Phloem Loading and Unloading of Sucrose: What a Long, Strange Trip from Source to Sink

Braun, David M.

doi:10.1146/annurev-arplant-070721-083240

Title: Phloem Loading and Unloading of Sucrose: What a Long, Strange Trip from Source to Sink

Journal Article · Fri May 20 00:00:00 EDT 2022 · Annual Review of Plant Biology

DOI:https://doi.org/10.1146/annurev-arplant-070721-083240· OSTI ID:1980839

Braun, David M. ^[1]

Division of Plant Science and Technology, Division of Biological Sciences, Interdisciplinary Plant Group, and Missouri Maize Center, University of Missouri-Columbia, Columbia, Missouri, USA,

Sucrose is transported from sources (mature leaves) to sinks (importing tissues such as roots, stems, fruits, and seeds) through the phloem tissues in veins. In many herbaceous crop species, sucrose must first be effluxed to the cell wall by a sugar transporter of the SWEET family prior to being taken up into phloem companion cells or sieve elements by a different sugar transporter, called SUT or SUC. The import of sucrose into these cells is termed apoplasmic phloem loading. In sinks, sucrose can similarly exit the phloem apoplasmically or, alternatively, symplasmically through plasmodesmata into connecting parenchyma storage cells. Recent advances describing the regulation and manipulation of sugar transporter expression and activities provide stimulating new insights into sucrose phloem loading in sources and unloading processes in sink tissues. Additionally, new breakthroughs have revealed distinct subpopulations of cells in leaves with different functions pertaining to phloem loading. These and other discoveries in sucrose transport are discussed.

Cite

Export

Save

Research Organization:: Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0018072

OSTI ID:: 1980839

Journal Information:: Annual Review of Plant Biology, Vol. 73, Issue 1; ISSN 1543-5008

Publisher:: Annual Reviews

Country of Publication:: United States

Language:: English

References (149)

Source-Sink Regulation Is Mediated by Interaction of an FT Homolog with a SWEET Protein in Potato Abelenda, José A.; Bergonzi, Sara; Oortwijn, Marian Current Biology, Vol. 29, Issue 7 https://doi.org/10.1016/j.cub.2019.02.018	journal	April 2019
Rice xa13 Recessive Resistance to Bacterial Blight Is Defeated by Induction of the Disease Susceptibility Gene Os- 11N3 Antony, Ginny; Zhou, Junhui; Huang, Sheng The Plant Cell, Vol. 22, Issue 11 https://doi.org/10.1105/tpc.110.078964	journal	November 2010
Membrane-Transport Systems for Sucrose in Relation to Whole-Plant Carbon Partitioning Ayre, Brian G. Molecular Plant, Vol. 4, Issue 3 https://doi.org/10.1093/mp/ssr014	journal	May 2011
Sucrose Transporter ZmSut1 Expression and Localization Uncover New Insights into Sucrose Phloem Loading Baker, R. Frank; Leach, Kristen A.; Boyer, Nathanial R. Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.00884	journal	September 2016
SWEET as Sugar: New Sucrose Effluxers in Plants Frank Baker, R.; Leach, Kristen A.; Braun, David M. Molecular Plant, Vol. 5, Issue 4 https://doi.org/10.1093/mp/SSS054	journal	July 2012
Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves Beebe, DwightU.; Turgeon, Robert Planta, Vol. 188, Issue 3 https://doi.org/10.1007/BF00192802	journal	October 1992
Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays Bezrutczyk, Margaret; Hartwig, Thomas; Horschman, Marc New Phytologist, Vol. 218, Issue 2 https://doi.org/10.1111/nph.15021	journal	February 2018
Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves Bezrutczyk, Margaret; Zöllner, Nora R.; Kruse, Colin P. S. The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa055	journal	January 2021
Regulation of assimilate import into sink organs: update on molecular drivers of sink strength Bihmidine, Saadia; Hunter, Charles T.; Johns, Christine E. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00177	journal	January 2013
Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems Bihmidine, Saadia; Julius, Benjamin T.; Dweikat, Ismail Plant Signaling & Behavior, Vol. 11, Issue 1 https://doi.org/10.1080/15592324.2015.1117721	journal	January 2016
Transport Mechanism of the Cloned Potato H ⁺ /Sucrose Cotransporter StSUT1 Boorer, Kathryn J.; Loo, Donald D. F.; Frommer, Wolf B. Journal of Biological Chemistry, Vol. 271, Issue 41 https://doi.org/10.1074/jbc.271.41.25139	journal	October 1996
Changes in structure and dimension of plasmodesmata in the phloem loading pathway in Tecoma capensis (Bignoniaceae) - locating the polymer trap Botha, Cej; Murugan, Nelisha South African Journal of Botany, Vol. 140 https://doi.org/10.1016/j.sajb.2021.03.032	journal	August 2021
Multiple C2 domains and transmembrane region proteins ( MCTP s) tether membranes at plasmodesmata Brault, Marie L.; Petit, Jules D.; Immel, Françoise EMBO reports, Vol. 20, Issue 8 https://doi.org/10.15252/embr.201847182	journal	July 2019
tie - dyed1 Regulates Carbohydrate Accumulation in Maize Leaves Braun, David M.; Ma, Yi; Inada, Noriko Plant Physiology, Vol. 142, Issue 4 https://doi.org/10.1104/pp.106.090381	journal	October 2006
Genetic Control of Carbon Partitioning in Grasses: Roles of Sucrose Transporters and Tie-dyed Loci in Phloem Loading Braun, David M.; Slewinski, Thomas L. Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.129049	journal	January 2009
Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security Braun, D. M.; Wang, L.; Ruan, Y. -L. Journal of Experimental Botany, Vol. 65, Issue 7 https://doi.org/10.1093/jxb/ert416	journal	December 2013
The H ⁺ -Sucrose Cotransporter NtSUT1 Is Essential for Sugar Export from Tobacco Leaves Bürkle, Lukas; Hibberd, Julian M.; Quick, W. Paul Plant Physiology, Vol. 118, Issue 1 https://doi.org/10.1104/pp.118.1.59	journal	September 1998
Electrogenicity, pH-Dependence, and Stoichiometry of the Proton-Sucrose Symport Bush, Daniel R. Plant Physiology, Vol. 93, Issue 4 https://doi.org/10.1104/pp.93.4.1590	journal	August 1990
Proton-Coupled Sugar and Amino Acid Transporters in Plants Bush, D. R. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 44, Issue 1 https://doi.org/10.1146/annurev.pp.44.060193.002501	journal	June 1993
Phloem-localized, Proton-coupled Sucrose Carrier ZmSUT1 Mediates Sucrose Efflux under the Control of the Sucrose Gradient and the Proton Motive Force Carpaneto, Armando; Geiger, Dietmar; Bamberg, Ernst Journal of Biological Chemistry, Vol. 280, Issue 22 https://doi.org/10.1074/jbc.M501785200	journal	April 2005
Tissue-specific transcriptome analysis within the maturing sugarcane stalk reveals spatial regulation in the expression of cellulose synthase and sucrose transporter gene families Casu, Rosanne E.; Rae, Anne L.; Nielsen, Janine M. Plant Molecular Biology, Vol. 89, Issue 6 https://doi.org/10.1007/s11103-015-0388-9	journal	October 2015
Transport of Sugars Chen, Li-Qing; Cheung, Lily S.; Feng, Liang Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-033904	journal	June 2015
Sugar transporters for intercellular exchange and nutrition of pathogens Chen, Li-Qing; Hou, Bi-Huei; Lalonde, Sylvie Nature, Vol. 468, Issue 7323 https://doi.org/10.1038/nature09606	journal	November 2010
Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport Chen, L. -Q.; Qu, X. -Q.; Hou, B. -H. Science, Vol. 335, Issue 6065 https://doi.org/10.1126/science.1213351	journal	December 2011
Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought Chen, Qingchao; Hu, Tao; Li, Xiaohua Nature Plants, Vol. 8, Issue 1 https://doi.org/10.1038/s41477-021-01040-7	journal	December 2021
FLOWERING LOCUS T mRNA is synthesized in specialized companion cells in Arabidopsis and Maryland Mammoth tobacco leaf veins Chen, Qingguo; Payyavula, Raja S.; Chen, Lin Proceedings of the National Academy of Sciences, Vol. 115, Issue 11 https://doi.org/10.1073/pnas.1719455115	journal	February 2018
Overexpression of the tonoplast sugar transporter CmTST2 in melon fruit increases sugar accumulation Cheng, Jintao; Wen, Suying; Xiao, Shuang Journal of Experimental Botany, Vol. 69, Issue 3 https://doi.org/10.1093/jxb/erx440	journal	December 2017
FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis Corbesier, L.; Vincent, C.; Jang, S. Science, Vol. 316, Issue 5827 https://doi.org/10.1126/science.1141752	journal	May 2007
Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress Cui, Weier; Lee, Jung-Youn Nature Plants, Vol. 2, Issue 5 https://doi.org/10.1038/nplants.2016.34	journal	April 2016
Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation Dasgupta, Kasturi; Khadilkar, Aswad S.; Sulpice, Ronan Plant Physiology, Vol. 165, Issue 2 https://doi.org/10.1104/pp.114.238410	journal	April 2014
The Calcium Sensor CBL2 and Its Interacting Kinase CIPK6 Are Involved in Plant Sugar Homeostasis via Interacting with Tonoplast Sugar Transporter TST2 Deng, Jinwu; Yang, Xiyan; Sun, Weinan Plant Physiology, Vol. 183, Issue 1 https://doi.org/10.1104/pp.19.01368	journal	March 2020
Vascular patterning and leaf shape Dengler, Nancy; Kang, Julie Current Opinion in Plant Biology, Vol. 4, Issue 1 https://doi.org/10.1016/S1369-5266(00)00135-7	journal	February 2001
Sugar transporters in grasses: Function and modulation in source and storage tissues Dhungana, Singha R.; Braun, David M. Journal of Plant Physiology, Vol. 266 https://doi.org/10.1016/j.jplph.2021.153541	journal	November 2021
Identification of a Vacuolar Sucrose Transporter in Barley and Arabidopsis Mesophyll Cells by a Tonoplast Proteomic Approach Endler, Anne; Meyer, Stefan; Schelbert, Silvia Plant Physiology, Vol. 141, Issue 1 https://doi.org/10.1104/pp.106.079533	journal	March 2006
SWEETs, transporters for intracellular and intercellular sugar translocation Eom, Joon-Seob; Chen, Li-Qing; Sosso, Davide Current Opinion in Plant Biology, Vol. 25 https://doi.org/10.1016/j.pbi.2015.04.005	journal	June 2015
Impaired Function of the Tonoplast-Localized Sucrose Transporter in Rice, OsSUT2 , Limits the Transport of Vacuolar Reserve Sucrose and Affects Plant Growth Eom, Joon-Seob; Cho, Jung-Il; Reinders, Anke Plant Physiology, Vol. 157, Issue 1 https://doi.org/10.1104/pp.111.176982	journal	July 2011
The mechanism of phloem loading in rice (Oryza sativa) Eom, Joon-Seob; Choi, Sang-Bong; Ward, John M. Molecules and Cells, Vol. 33, Issue 5 https://doi.org/10.1007/s10059-012-0071-9	journal	March 2012
Sieve-Tube Structure in Relation to Function Evert, Ray F. BioScience, Vol. 32, Issue 10 https://doi.org/10.2307/1308972	journal	November 1982
Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Evert, R. F.; Eschrich, W.; Heyser, W. Planta, Vol. 136, Issue 1 https://doi.org/10.1007/BF00387929	journal	January 1977
Leaf structure in relation to solute transport and phloem loading in Zea mays L. Evert, R. F.; Eschrich, W.; Heyser, W. Planta, Vol. 138, Issue 3 https://doi.org/10.1007/BF00386823	journal	January 1978
Anatomical and Ultrastructural Changes Associated with Sink-to-Source Transition in Developing Maize Leaves Evert, Ray F.; Russin, William A.; Bosabalidis, Artemios M. International Journal of Plant Sciences, Vol. 157, Issue 3 https://doi.org/10.1086/297344	journal	May 1996
Shoot, Stolon, and Tuber Formation on Potato (Solanum tuberosum L.) Cuttings in Response to Photoperiod Ewing, Elmer E.; Wareing, Philip F. Plant Physiology, Vol. 61, Issue 3 https://doi.org/10.1104/pp.61.3.348	journal	March 1978
OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice Fei, Honghong; Yang, Zhipan; Lu, Qingtao Plant Science, Vol. 306 https://doi.org/10.1016/j.plantsci.2021.110851	journal	May 2021
Microautoradiographic studies of phloem loading and transport in the leaf of Zea mays L. Fritz, Eberhard; Evert, Ray F.; Heyser, Wolfgang Planta, Vol. 159, Issue 3 https://doi.org/10.1007/BF00397525	journal	November 1983
Loading and transport of assimilates in different maize leaf bundles Fritz, Eberhard; Evert, Ray F.; Nasse, Hubert Planta, Vol. 178, Issue 1 https://doi.org/10.1007/BF00392520	journal	January 1989
Structure and function of leaf minor veins in trees and herbs: A taxonomic review Gamalei, Yuri Trees, Vol. 3, Issue 2 https://doi.org/10.1007/BF01021073	journal	January 1989
What determines the composition of the phloem sap? Is there any selectivity filter for macromolecules entering the phloem sieve elements? Garg, Varsha; Kühn, Christina Plant Physiology and Biochemistry, Vol. 151 https://doi.org/10.1016/j.plaphy.2020.03.023	journal	June 2020
Solute Distribution in Sugar Beet Leaves in Relation to Phloem Loading and Translocation Geiger, D. R.; Giaquinta, R. T.; Sovonick, S. A. Plant Physiology, Vol. 52, Issue 6 https://doi.org/10.1104/pp.52.6.585	journal	December 1973
Raman spectroscopy reveals high phloem sugar content in leaves of canopy red oak trees Gersony, Jess T.; McClelland, Arthur; Holbrook, N. Michele New Phytologist, Vol. 232, Issue 1 https://doi.org/10.1111/nph.17465	journal	July 2021
Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters Gottwald, J. R.; Krysan, P. J.; Young, J. C. Proceedings of the National Academy of Sciences, Vol. 97, Issue 25 https://doi.org/10.1073/pnas.250473797	journal	November 2000
Concurrent overexpression of amino acid permease Grant, Jan E.; Ninan, Annu; Cripps-Guazzone, Natalia Functional Plant Biology, Vol. 48, Issue 9 https://doi.org/10.1071/FP21011	journal	May 2021
SWEET17, a Facilitative Transporter, Mediates Fructose Transport across the Tonoplast of Arabidopsis Roots and Leaves Guo, Woei-Jiun; Nagy, Reka; Chen, Hsin-Yi Plant Physiology, Vol. 164, Issue 2 https://doi.org/10.1104/pp.113.232751	journal	December 2013
Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways Hackel, Aleksandra; Schauer, Nicolas; Carrari, Fernando The Plant Journal, Vol. 45, Issue 2 https://doi.org/10.1111/j.1365-313X.2005.02572.x	journal	January 2006
Identification of Phloem Involved in Assimilate Loading in Leaves by the Activity of the Galactinol Synthase Promoter Haritatos, Edith; Ayre, Brian G.; Turgeon, Robert Plant Physiology, Vol. 123, Issue 3 https://doi.org/10.1104/pp.123.3.929	journal	July 2000
Minor vein structure and sugar transport in Arabidopsis thaliana Haritatos, Edith; Medville, Richard; Turgeon, Robert Planta, Vol. 211, Issue 1 https://doi.org/10.1007/s004250000268	journal	June 2000
Evidence for Symplastic Phloem Unloading in Sink Leaves of Barley Haupt, Sophie; Duncan, George H.; Holzberg, Steve Plant Physiology, Vol. 125, Issue 1 https://doi.org/10.1104/pp.125.1.209	journal	January 2001
Sucrose in the Free Space of Translocating Maize Leaf Bundles Heyser, Wolfgang; Evert, Ray F.; Fritz, Eberhard Plant Physiology, Vol. 62, Issue 4 https://doi.org/10.1104/pp.62.4.491	journal	October 1978
Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected Hirose, Tatsuro; Zhang, Zujian; Miyao, Akio Journal of Experimental Botany, Vol. 61, Issue 13 https://doi.org/10.1093/jxb/erq175	journal	July 2010
CBL2-CIPK6-TST2-Mediated Regulation of Sugar Homeostasis Hunter, Kerri Plant Physiology, Vol. 183, Issue 1 https://doi.org/10.1104/pp.20.00370	journal	May 2020
Antisense Expression of a Rice Sucrose Transporter OsSUT1 in Rice (Oryza sativa L.) Ishimaru, Ken; Hirose, Tatsurou; Aoki, Naohiro Plant and Cell Physiology, Vol. 42, Issue 10 https://doi.org/10.1093/pcp/pce148	journal	October 2001
Carbohydrate metabolism in a heat‐girdled maize source leaf Jeannette, E.; Reyss, A.; Grégory, N. Plant, Cell & Environment, Vol. 23, Issue 1 https://doi.org/10.1046/j.1365-3040.2000.00519.x	journal	January 2000
Border Control--A Membrane-Linked Interactome of Arabidopsis Jones, A. M.; Xuan, Y.; Xu, M. Science, Vol. 344, Issue 6185 https://doi.org/10.1126/science.1251358	journal	May 2014
Sugar Transporters in Plants: New Insights and Discoveries Julius, Benjamin T.; Leach, Kristen A.; Tran, Thu M. Plant and Cell Physiology, Vol. 58, Issue 9 https://doi.org/10.1093/pcp/pcx090	journal	June 2017
Maize Carbohydrate partitioning defective1 impacts carbohydrate distribution, callose accumulation, and phloem function Julius, Benjamin T.; Slewinski, Thomas L.; Baker, R. Frank Journal of Experimental Botany, Vol. 69, Issue 16 https://doi.org/10.1093/jxb/ery203	journal	May 2018
Identification of the transporter responsible for sucrose accumulation in sugar beet taproots Jung, Benjamin; Ludewig, Frank; Schulz, Alexander Nature Plants, Vol. 1, Issue 1 https://doi.org/10.1038/nplants.2014.1	journal	January 2015
Sucrose transport into vacuoles isolated from barley mesophyll protoplasts Kaiser, Georg; Heber, Ulrich Planta, Vol. 161, Issue 6 https://doi.org/10.1007/BF00407090	journal	January 1984
AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes Kanno, Yuri; Oikawa, Takaya; Chiba, Yasutaka Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13245	journal	October 2016
Distinct identities of leaf phloem cells revealed by single cell transcriptomics Kim, Ji-Yun; Symeonidi, Efthymia; Pang, Tin Yau The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa060	journal	January 2021
Testing the Münch hypothesis of long distance phloem transport in plants Knoblauch, Michael; Knoblauch, Jan; Mullendore, Daniel L. eLife, Vol. 5 https://doi.org/10.7554/eLife.15341	journal	June 2016
What actually is the Münch hypothesis? A short history of assimilate transport by mass flow: A history of the Münch hypothesis Knoblauch, Michael; Peters, Winfried S. Journal of Integrative Plant Biology, Vol. 59, Issue 5 https://doi.org/10.1111/jipb.12532	journal	May 2017
Multispectral Phloem-Mobile Probes: Properties and Applications Knoblauch, Michael; Vendrell, Marc; de Leau, Erica Plant Physiology, Vol. 167, Issue 4 https://doi.org/10.1104/pp.114.255414	journal	February 2015
The Coumarin Glucoside, Esculin, Reveals Rapid Changes in Phloem-Transport Velocity in Response to Environmental Cues Knox, Kirsten; Paterlini, Andrea; Thomson, Simon Plant Physiology, Vol. 178, Issue 2 https://doi.org/10.1104/pp.18.00574	journal	August 2018
Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development Koch, Karen Current Opinion in Plant Biology, Vol. 7, Issue 3 https://doi.org/10.1016/j.pbi.2004.03.014	journal	June 2004
Transport and Sorting of the Solanum tuberosum Sucrose Transporter SUT1 Is Affected by Posttranslational Modification Krügel, Undine; Veenhoff, Liesbeth M.; Langbein, Jennifer The Plant Cell, Vol. 20, Issue 9 https://doi.org/10.1105/tpc.108.058271	journal	September 2008
ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging Kurihara, Daisuke; Mizuta, Yoko; Sato, Yoshikatsu Development https://doi.org/10.1242/dev.127613	journal	January 2015
Phloem loading and unloading of sugars and amino acids Lalonde, S.; Tegeder, M.; Throne-Holst, M. Plant, Cell and Environment, Vol. 26, Issue 1 https://doi.org/10.1046/j.1365-3040.2003.00847.x	journal	January 2003
Transport Mechanisms for Organic Forms of Carbon and Nitrogen Between Source and sink Lalonde, Sylvie; Wipf, Daniel; Frommer, Wolf B. Annual Review of Plant Biology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.arplant.55.031903.141758	journal	June 2004
Disruption of the Sugar Transporters AtSWEET11 and AtSWEET12 Affects Vascular Development and Freezing Tolerance in Arabidopsis Le Hir, Rozenn; Spinner, Lara; Klemens, Patrick A. W. Molecular Plant, Vol. 8, Issue 11 https://doi.org/10.1016/j.molp.2015.08.007	journal	November 2015
Sucrose transporter2 contributes to maize growth, development, and crop yield: ZmSUT2 contributes to plant growth and yield Leach, Kristen A.; Tran, Thu M.; Slewinski, Thomas L. Journal of Integrative Plant Biology, Vol. 59, Issue 6 https://doi.org/10.1111/jipb.12527	journal	April 2017
Overexpression of the sucrose transporter SoSUT1 in potato results in alterations in leaf carbon partitioning and in tuber metabolism but has little impact on tuber morphology Leggewie, Georg; Kolbe, Anna; Lemoine, Rémi Planta, Vol. 217, Issue 1 https://doi.org/10.1007/s00425-003-0975-x	journal	February 2003
Transport of sucrose, not hexose, in the phloem Liu, David D.; Chao, Wesley M.; Turgeon, Robert Journal of Experimental Botany, Vol. 63, Issue 11 https://doi.org/10.1093/jxb/ers127	journal	May 2012
FTIP1 Is an Essential Regulator Required for Florigen Transport Liu, Lu; Liu, Chang; Hou, Xingliang PLoS Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pbio.1001313	journal	April 2012
Manipulation of sucrose phloem and embryo loading affects pea leaf metabolism, carbon and nitrogen partitioning to sinks as well as seed storage pools Lu, Ming‐Zhu; Snyder, Rachel; Grant, Jan The Plant Journal, Vol. 101, Issue 1 https://doi.org/10.1111/tpj.14533	journal	October 2019
The Plant Vascular System: Evolution, Development and Functions ^F Lucas, William J.; Groover, Andrew; Lichtenberger, Raffael Journal of Integrative Plant Biology, Vol. 55, Issue 4 https://doi.org/10.1111/jipb.12041	journal	April 2013
An apple sucrose transporter MdSUT2.2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought Ma, Qi-Jun; Sun, Mei-Hong; Lu, Jing Plant Biotechnology Journal, Vol. 17, Issue 3 https://doi.org/10.1111/pbi.13003	journal	October 2018
Unraveling the puzzle of phloem parenchyma transfer cell wall ingrowth McCubbin, Tyler J.; Braun, David M. Journal of Experimental Botany, Vol. 71, Issue 16 https://doi.org/10.1093/jxb/eraa311	journal	July 2020
Phloem anatomy and function as shaped by the cell wall McCubbin, Tyler J.; Braun, David M. Journal of Plant Physiology, Vol. 266 https://doi.org/10.1016/j.jplph.2021.153526	journal	November 2021
Mechanisms of phloem unloading: shaped by cellular pathways, their conductances and sink function Milne, Ricky J.; Grof, Christopher PL; Patrick, John W. Current Opinion in Plant Biology, Vol. 43 https://doi.org/10.1016/j.pbi.2017.11.003	journal	June 2018
Transfer Cells: Cells Specialized for a Special Purpose Offler, Christina E.; McCurdy, David W.; Patrick, John W. Annual Review of Plant Biology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.arplant.54.031902.134812	journal	June 2003
Real-time imaging of phloem unloading in the root tip of Arabidopsis Oparka, K. J.; Duckett, C. M.; Prior, D. A. M. The Plant Journal, Vol. 6, Issue 5 https://doi.org/10.1046/j.1365-313X.1994.6050759.x	journal	November 1994
Simple, but Not Branched, Plasmodesmata Allow the Nonspecific Trafficking of Proteins in Developing Tobacco Leaves Oparka, Karl J.; Roberts, Alison G.; Boevink, Petra Cell, Vol. 97, Issue 6 https://doi.org/10.1016/S0092-8674(00)80786-2	journal	June 1999
Transfer Cells Pate, J. S.; Gunning, B. E. S. Annual Review of Plant Physiology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.pp.23.060172.001133	journal	June 1972
PHLOEM UNLOADING: Sieve Element Unloading and Post-Sieve Element Transport Patrick, J. W. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.arplant.48.1.191	journal	June 1997
Metabolic engineering of sugars and simple sugar derivatives in plants W. Patrick, John; C. Botha, Frikkie; G. Birch, Robert Plant Biotechnology Journal, Vol. 11, Issue 2 https://doi.org/10.1111/pbi.12002	journal	October 2012
Lost in Transit: Long-Distance Trafficking and Phloem Unloading of Protein Signals in Arabidopsis Homografts Paultre, Danae Simone Genevieve; Gustin, Marie-Paule; Molnar, Attila The Plant Cell, Vol. 28, Issue 9 https://doi.org/10.1105/tpc.16.00249	journal	September 2016
Protein phosphorylation plays a key role in sucrose-mediated transcriptional regulation of a phloem-specific proton?sucrose symporter Ransom-Hodgkins, Wendy D.; Vaughn, Matthew W.; Bush, Daniel R. Planta, Vol. 217, Issue 3 https://doi.org/10.1007/s00425-003-1011-x	journal	July 2003
Phloem Loading Strategies in Three Plant Species That Transport Sugar Alcohols Reidel, Edwin J.; Rennie, Emilie A.; Amiard, Véronique Plant Physiology, Vol. 149, Issue 3 https://doi.org/10.1104/pp.108.134791	journal	January 2009
Evolution of plant sucrose uptake transporters Reinders, Anke Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00022	journal	January 2012
Evolutionary gain of oligosaccharide hydrolysis and sugar transport enhanced carbohydrate partitioning in sweet watermelon fruits Ren, Yi; Li, Maoying; Guo, Shaogui The Plant Cell, Vol. 33, Issue 5 https://doi.org/10.1093/plcell/koab055	journal	February 2021
A comprehensive picture of phloem loading strategies Rennie, E. A.; Turgeon, R. Proceedings of the National Academy of Sciences, Vol. 106, Issue 33 https://doi.org/10.1073/pnas.0902279106	journal	July 2009
Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. Riesmeier, J. W.; Willmitzer, L.; Frommer, W. B. The EMBO Journal, Vol. 11, Issue 13 https://doi.org/10.1002/j.1460-2075.1992.tb05575.x	journal	December 1992
Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. Riesmeier, J. W.; Willmitzer, L.; Frommer, W. B. The EMBO Journal, Vol. 13, Issue 1 https://doi.org/10.1002/j.1460-2075.1994.tb06229.x	journal	January 1994
Increased capacity for sucrose uptake leads to earlier onset of protein accumulation in developing pea seeds Rosche, Elke G.; Blackmore, Daniel; Offler, Christina E. Functional Plant Biology, Vol. 32, Issue 11 https://doi.org/10.1071/FP05127	journal	January 2005
Seed-specific overexpression of a potato sucrose transporter increases sucrose uptake and growth rates of developing pea cotyledons Rosche, Elke; Blackmore, Daniel; Tegeder, Mechthild The Plant Journal, Vol. 30, Issue 2 https://doi.org/10.1046/j.1365-313X.2002.01282.x	journal	April 2002
Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle Ross-Elliott, Timothy J.; Jensen, Kaare H.; Haaning, Katrine S. eLife, Vol. 6 https://doi.org/10.7554/eLife.24125	journal	February 2017
Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling Ruan, Yong-Ling Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040251	journal	April 2014
Leaf vasculature in Zea mays L. Russell, S. H.; Evert, R. F. Planta, Vol. 164, Issue 4 https://doi.org/10.1007/BF00395960	journal	January 1985
Molecular physiology of higher plant sucrose transporters Sauer, Norbert FEBS Letters, Vol. 581, Issue 12 https://doi.org/10.1016/j.febslet.2007.03.048	journal	March 2007
Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis Scofield, Graham N.; Hirose, Tatsuro; Gaudron, Judy A. Functional Plant Biology, Vol. 29, Issue 7 https://doi.org/10.1071/PP01204	journal	January 2002
Current perspectives on the regulation of whole-plant carbohydrate partitioning Slewinski, Thomas L.; Braun, David M. Plant Science, Vol. 178, Issue 4 https://doi.org/10.1016/j.plantsci.2010.01.010	journal	April 2010
The Psychedelic Genes of Maize Redundantly Promote Carbohydrate Export From Leaves Slewinski, Thomas L.; Braun, David M. Genetics, Vol. 185, Issue 1 https://doi.org/10.1534/genetics.109.113357	journal	February 2010
Maize SUT1 functions in phloem loading Slewinski, Thomas L.; Garg, Anshu; Johal, Gurmukh S. Plant Signaling & Behavior, Vol. 5, Issue 6 https://doi.org/10.4161/psb.5.6.11575	journal	June 2010
Sucrose transporter1 functions in phloem loading in maize leaves Slewinski, Thomas L.; Meeley, Robert; Braun, David M. Journal of Experimental Botany, Vol. 60, Issue 3 https://doi.org/10.1093/jxb/ern335	journal	January 2009
Structural and functional heterogeneity in phloem loading and transport Slewinski, Thomas L.; Zhang, Cankui; Turgeon, Robert Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00244	journal	January 2013
Starch: A Flexible, Adaptable Carbon Store Coupled to Plant Growth Smith, Alison M.; Zeeman, Samuel C. Annual Review of Plant Biology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-arplant-050718-100241	journal	April 2020
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 Srivastava, Avinash C.; Dasgupta, Kasturi; Ajieren, Eric Annals of Botany, Vol. 104, Issue 6 https://doi.org/10.1093/aob/mcp215	journal	September 2009
Functional Characterization of the Arabidopsis AtSUC2 Sucrose/H ⁺ Symporter by Tissue-Specific Complementation Reveals an Essential Role in Phloem Loading But Not in Long-Distance Transport Srivastava, Avinash C.; Ganesan, Savita; Ismail, Ihab O. Plant Physiology, Vol. 148, Issue 1 https://doi.org/10.1104/pp.108.124776	journal	July 2008
Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots Stadler, Ruth; Wright, Kathryn M.; Lauterbach, Christian The Plant Journal, Vol. 41, Issue 2 https://doi.org/10.1111/j.1365-313X.2004.02298.x	journal	December 2004
Amino acid transporter expression and localisation studies in pea (Pisum sativum) Tegeder, Mechthild; Tan, Qiumin; Grennan, Aleel K. Functional Plant Biology, Vol. 34, Issue 11 https://doi.org/10.1071/FP07107	journal	January 2007
Sucrose transport into developing seeds of Pisum sativum L. Tegeder, Mechthild; Wang, Xin-Ding; Frommer, Wolf B. . The Plant Journal, Vol. 18, Issue 2 https://doi.org/10.1046/j.1365-313X.1999.00439.x	journal	April 1999
Maize Carbohydrate Partitioning Defective33 Encodes an MCTP Protein and Functions in Sucrose Export from Leaves Tran, Thu M.; McCubbin, Tyler J.; Bihmidine, Saadia Molecular Plant, Vol. 12, Issue 9 https://doi.org/10.1016/j.molp.2019.05.001	journal	September 2019
Phloem Loading: How Leaves Gain Their Independence Turgeon, Robert BioScience, Vol. 56, Issue 1 https://doi.org/10.1641/0006-3568(2006)056[0015:PLHLGT]2.0.CO;2	journal	January 2006
Phloem Transport: Cellular Pathways and Molecular Trafficking Turgeon, Robert; Wolf, Shmuel Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.092045	journal	June 2009
The C2-domain protein QUIRKY and the receptor-like kinase STRUBBELIG localize to plasmodesmata and mediate tissue morphogenesis in Arabidopsis thaliana Vaddepalli, Prasad; Herrmann, Anja; Fulton, Lynette Development, Vol. 141, Issue 21 https://doi.org/10.1242/dev.113878	journal	November 2014
The phloem, a miracle of ingenuity Van Bel, A. J. E. Plant, Cell and Environment, Vol. 26, Issue 1 https://doi.org/10.1046/j.1365-3040.2003.00963.x	journal	January 2003
Tuberization in Potato Involves a Switch from Apoplastic to Symplastic Phloem Unloading Viola, Roberto; Roberts, Alison G.; Haupt, Sophie The Plant Cell, Vol. 13, Issue 2 https://doi.org/10.1105/tpc.13.2.385	journal	February 2001
Evidence for functional heterogeneity of sieve element–companion cell complexes in minor vein phloem of Alonsoa meridionalis Voitsekhovskaja, Olga V.; Rudashevskaya, Elena L.; Demchenko, Kirill N. Journal of Experimental Botany, Vol. 60, Issue 6 https://doi.org/10.1093/jxb/erp074	journal	March 2009
Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. von Schaewen, A.; Stitt, M.; Schmidt, R. The EMBO Journal, Vol. 9, Issue 10 https://doi.org/10.1002/j.1460-2075.1990.tb07499.x	journal	October 1990
Phloem loading in rice leaves depends strongly on the apoplastic pathway Wang, Gaopeng; Wu, Yue; Ma, Li Journal of Experimental Botany, Vol. 72, Issue 10 https://doi.org/10.1093/jxb/erab085	journal	February 2021
Studies on the root of Hordeum Vulgare l.– Ultrastructure of the Seminal root with Special Reference to the Phloem Warmbrodt, Robert D. American Journal of Botany, Vol. 72, Issue 3 https://doi.org/10.1002/j.1537-2197.1985.tb05365.x	journal	March 1985
Sucrose regulates wall ingrowth deposition in phloem parenchyma transfer cells in Arabidopsis via affecting phloem loading activity Wei, Xiaoyang; Nguyen, Suong T. T.; Collings, David A. Journal of Experimental Botany, Vol. 71, Issue 16 https://doi.org/10.1093/jxb/eraa246	journal	May 2020
Increasing Sucrose Uptake Capacity of Wheat Grains Stimulates Storage Protein Synthesis Weichert, Nicola; Saalbach, Isolde; Weichert, Heiko Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.150854	journal	December 2009
A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake: Regulation of vacuolar glucose transport Wingenter, Karina; Trentmann, Oliver; Winschuh, Irina The Plant Journal, Vol. 68, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04739.x	journal	September 2011
Molecular Identification and Physiological Characterization of a Novel Monosaccharide Transporter from Arabidopsis Involved in Vacuolar Sugar Transport Wormit, Alexandra; Trentmann, Oliver; Feifer, Ingmar The Plant Cell, Vol. 18, Issue 12 https://doi.org/10.1105/tpc.106.047290	journal	December 2006
The fluorescent probe HPTS as a phloem-mobile, symplastic tracer: an evaluation using confocal laser scanning microscopy Wright, Kathryn M.; Oparka, Karl J. Journal of Experimental Botany, Vol. 47, Issue 3 https://doi.org/10.1093/jxb/47.3.439	journal	January 1996
Rice Transcription Factor OsDOF11 Modulates Sugar Transport by Promoting Expression of Sucrose Transporter and SWEET Genes Wu, Yunfei; Lee, Sang-Kyu; Yoo, Youngchul Molecular Plant, Vol. 11, Issue 6 https://doi.org/10.1016/j.molp.2018.04.002	journal	June 2018
Regulation of Sucrose Transporters and Phloem Loading in Response to Environmental Cues Xu, Qiyu; Chen, Siyuan; Yunjuan, Ren Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.01088	journal	November 2017
Sugar export from Arabidopsis leaves: actors and regulatory strategies Xu, Qiyu; Liesche, Johannes Journal of Experimental Botany, Vol. 72, Issue 15 https://doi.org/10.1093/jxb/erab241	journal	May 2021
Carbon export from leaves is controlled via ubiquitination and phosphorylation of sucrose transporter SUC2 Xu, Qiyu; Yin, Shijiao; Ma, Yue Proceedings of the National Academy of Sciences, Vol. 117, Issue 11 https://doi.org/10.1073/pnas.1912754117	journal	March 2020
When SWEETs Turn Tweens: Updates and Perspectives Xue, Xueyi; Wang, Jiang; Shukla, Diwakar Annual Review of Plant Biology, Vol. 73, Issue 1 https://doi.org/10.1146/annurev-arplant-070621-093907	journal	May 2022
Cotton phloem loads from the apoplast using a single member of its nine-member sucrose transporter gene family Yadav, Umesh P.; Evers, John F.; Shaikh, Mearaj A. Journal of Experimental Botany, Vol. 73, Issue 3 https://doi.org/10.1093/jxb/erab461	journal	October 2021
Regulation of sugar transporter activity for antibacterial defense in Arabidopsis Yamada, Kohji; Saijo, Yusuke; Nakagami, Hirofumi Science, Vol. 354, Issue 6318 https://doi.org/10.1126/science.aah5692	journal	November 2016
Symplastic Phloem Loading in Poplar Zhang, Cankui; Han, Lu; Slewinski, Thomas L. Plant Physiology, Vol. 166, Issue 1 https://doi.org/10.1104/pp.114.245845	journal	July 2014
Two evolutionarily duplicated domains individually and post‐transcriptionally controlSWEETexpression for phloem transport Zhang, Chen; Li, Ye; Wang, Jiang New Phytologist, Vol. 232, Issue 4 https://doi.org/10.1111/nph.17688	journal	September 2021
Mechanisms of phloem loading Zhang, Cankui; Turgeon, Robert Current Opinion in Plant Biology, Vol. 43 https://doi.org/10.1016/j.pbi.2018.01.009	journal	June 2018
Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids Zhang, Lizhi; Garneau, Matthew G.; Majumdar, Rajtilak The Plant Journal, Vol. 81, Issue 1 https://doi.org/10.1111/tpj.12716	journal	December 2014
Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons Zhou, Yuchan; Chan, Katie; Wang, Trevor L. Journal of Experimental Botany, Vol. 60, Issue 1 https://doi.org/10.1093/jxb/ern254	journal	October 2008
MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato Zhu, Lingcheng; Li, Baiyun; Wu, Limin Proceedings of the National Academy of Sciences, Vol. 118, Issue 1 https://doi.org/10.1073/pnas.2022788118	journal	December 2020
Tuber and Tuberous Root Development Zierer, Wolfgang; Rüscher, David; Sonnewald, Uwe Annual Review of Plant Biology, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-arplant-080720-084456	journal	June 2021

Similar Records

Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression

Journal Article · Thu Jul 30 00:00:00 EDT 2015 · BMC Plant Biology · OSTI ID:1980839

Bihmidine, Saadia; Baker, R. Frank; Hoffner, Cassandra; +1 more

Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock‐out mutants in Zea mays

Journal Article · Fri Feb 16 00:00:00 EST 2018 · New Phytologist · OSTI ID:1980839

Bezrutczyk, Margaret; Hartwig, Thomas; Horschman, Marc; +5 more

Sucrose transport and phloem unloading in stem of Vicia faba: possible involvement of a sucrose carrier and osmotic regulation

Journal Article · Sun Jun 01 00:00:00 EDT 1986 · Plant Physiol.; (United States) · OSTI ID:1980839

Aloni, B; Wyse, R E; Griffith, S

Related Subjects

Plant Sciences

Title: Phloem Loading and Unloading of Sucrose: What a Long, Strange Trip from Source to Sink

Citation Formats

References (149)

Similar Records

Related Subjects