Advertisement

Water Motion and Sugar Translocation in Leaves

  • Tomas Bohr
  • Hanna Rademaker
  • Alexander Schulz
Chapter

Abstract

We give an overview of the current understanding of the coupled water—and sugar flows in plants with special emphasis on the leaves. We introduce the Münch mechanism and discuss the particularities of osmotically driven flow in the phloem and the consequences for the allometry of the vasculature. This is first done in the context of the entire tree, where we discuss the optimum radius for the phloem tubes, and later for a single needle, where we give a more detailed solution of the osmotic flow profile, allowing us to understand the constraints on needle sizes. We then discuss recent results from microscopy of cross sections along the midvein of a birch leaf, allowing us to measure how the number and radius of the sieve elements depend on the distance from the petiole and compare this to the available area and the minor vein endings in the entire leaf. We finally discuss the pre-phloem water flow in the leaf, i.e. the coupled water/sugar transport from the mesophyll via the bundle sheath into the sieve tubes. We review the distinct sugar loading mechanisms with special emphasis on active symplasmic loading (‘polymer trapping’), where one needs to compute water and sugar flow through extremely narrow channels.

References

  1. Bi Z, Merl-Pham J, Uehlein N, Zimmer I, Mühlhans S, Aichler M, Walch AK, Kaldenhoff R, Palme K, Schnitzler J-P, Block K (2015) RNAi-mediated downregulation of poplar plasma membrane intrinsic proteins (PIPs) changes plasma membrane proteome composition and affects leaf physiology. J Proteomics 128:321–332CrossRefPubMedGoogle Scholar
  2. Carvalho MR, Turgeon R, Owens T, Niklas KJ (2017a) The hydraulic architecture of ginkgo leaves. Am J Bot 104(9):1285–1298CrossRefPubMedGoogle Scholar
  3. Carvalho MR, Turgeon R, Owens T, Niklas KJ (2017b) The scaling of the hydraulic architecture in poplar leaves. New Phytol 214:145–157CrossRefPubMedGoogle Scholar
  4. Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by sweet proteins as a key step for phloem transport. Science 335(6065):207–211CrossRefPubMedGoogle Scholar
  5. Comtet J, Turgeon R, Stroock AD (2017) Phloem loading through plasmodesmata: a biophysical analysis. Plant Physiol 175(2):904–915PubMedPubMedCentralGoogle Scholar
  6. Dechadilok P, Deen WM (2006) Hindrance factors for diffusion and convection in pores. Ind Eng Chem Res 45(21):6953–6959CrossRefGoogle Scholar
  7. Dölger J, Rademaker H, Liesche J, Schulz A, Bohr Tomas (2014) Diffusion and bulk flow in phloem loading: a theoretical analysis of the polymer trap mechanism for sugar transport in plants. Phys Rev E 90(4):042704CrossRefGoogle Scholar
  8. Fisher DB, Gifford RM (1986) Accumulation and conversion of sugars by developing wheat grains vi. gradients along the transport pathway from the peduncle to the endosperm cavity during grain filling. Plant Physiol 82(4):1024–1030CrossRefPubMedPubMedCentralGoogle Scholar
  9. Jensen KH, Berg-Sørensen K, Bruus H, Holbrook NM, Liesche J, Schulz A, Zwieniecki MA, Bohr T (2016) Sap flow and sugar transport in plants. Rev Mod Phys 88:035007 (1–63)Google Scholar
  10. Jensen KH, Lee J, Bohr T, Bruus H, Holbrook NM, Zwieniecki MA (2011) Optimality of the Münch mechanism for translocation of sugars in plants. J R Soc Interface 8(61):1155–1165CrossRefPubMedPubMedCentralGoogle Scholar
  11. Jensen KH, Berg-Sørensen K, Friis SMM, Bohr T (2012a) Analytic solutions and universal properties of sugar loading models in münch phloem flow. J Theor Biol 304:286–296CrossRefPubMedGoogle Scholar
  12. Jensen KH, Liesche J, Bohr T, Schulz A (2012b) Universality of phloem transport in seed plants. Plant Cell Environ 35:1065–1076CrossRefPubMedGoogle Scholar
  13. Jensen KH, Mullendore DL, Holbrook NM, Bohr T, Knoblauch M, Bruus H (2012c) Modeling the hydrodynamics of phloem sieve plates. Front Plant Sci 3Google Scholar
  14. Jensen KH, Zwieniecki MA (2013) Physical limits to leaf size in tall trees. Phys Rev Lett 110(1)Google Scholar
  15. Kedem O, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. BBA—Biochim Et Biophys Acta 27:229–246CrossRefGoogle Scholar
  16. Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA, Beecher SD, Dodgen AC, Jensen KH, Holbrook NM (2016) Testing the Munch hypothesis of long distance phloem transport in plants. Elife 5Google Scholar
  17. Kühn C, Grof CPL (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13(3):287–297CrossRefGoogle Scholar
  18. Landsberg JJ, Fowkes ND (1978) Water movements through plant roots. Ann Bot 42:493–508CrossRefGoogle Scholar
  19. Liesche J, Martens HJ, Schulz A (2011) Symplasmic transport and phloem loading in gymnosperm leaves. Protoplasma 248(1):181–190CrossRefPubMedGoogle Scholar
  20. Liesche J, Windt C, Bohr T, Schulz A, Jensen KH (2015) Slower phloem transport in gymnosperm trees can be attributed to higher sieve element resistance. Tree Physiol (in press)Google Scholar
  21. Lu SY, Zhao HY, Des Marais DL, Parsons EP, Wen XX, Xu XJ, Bangarusamy DK, Wang GC, Rowland O, Juenger T, Bressan RA, Jenks MA (2012) Arabidopsis eceriferum9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol 159:930–944CrossRefPubMedPubMedCentralGoogle Scholar
  22. Martens HJ (2017) Private correspondenceGoogle Scholar
  23. Niklas KJ (1994) Plant allometry: the scaling of plant form and process. University of Chicago PressGoogle Scholar
  24. Nixon-Abell J, Obara CJ, Weigel AV, Li D, Legant WR, Xu CS, Pasolli HA, Harvey K, Hess HF, Betzig E, Blackstone C, Lippincott-Schwartz J (2016) Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER. Science 354, aaf3928–1–12CrossRefPubMedGoogle Scholar
  25. Rademaker H (2016) Microfluidics of sugar transport in plant leaves and in biomimetic devices. PhD thesis, Technical University of DenmarkGoogle Scholar
  26. Rademaker H, Jensen KH, Bohr T (2016) Osmotically driven flows and maximal transport rates in systems of long, linear porous pipes. arXiv:1610.09175
  27. Rademaker H, Zwieniecki MA, Bohr T, Jensen KH (2017) Sugar export limits size of conifer needles. Phys Rev E 95:042402CrossRefPubMedGoogle Scholar
  28. Ronellenfitsch H, Liesche J, Jensen Kaare H, Holbrook NM, Schulz A, Katifori E (2015) Scaling of phloem structure and optimality of photoassimilate transport in conifer needles. In: Proceedings of the royal society of london B: biological sciences, vol 282(1801)CrossRefPubMedGoogle Scholar
  29. Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581(12):2309–2317CrossRefPubMedGoogle Scholar
  30. Schmitz K, Cuypers B, Moll M (1987) Pathway of assimilate transfer between mesophyll-cells and minor veins in leaves. Cucumis melo L. Planta 171(1):19–29CrossRefPubMedGoogle Scholar
  31. Schulz A (2015) Diffusion or bulk flow: how plasmodesmata facilitate pre-phloem transport of assimilates. J Plant Res 128(1):49–61CrossRefPubMedGoogle Scholar
  32. Tadrist L, Darbois-Texier B (2016) Are leaves optimally designed for self-support? an investigation on giant monocots. J Theor Biol 396:125–131CrossRefPubMedGoogle Scholar
  33. Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc, Sunderland, MAGoogle Scholar
  34. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694CrossRefPubMedGoogle Scholar
  35. Volk GM, Turgeon R, Beebe DU (1996) Secondary plasmodesmata formation in the minor-vein phloem. Cucumis Melo L and Cucurbita pepo L Planta 199(3):425–432Google Scholar
  36. Waigmann E, Turner A, Peart J, Roberts K, Zambryski P (1997) Ultrastructural analysis of leaf trichome plasmodesmata reveals major differences from mesophyll plasmodesmata. Planta (Heidelberg) 203(1):75–84CrossRefGoogle Scholar
  37. Zeuthen T, Gorraitz E, Her K, Wright EM, Loo DDF (2016) Structural and functional significance of water permeation through cotransporters. Proc Nat Acad Sci (USA) 113(44):E6887–E6894CrossRefGoogle Scholar
  38. Zeuthen T, MacAulay N (2012) Transport of water against its concentration gradient: fact or fiction? WIREs membr transp signal 2012.  https://doi.org/10.1002/wmts.54Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PhysicsTechnical University of DenmarkLyngbyDenmark
  2. 2.Department of Plant and Environmental SciencesUniversity of CopenhagenCopenhagenDenmark

Personalised recommendations