Article

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

  • Nature Plants 3, Article number: 17032 (2017)
  • doi:10.1038/nplants.2017.32
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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.

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References

  1. 1.

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

  2. 2.

    & Münch, morphology, microfluidics – our structural problem with the phloem. Plant Cell Environ. 33, 1439–1452 (2010).

  3. 3.

    , , & The physicochemical hydrodynamics of vascular plants. Annu. Rev. Fluid Mech. 46, 615–642 (2014).

  4. 4.

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

  5. 5.

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

  6. 6.

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

  7. 7.

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

  8. 8.

    , , & Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol. 157, 1518–1527 (2011).

  9. 9.

    , , & Osmotically driven flows in microchannels separated by a semipermeable membrane. Lab. Chip. 9, 2093–2099 (2009).

  10. 10.

    , , , & Osmotically driven pipe flows and their relation to sugar transport in plants. J. Fluid Mech. 636, 371–396 (2009).

  11. 11.

    & The transpiration of water at negative pressures in a synthetic tree. Nature 455, 208–212 (2008).

  12. 12.

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

  13. 13.

    , & Solution flow in tubular semipermeable membranes. Planta 107, 279–300 (1972).

  14. 14.

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

  15. 15.

    & On the ascent of sap. Phil. Trans. R. Soc. Lond. B 186, (1895).

  16. 16.

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

  17. 17.

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

  18. 18.

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

  19. 19.

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

  20. 20.

    , & A water-activated pump for portable microfluidic applications. J. Colloid Interface Sci. 305, 239–249 (2007).

  21. 21.

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

  22. 22.

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

  23. 23.

    , , & Osmotic micropumps for drug delivery. Adv. Drug Deliv. Rev. 64, 1617–1627 (2012).

  24. 24.

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

  25. 25.

    , & Phloem loading through plasmodesmata: a biophysical analysis. Preprint at (2016).

  26. 26.

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

  27. 27.

    & Direct measurement of sieve tube turgor pressure using severed aphid stylets. Plant Physiol. 65, 1133–1135 (1980).

  28. 28.

    & Estimation of the volumetric elastic modulus and membrane hydraulic conductivity of willow sieve tubes. Plant Physiol. 73, 1042–1047 (1983).

  29. 29.

    , & Direct measurements of sieve element hydrostatic pressure reveal strong regulation after pathway blockage. Funct. Plant Biol. 31, 987 (2004).

  30. 30.

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

  31. 31.

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

  32. 32.

    & Water relations of plants and soils. Soil Sci. 161, 42–79 (1996).

  33. 33.

    & 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).

  34. 34.

    , & Optimal concentration for sugar transport in plants. J. R. Soc. Interface 10, 20130055 (2013).

  35. 35.

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

  36. 36.

    & Physical limits to leaf size in tall trees. Phys. Rev. Lett. 110, 018104 (2013).

  37. 37.

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

  38. 38.

    & Studies on the leaf of Populus deltoides (Salicaceae): ultrastructure, plasmodesmatal frequency, and solute concentrations. Am. J. Bot. 72, 1232 (1985).

  39. 39.

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

  40. 40.

    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).

  41. 41.

    & Hindrance factors for diffusion and convection in pores. Ind. Eng. Chem. Res. 45, 6953–6959 (2006).

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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).

Author information

Affiliations

  1. MIT Mechanical Engineering, Cambridge, Massachusetts 02139, 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, New York 14853, USA

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

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

    • 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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jean Comtet.

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