatment of water transport in plants. That paper is particularly appropriate for the readers of Physics Today because it assumes high literacy in the physical sciences rather than detailed knowledge of plant anatomy. REFERENCESSection:ChooseTop of pageREFERENCES <<1. P. J. Melcher, F. C. Meinzer, D. E. Yount, G. Goldstein, U. Zimmermann, J. Exp. Bot. 49, 1757 (1998). https://doi.org/10.1093/jxb/49.327.1757 , Google ScholarCrossref, CAS2. G. Angeles et al. , New Phytol. 163, 451 (2004). https://doi.org/10.1111/j.1469-8137.2004.01142.x , Google ScholarCrossref3. I. Woodward, New Phytol. 163, 453 (2004). https://doi.org/10.1111/j.1469-8137.2004.01141.x , Google ScholarCrossref© 2008 American Institute of Physics.