Architectural solutions for hydraulically-coupled material transport in plants

Abstract

Whether for removal or retention, the movement of materials through a plant's body is a crucial aspect of its life. Much emphasis has been placed on the active biological processes involved in plant transport problems, but I argue that their physical and architectural solutions must also be considered. In this dissertation, I use mathematical modeling, complemented by imaging studies and physiological measurements, to explore the structural basis for the hydraulically-coupled transport of materials in plants. In Chapter 1, I explore the structural properties required for safe and efficient desalination in secreting halophytes. Efforts to understand and manipulate gland-mediated secretion typically focus on the optimization and regulation of ion transporters but often neglect its biomechanical underpinnings. Using Nolana mollis as a model system, I integrate anatomy, physiology, and theory to show how the structural maintenance of a distinct subcuticular space is necessary to circumvent the energetic limitations of ion transport against steep concentration gradients across the cell membrane. I show that the integrity of this separate compartment determines the functional state of the salt gland and depends on the fracture mechanics of the gland’s cuticle. By exploring the biomechanical determinants of secretory salt tolerance, this work offers insights into alternative approaches for engineering salt-tolerant agriculture or biomimetic desalination devices. In Chapter 2, I clarify the physiological function of the enigmatic transfusion tissue of conifer needles, which has remained unclear despite extensive anatomical characterization. Ubiquitous among conifer needles, the transfusion tissue mediates the radial transport of water and sugar between the endodermis and axial vasculature and faces potential bottlenecks at both of its boundaries, where the opposition of sugar and water flows may frustrate sugar export. Using anatomical data from imaging studies of Pinus pinea needles, I develop a network model of the transfusion tissue to explore how its structure and composition affect the delivery of sugars to the axial phloem. I show that bisection of the transfusion tissue into separate water- and sugar-conducting pathways, along with a branching structure between the vasculature and endodermis, mitigates interference between the inbound diffusive sugar flux and the outbound advective water flux. This work resolves the structure-based function of the transfusion tissue under conditions free of physiological stress and establishes the groundwork for further research of the transfusion tissue's physiology in other gymnosperms. In Chapter 3, I model the coupled transport of methane and water through wetland trees to understand the structural and environmental determinants of arboreal methane emissions. Trees are important pathways for methane, which can be taken up by roots within the waterlogged, anoxic zone and released from the trunk directly into the atmosphere. I develop a model of a typical tree within a swamp to explore methane dynamics over a range of environmental and physiological conditions, in the context of measurements made in wetland Nyssa sylvatica. The model explores the parameter space of fundamental properties that affect patterns of arboreal methane emissions. Using insights from the model, I identify pertinent questions to advise the design of future empirical studies. By describing the relevant physiological and environmental parameters of this problem, the model provides a foundation for scaled-up predictions of tree-mediated methane emissions. Given the near-infinite solution space for a plant's architecture that arises from its modularity, modeling offers a useful approach to organizing and distilling the physiologically relevant information. In this dissertation, I build models to explain these transport phenomena and further ground and contextualize those models in empirical observations.