Relieving the transfusion tissue traffic jam: a network model of radial transport in conifer needles

Abstract

The linear geometry of conifer leaves (e.g., pine needles) imposes architectural constraints on solute transport. The needle's structural solution to prevent axial stagnation, however, introduces an additional challenge to radial transport by restricting loading and unloading of sugar and water, respectively, to a narrow zone at the periphery of the vascular bundle. Moreover, a Casparian strip blocks apoplastic flow through the endodermis between the vasculature and photosynthetic tissue, forcing countercurrents of water and sugar to travel simultaneously through the cell lumen at this interface. In between these two potential bottlenecks is the transfusion tissue, a distinctive anatomical feature of conifer needles. Here we develop a network-based mathematical model to explore how the structure of the intervening transfusion tissue facilitates radial transport of sugar and water. To describe extravascular transport with cellular resolution, we construct networks from images of Pinus pinea needles obtained through X-ray microCT, as well as fluorescence and electron microscopy. Our results show that the physical separation of sugar and water pathways within the transfusion tissue mitigates the consequences of constricting flow at both the vascular access points and the endodermis.