Fluid mechanics of nanopore transport in plants

Research output: Book/ReportPh.D. thesis

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Abstract

Like other multicellular organisms, plants must solve the problem of transporting nutrients and signalling molecules between different cells. One way plants solve this problem is by using plasmodesmata nanopores. Plasmodesmata nanopores are permanent nanoscopic openings in the cell wall that connect neighbouring plant cells, linking the cytoplasmic fluid between them. They are probably the most abundant nanochannel on Earth; however, unexplained observations about their transport processes still exist. In this thesis, we use theoretical models based on continuum theory to elucidate three puzzling transport phenomena. Further, we look at how biologically inspired systems may inspire solutions to problems in the technical sciences and other biological systems.
First, we consider how variations in the channel geometry may affect diffusive and pressure-driven fluid flow through plasmodesmata nanopores. Models considering transport through plasmodesmata generally assume a uniform pore geometry across all pores, though experiments have revealed variations in pore morphology. Moreover, experiments have surprisingly shown that particles larger than the apparent opening in the pore can migrate through plasmodesmata. One characteristic of plasmodesmata pore morphology is the presence of a central rod, the desmotubule, that blocks part of the channel. The effect of two ideal modes of shape-perturbations on the diffusive and advective transport are evaluated: the effect of an axial variation in the pore geometry along its length and the effect of a radial displacement of the desmotubule. We find that oversized particles can migrate if the desmotubule is displaced radially towards the side of the pore due to, e.g., thermal fluctuations.
Inspired by experimental observations showing the permeability through plasmodesmata nanopores can be pressure-dependent, we looked at how another type of variation of the pore geometry can influence pressure-driven transport. The pore geometry can be altered if the inner desmotubule is axially displaced in the pore due to a pressure difference across it. The model system inspired a fluidic valve, taking advantage of fluid-structure interactions. Usually, the fluid flow rate as a function of applied pressure drop is found for a known pore geometry. With the system inspired by an axially displaced desmotubule inside a plasmodesma pore, we find that the inverse problem of finding a channel geometry that leads to a desired fluid
flow rate characteristic can be solved.
Apart from considering variations in the pore geometry, we look at how electrical interactions influence transport through plasmodesmata nanopores. Biological membranes are often negatively charged, and charged particles migrate across them. Currently, however, it is assumed that only the size of the migrating particles is important for the permeability through plasmodesmata nanopores. To quantify the effect electrical interactions have on transport through plasmodesmata nanopores, the permeabilities of
fluorophores with different charges and sizes were extracted from experimental data from plants obtained from our collaborators. The permeability of negatively charged fluorophores is found to be greater than that of positively charged ones. Further, we develop a mathematical model to describe how the diffusive transport of tracer particles is influenced by particle-surface interactions. The theory can be used to describe the experiments when considering the particle-surface interaction between an electrically charged tracer particle and an electrical double layer. We find that the theory is not inconsistent with the data when the pore surfaces are modelled as positively charged instead of negatively charged. Additionally, for the case of charged tracer particles interacting with an electrical double layer, we demonstrate that the diffusive current can increase as the area of the pore decreases.
Lastly, we consider examples of applications of fluid-structure interaction problems inspired by nature. We look at how a biologically inspired fluidic device, taking advantage of fluid-structure interactions, can be used to smooth oscillatory peristaltic pump flow. Further, we consider how fluid-structure interactions may play a role in fluid transport in the brain by acting as a valve and converting pressure oscillations into directed fluid flow.
Additionally, the suitability of the various assumptions used in modelling plasmodesmata transport in this thesis is discussed, and other potential effects are mentioned.
Finally, future research directions are commented on.
Original languageEnglish
PublisherDepartment of Physics, Technical University of Denmark
Number of pages224
Publication statusPublished - 2023

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