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

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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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.

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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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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.

Corresponding author

Correspondence to Jean Comtet.

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The authors declare no competing financial interests.

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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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