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Rheology and Conductivity of Phloem

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Rheology and Conductivity of Phloem RHEOLOGY AND CONDUCTIVITY OF PHLOEM By SIERRA DAWN BEECHER A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY WASHINGTON STATE UNIVERSITY Molecular Plant Sciences JULY 2016 © Copyright by SIERRA DAWN BEECHER, 2016 All Rights Reserved © Copyright by SIERRA DAWN BEECHER, 2016 All Rights Reserved To the Faculty of Washington State University: The members of the Committee appointed to examine the dissertation of SIERRA DAWN BEECHER find it satisfactory and recommend that it be accepted. ____________________________________ Michael Knoblauch, Ph.D. Chair ____________________________________ Asaph Cousins, Ph.D. ____________________________________ Andrei Smertenko, Ph.D. ____________________________________ Eric Shelden, Ph.D. ii Acknowledgements I have been very fortunate to have had a lot of excellent support with these projects. My advisor, Michael Knoblauch helped me design experiments to address the questions I was most curious about, and generously made available all tools and technology to carry them out. Dan Froelich shared many of the techniques he had developed for in vivo confocal imaging, which were the foundation for the methods that I developed to do cold stimulation experiments. Dan Mullendore graciously shared many insights, and technical tricks about new possibilities presented by the Leica SP8. These were used for fluorescence lifetime imaging to measure the viscosity of translocating phloem sap. Tim Ross-Elliot was always generous with his methods, and helped me develop better molecular biology skills. All members of the Knoblauch Lab, and my committee members, Eric Shelden, Andrei Smertenko, and Asaph Cousins have inspired me with their passion and intelligence. Michael Neff has also been very supportive and helpful. I would like to thank Valerie Lynch-Holm and Chris Davitt, whose kindness and incredible expertise in all aspects of imaging have been very valuable. Chuck Cody’s wealth of taxonomic knowledge and magical ability to keep plants alive has been very much appreciated. Kåre Hartvig Jensen has been a constant collaborator, and his excellent skills in math and physics were crucial assets for this work. Jessica Savage provided all of the plant materials for analyses in Chapter 4, even climbing trees to do so. My husband, Horst Onken has provided a steady stream of intellectual insight and friendship, which I could not have done without. My parents, Ron and Cookie Beecher, and their spouses have helped me in more ways than I can count, and my children, Emily and Kevin Beecher have been a wellspring of joy and support. iii RHEOLOGY AND CONDUCTIVITY OF PHLOEM Abstract by Sierra Dawn Beecher, Ph.D. Washington State University July 2016 Chair: Michael Knoblauch The Pressure Flow Hypothesis, presented in 1930 by Ernst Münch, is the most accepted model for photoassimilate translocation by the phloem of plants. Net photosynthetic sugar production occurs in source tissues, often mature leaves. These photoassimilates are transported along the sieve tube system to consumptive sink tissues such as roots, meristems, and seeds. Münch’s hypothesis states that a sugar concentration gradient between sources and sinks osmotically generates a hydrostatic pressure differential that drives sap flow. If phloem sap is driven by a pressure differential, geometries of the sieve tube system, and the rheology of phloem sap should scale to equations describing pressure flow in low Reynolds number tubes. Imaging methods developed in this work provide robust geometric and rheological data, expanding the phloem biophysics toolkit. Additionally, insight into a mysterious phenomenon in which transient inhibition of translocation is induced by sudden localized stem chilling is presented. A novel application of fluorescence recovery after photobleaching (FRAP) allowed simultaneous measurement of sap velocity, and diffusivity of a phloem-mobile probe. This technique was used to investigate the cold shock phenomenon directly at the site of cold stimulus at higher resolution than was previously possible. Cold-induced sap velocity declines were not accompanied by similar reductions in sap viscosity. A Fluorescence Lifetime Imaging Microscopy iv (FLIM) method was also developed, providing direct in vivo measurements of viscosity in translocating phloem sap. Values obtained indicate phloem sap viscosities of less than 2 mPas, consistent with sugar concentrations estimated by previous time-intensive exudate analyses. Questions regarding pressure flow in trees, where tube lengths are very long and source phloem turgor pressures have been measured as surprisingly low were also addressed. Sieve element lengths, diameters, and sieve plate angles were measured in 3 positions of 22 different angiosperms. These conductivity factors were large, and scaled to stem length in trees. Because pressure flow equations indicate an inversely proportional relationship between conductivity and pressure, these data are consistent with pressure driven flow as the mechanism for translocation in trees. v TABLE OF CONTENTS Page Acknowledgments...................................................................................................................... iii Abstract ...................................................................................................................................... iv List of Tables .............................................................................................................................. ix List of Figures .............................................................................................................................. x Chapter 1: Introduction to Phloem ............................................................................................. 1 Overview ......................................................................................................................... 1 Evolution of Translocation .............................................................................................. 1 Development of Angiosperm Phloem............................................................................. 6 Structure of Angiosperm Phloem ................................................................................... 9 Sieve Elements ....................................................................................................... 9 Sieve Element Organelles and Subcellular Structures ......................................... 12 Sieve Element Plastids ................................................................................... 12 Sieve Element Mitochondria .......................................................................... 12 Sieve Element Endoplasmic Reticulum .......................................................... 12 Sieve Element Proteins .................................................................................. 13 Sieve Element Plasmalemma ......................................................................... 14 Sieve Element Cell Walls and Sieve Plate Pores ............................................ 15 Companion Cells .................................................................................................. 16 Phloem Parenchyma ............................................................................................ 17 Phloem Fibers ...................................................................................................... 17 Function of the Phloem ................................................................................................ 18 vi Phloem Loading.................................................................................................... 21 Passive Symplastic Phloem Loading ............................................................... 23 Active Symplastic Phloem Loading ................................................................ 24 Apoplastic Phloem Loading ............................................................................ 24 Transport Phloem ................................................................................................ 25 Unloading Phloem ................................................................................................ 27 Rheological Considerations .................................................................................. 27 Problems with the Pressure Flow Hypothesis ..................................................... 28 Works Cited ................................................................................................................... 30 Chapter 2: Diffusion and Velocity ............................................................................................. 36 Abstract ......................................................................................................................... 36 Introduction .................................................................................................................. 36 Materials and Methods ................................................................................................. 38 Results ........................................................................................................................... 39 Discussion...................................................................................................................... 46 Works Cited ................................................................................................................... 51 Chapter 3: Phloem Sap Viscosity .............................................................................................
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