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Passive phloem loading and long-distance transport in a synthetic tree-on-a-chip

Nature Plants volume 3, Article number: 17032 (2017) Cite this article

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Abstract

Vascular plants rely on differences in osmotic pressure to export sugars from regions of synthesis (mature leaves) to sugar sinks (roots, fruits). In this process, known as Münch pressure flow, the loading of sugars from photosynthetic cells to the export conduit (the phloem) is crucial, as it sets the pressure head necessary to power long-distance transport. Whereas most herbaceous plants use active mechanisms to increase phloem sugar concentration above that of the photosynthetic cells, in most tree species, for which transport distances are largest, loading seems, counterintuitively, to occur by means of passive symplastic diffusion from the mesophyll to the phloem. Here, we use a synthetic microfluidic model of a passive loader to explore the non-linear dynamics that arise during export and determine the ability of passive loading to drive long-distance transport. We first demonstrate that in our device, the phloem concentration is set by the balance between the resistances to diffusive loading from the source and convective export through the phloem. Convection-limited export corresponds to classical models of Münch transport, where the phloem concentration is close to that of the source; in contrast, diffusion-limited export leads to small phloem concentrations and weak scaling of flow rates with hydraulic resistance. We then show that the effective regime of convection-limited export is predominant in plants with large transport resistances and low xylem pressures. Moreover, hydrostatic pressures developed in our synthetic passive loader can reach botanically relevant values as high as 10 bars. We conclude that passive loading is sufficient to drive long-distance transport in large plants, and that trees are well suited to take full advantage of passive phloem loading strategies.

The mechanism by which plants transport sugars from the mesophyll (Fig. 1a; green) to export conduits (Fig. 1a; red), known as phloem loading, is crucial. The loading of sugars lowers the chemical potential of water in the phloem cells, allowing water to enter the phloem via osmosis from the adjacent xylem (Fig. 1a, blue), and to be subsequently exported through the transport phloem. Phloem loading thus sets the pressure head available to power long-distance transport. In most plants, energy is used to increase the sugar concentration in leaf phloem above that of the mesophyll cells, which has traditionally been thought a requirement to overcome viscous drag in the sieve tubes and drive long-distance transport via Münch pressure flow4. Because transport resistances scale with the height of the plant, one might expect trees to require the largest phloem pressures of all plants to sustain similar rates of sugar export. Oddly, the majority of trees seem to rely on a passive phloem loading mechanism, in which the sugar concentration in the phloem is slightly lower than that of the photosynthetic cells (Fig. 1a, concentration diagram), thus reducing the apparent available driving force5. Some experiments have provided evidence for the use of passive loading in trees6,7. Fu et al.8 suggested that the low water potential in leaf xylem of trees requires large sugar concentrations in the mesophyll cells, making active phloem loading unnecessary, but this factor is not directly coupled to the kinetics of phloem transport. Hence, the ability of the passive loading mechanism to generate sufficient pressure to drive long-distance transport in plants is uncertain and the reasons for absence of active loading in trees are not well understood.

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Figure 1: Passive phloem loading in plants and in the synthetic tree-on-a-chip.
Figure 2: Steady-state flow rates deviate from standard Münch models.
Figure 3: Convection and diffusion limited export regimes.
Figure 4: Large hydrostatic pressures can be obtained in the synthetic passive loader.
Figure 5: Meta-analysis of phloem loading strategies in trees and herbs.

References

  1. Turgeon, R. The role of phloem loading reconsidered. Plant Physiol. 152, 1817–1823 (2010).

    Google Scholar 

  2. Knoblauch, M. & Peters, W. S. Münch, morphology, microfluidics – our structural problem with the phloem. Plant Cell Environ. 33, 1439–1452 (2010).

    Google Scholar 

  3. Stroock, A. D., Pagay, V. V., Zwieniecki, M. A. & Michele Holbrook, N. The physicochemical hydrodynamics of vascular plants. Annu. Rev. Fluid Mech. 46, 615–642 (2014).

    Google Scholar 

  4. Giaquinta, R. T. Phloem loading of sucrose. Annu. Rev. Plant Physiol. 34, 347–387 (1983).

    Google Scholar 

  5. Turgeon, R. The puzzle of phloem pressure. Plant Physiol. 154, 578–581 (2010).

    Google Scholar 

  6. Zhang, C. et al. Symplastic phloem loading in poplar. Plant Physiol. 166, 306–313 (2014).

    Google Scholar 

  7. Turgeon, R. & Medville, R. The absence of phloem loading in willow leaves. Proc. Natl Acad. Sci. USA 95, 12055–12060 (1998).

    Google Scholar 

  8. Fu, Q., Cheng, L., Guo, Y. & Turgeon, R. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol. 157, 1518–1527 (2011).

    Google Scholar 

  9. Jensen, K. H., Lee, J., Bohr, T. & Bruus, H. Osmotically driven flows in microchannels separated by a semipermeable membrane. Lab. Chip. 9, 2093–2099 (2009).

    Google Scholar 

  10. Jensen, K. H., Rio, E., Hansen, R., Clanet, C. & Bohr, T. Osmotically driven pipe flows and their relation to sugar transport in plants. J. Fluid Mech. 636, 371–396 (2009).

    Google Scholar 

  11. Wheeler, T. D. & Stroock, A. D. The transpiration of water at negative pressures in a synthetic tree. Nature 455, 208–212 (2008).

    Google Scholar 

  12. Lang, A. A working model of a sieve tube. J. Exp. Bot. 24, 896–904 (1973).

    Google Scholar 

  13. Eschrich, W., Evert, R. F. & Young, J. H. Solution flow in tubular semipermeable membranes. Planta 107, 279–300 (1972).

    Google Scholar 

  14. Noblin, X. et al. Optimal vein density in artificial and real leaves. Proc. Natl Acad. Sci. USA 105, 9140–9144 (2008).

    Google Scholar 

  15. Dixon, H. H. & Joly, J. On the ascent of sap. Phil. Trans. R. Soc. Lond. B 186, (1895).

  16. Münch, E. Versuche über den saftkreislauf. Ber. Dtsch. Bot. Ges. 45, 340–356 (1927).

    Google Scholar 

  17. Münch, E. in Stoffbewegungen in der Pflanze (ed. Jena, G. F.) 234 (Fischer, 1930).

  18. Lancashire, J. R. & Ennos, A. R. Modelling the hydrodynamic resistance of bordered pits. J. Exp. Bot. 53, 1485–1493 (2002).

    Google Scholar 

  19. Velten, T. et al. Intelligent intraoral drug delivery microsystem. Proc. Inst. Mech. Eng. C 220, 1609–1617 (2006).

    Google Scholar 

  20. Good, B. T., Bowman, C. N. & Davis, R. H. A water-activated pump for portable microfluidic applications. J. Colloid Interface Sci. 305, 239–249 (2007).

    Google Scholar 

  21. Xu, Z.-R. et al. An osmotic micro-pump integrated on a microfluidic chip for perfusion cell culture. Talanta 80, 1088–1093 (2010).

    Google Scholar 

  22. Bruhn, B. R. et al. Osmosis-based pressure generation: dynamics and application. PLoS ONE 9, e91350 (2014).

    Google Scholar 

  23. Herrlich, S., Spieth, S., Messner, S. & Zengerle, R. Osmotic micropumps for drug delivery. Adv. Drug Deliv. Rev. 64, 1617–1627 (2012).

    Google Scholar 

  24. Jensen, K. H. et al. Optimality of the Münch mechanism for translocation of sugars in plants. J. R. Soc. Interface 8, 1155–1165 (2011).

    Google Scholar 

  25. Comtet, J., Turgeon, R. & Stroock, A. D. Phloem loading through plasmodesmata: a biophysical analysis. Preprint at https://arxiv.org/abs/1603.04058 (2016).

  26. Knoblauch, M. et al. Testing the Münch hypothesis of long distance phloem transport in plants. eLife 5, e15341 (2016).

    Google Scholar 

  27. Wright, J. P. & Fisher, D. B. Direct measurement of sieve tube turgor pressure using severed aphid stylets. Plant Physiol. 65, 1133–1135 (1980).

    Google Scholar 

  28. Wright, J. P. & Fisher, D. B. Estimation of the volumetric elastic modulus and membrane hydraulic conductivity of willow sieve tubes. Plant Physiol. 73, 1042–1047 (1983).

    Google Scholar 

  29. Gould, N., Minchin, P. E. H. & Thorpe, M. R. Direct measurements of sieve element hydrostatic pressure reveal strong regulation after pathway blockage. Funct. Plant Biol. 31, 987 (2004).

    Google Scholar 

  30. Gamalei, Y. Phloem loading and its development related to plant evolution from trees to herbs. Trees 5, 50–64 (1991).

    Google Scholar 

  31. Liesche, J. & Schulz, A. In vivo quantification of cell coupling in plants with different phloem-loading strategies. Plant Physiol. 159, 355–365 (2012).

    Google Scholar 

  32. Kramer, P. J. & Boyer, J. S. Water relations of plants and soils. Soil Sci. 161, 42–79 (1996).

    Google Scholar 

  33. Thompson, M. V. & Holbrook, N. M. Application of a single-solute non-steady-state phloem model to the study of long-distance assimilate transport. J. Theor. Biol. 220, 419–455 (2003).

    Google Scholar 

  34. Jensen, K. H., Savage, J. A. & Holbrook, N. M. Optimal concentration for sugar transport in plants. J. R. Soc. Interface 10, 20130055 (2013).

    Google Scholar 

  35. Jensen, K. H. et al. Modeling the hydrodynamics of phloem sieve plates. Front. Plant Sci. 3, 151 (2012).

    Google Scholar 

  36. Jensen, K. H. & Zwieniecki, M. A. Physical limits to leaf size in tall trees. Phys. Rev. Lett. 110, 018104 (2013).

  37. Jensen, K. H. et al. Optimality of the Münch mechanism for translocation of sugars in plants. J. R. Soc. Interface 8, 1155–1165 (2011).

    Google Scholar 

  38. Russin, W. A. & Evert, R. F. Studies on the leaf of Populus deltoides (Salicaceae): ultrastructure, plasmodesmatal frequency, and solute concentrations. Am. J. Bot. 72, 1232 (1985).

    Google Scholar 

  39. Schulz, A. Diffusion or bulk flow: how plasmodesmata facilitate pre-phloem transport of assimilates. J. Plant Res. 128, 49–61 (2014).

    Google Scholar 

  40. Srivastava, A. C. et al. Arabidopsis plants harbouring a mutation in AtSUC2, encoding the predominant sucrose/proton symporter necessary for efficient phloem transport, are able to complete their life cycle and produce viable seed. Ann. Bot. 104, 1121–1128 (2009).

    Google Scholar 

  41. Dechadilok, P. & Deen, W. M. Hindrance factors for diffusion and convection in pores. Ind. Eng. Chem. Res. 45, 6953–6959 (2006).

    Google Scholar 

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Acknowledgements

J.C. would like to thank J. Alvarado for his support, A. Barbati for advice on the device fabrication and B. Keshavarz for help with the rheology measurements. A.E.H. and J.C. acknowledge support from DARPA (W31P4Q-13-1-0013). K.H.J. was supported by a research grant from VILLUM FONDEN (13166). A.D.S. acknowledges support from the AFOSR (FA9550-15-1-0052). R.T. was supported by National Science Foundation (USA) (grant no. IOS-1354718).

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Authors and Affiliations

  1. MIT Mechanical Engineering, Cambridge, 02139, Massachusetts, USA

    Jean Comtet & A. E. Hosoi

  2. Department of Physics, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark

    Kaare H. Jensen

  3. Section of Plant Biology, Cornell University, Ithaca, 14853, New York, USA

    Robert Turgeon

  4. School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, 14853, New York, USA

    Abraham D. Stroock

  5. Kavli Institute at Cornell for Nanoscale Science, Cornell University, Ithaca, 14853, New York, USA

    Abraham D. Stroock

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  1. Jean Comtet
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  2. Kaare H. Jensen
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  4. Abraham D. Stroock
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Contributions

J.C. and A.E.H. conceived the project. J.C. designed and executed the experiments and developed the theoretical model, with input from all authors. J.C., K.H.J., R.T., A.D.S. and A.E.H. interpreted the experimental data and the meta-analysis and wrote the paper.

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Correspondence to Jean Comtet.

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Comtet, J., Jensen, K., Turgeon, R. et al. Passive phloem loading and long-distance transport in a synthetic tree-on-a-chip. Nature Plants 3, 17032 (2017). https://doi.org/10.1038/nplants.2017.32

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