1932

Abstract

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.

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2022-05-20
2024-04-20
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Literature Cited

  1. 1.
    Abelenda JA, Bergonzi S, Oortwijn M, Sonnewald S, Du M et al. 2019. Source-sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr. Biol. 29:1178–86.e6Interaction between StSP6A and StSWEET11 proteins inhibited sugar efflux and promoted apoplasmic-to-symplasmic phloem unloading.
    [Google Scholar]
  2. 2.
    Antony G, Zhou J, Huang S, Li T, Liu B et al. 2010. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–76
    [Google Scholar]
  3. 3.
    Ayre BG. 2011. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol. Plant 4:377–94
    [Google Scholar]
  4. 4.
    Baker RF, Leach KA, Boyer NR, Swyers MJ, Benitez-Alfonso Y et al. 2016. Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading. Plant Physiol 172:1876–98
    [Google Scholar]
  5. 5.
    Baker RF, Leach KA, Braun DM. 2012. SWEET as sugar: New sucrose effluxers in plants. Mol. Plant 5:766–68
    [Google Scholar]
  6. 6.
    Beebe DU, Turgeon R. 1992. Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves. Planta 188:354–61
    [Google Scholar]
  7. 7.
    Bezrutczyk M, Hartwig T, Horschman M, Char SN, Yang J et al. 2018. Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays. New Phytol. 218:594–603
    [Google Scholar]
  8. 8.
    Bezrutczyk M, Zöllner NR, Kruse CPS, Hartwig T, Lautwein T et al. 2021. Evidence for phloem loading via the abaxial bundle sheath cells in maize leaves. Plant Cell 33:531–47Identified distinct bundle sheath (BS) cells in maize leaves; demonstrated that ZmSWEET13 proteins are preferentially expressed in abBS cells.
    [Google Scholar]
  9. 9.
    Bihmidine S, Hunter CTIII, Johns CE, Koch KE, Braun DM. 2013. Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front. Plant Sci. 4:177
    [Google Scholar]
  10. 10.
    Bihmidine S, Julius BT, Dweikat I, Braun DM 2016. Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems. Plant Signal. Behav. 11:e1117721
    [Google Scholar]
  11. 11.
    Boorer KJ, Loo DDF, Frommer WB, Wright EM. 1996. Transport mechanism of the cloned potato H+/sucrose cotransporter StSUT1. J. Biol. Chem. 271:25139–44
    [Google Scholar]
  12. 12.
    Botha CEJ 2005. Interaction of phloem and xylem during phloem loading: functional symplasmic roles for thin- and thick-walled sieve tubes in monocotyledons. Vascular Transport in Plants NM Holbrook, MA Zwieniecki 115–30 Amsterdam: Elsevier
    [Google Scholar]
  13. 13.
    Botha CEJ, Murugan N. 2021. Changes in structure and dimension of plasmodesmata in the phloem loading pathway in Tecoma capensis (Bignoniaceae)—locating the polymer trap. S. Afr. J. Bot. 140:76–86
    [Google Scholar]
  14. 14.
    Brault ML, Petit JD, Immel F, Nicolas WJ, Glavier M et al. 2019. Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep 20:e47182
    [Google Scholar]
  15. 15.
    Braun DM, Ma Y, Inada N, Muszynski MG, Baker RF. 2006. tie-dyed1 regulates carbohydrate accumulation in maize leaves. Plant Physiol 142:1511–22
    [Google Scholar]
  16. 16.
    Braun DM, Slewinski TL. 2009. Genetic control of carbon partitioning in grasses: roles of Sucrose Transporters and Tie-dyed loci in phloem loading. Plant Physiol 149:71–81
    [Google Scholar]
  17. 17.
    Braun DM, Wang L, Ruan Y-L 2014. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J. Exp. Bot. 65:1713–35
    [Google Scholar]
  18. 18.
    Bürkle L, Hibberd JM, Quick WP, Kühn C, Hirner B, Frommer WB. 1998. The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol 118:59–68
    [Google Scholar]
  19. 19.
    Bush DR. 1990. Electrogenicity, pH-dependence, and stoichiometry of the proton-sucrose symport. Plant Physiol 93:1590–96
    [Google Scholar]
  20. 20.
    Bush DR. 1993. Proton-coupled sugar and amino acid transporters in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:513–42
    [Google Scholar]
  21. 21.
    Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R 2005. Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J. Biol. Chem. 280:21437–43
    [Google Scholar]
  22. 22.
    Casu RE, Rae AL, Nielsen JM, Perroux JM, Bonnett GD, Manners JM. 2015. Tissue-specific transcriptome analysis within the maturing sugarcane stalk reveals spatial regulation in the expression of cellulose synthase and sucrose transporter gene families. Plant Mol. Biol. 89:607–28
    [Google Scholar]
  23. 23.
    Chen L-Q, Cheung LS, Feng L, Tanner W, Frommer WB 2015. Transport of sugars. Annu. Rev. Biochem. 84:865–94
    [Google Scholar]
  24. 24.
    Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–32
    [Google Scholar]
  25. 25.
    Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–11Identified redundant SWEET11 and SWEET12 sucrose effluxers that function in phloem loading in Arabidopsis leaves.
    [Google Scholar]
  26. 26.
    Chen Q, Hu T, Li X, Song C-P, Zhu J-K et al. 2021. Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought. Nat. Plants 8:68–77Demonstrated phosphorylation of AtSWEET11 and AtSWEET12 by SnRK2 under drought, enhancing sucrose transport and root growth.
    [Google Scholar]
  27. 27.
    Chen Q, Payyavula RS, Chen L, Zhang J, Zhang C, Turgeon R. 2018. FLOWERING LOCUS T mRNA is synthesized in specialized companion cells in Arabidopsis and Maryland Mammoth tobacco leaf veins. PNAS 115:2830–35Identified distinct companion cell populations in Arabidopsis and tobacco leaves; demonstrated that AtFT is produced in only one.
    [Google Scholar]
  28. 28.
    Cheng J, Wen S, Xiao S, Lu B, Ma M, Bie Z 2017. Overexpression of the tonoplast sugar transporter CmTST2 in melon fruit increases sugar accumulation. J. Exp. Bot. 69:511–23
    [Google Scholar]
  29. 29.
    Corbesier L, Vincent C, Jang S, Fornara F, Fan Q et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–33
    [Google Scholar]
  30. 30.
    Cui W, Lee J-Y. 2016. Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nat. Plants 2:16034
    [Google Scholar]
  31. 31.
    Dasgupta K, Khadilkar AS, Sulpice R, Pant B, Scheible W-R et al. 2014. 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. Plant Physiol 165:715–31
    [Google Scholar]
  32. 32.
    Deng J, Yang X, Sun W, Miao Y, He L, Zhang X. 2020. The calcium sensor CBL2 and its interacting kinase CIPK6 are involved in plant sugar homeostasis via interacting with tonoplast sugar transporter TST2. Plant Physiol 183:236–49
    [Google Scholar]
  33. 33.
    Dengler N, Kang J. 2001. Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4:50–56
    [Google Scholar]
  34. 34.
    Dhungana SR, Braun DM. 2021. Sugar transporters in grasses: function and modulation in source and storage tissues. J. Plant Phys. 266:153541
    [Google Scholar]
  35. 35.
    Edwards GE, Franceschi VR, Ku MSB, Voznesenskaya EV, Pyankov VI, Andreo CS. 2001. Compartmentation of photosynthesis in cells and tissues of C4 plants. J. Exp. Bot. 52:577–90
    [Google Scholar]
  36. 36.
    Endler A, Meyer S, Schelbert S, Schneider T, Weschke W et al. 2006. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141:196–207
    [Google Scholar]
  37. 37.
    Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin IW et al. 2015. SWEETs, transporters for intracellular and intercellular sugar translocation. Curr. Opin. Plant Biol. 25:53–62
    [Google Scholar]
  38. 38.
    Eom J-S, Cho J-I, Reinders A, Lee S-W, Yoo Y et al. 2011. Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol 157:109–19
    [Google Scholar]
  39. 39.
    Eom J-S, Choi S-B, Ward JM, Jeon J-S. 2012. The mechanism of phloem loading in rice (Oryza sativa). Mol. Cells 33:431–38
    [Google Scholar]
  40. 40.
    Esau K. 1977. Anatomy of Seed Plants New York: Wiley
  41. 41.
    Evert RF. 1982. Sieve-tube structure in relation to function. Bioscience 32:789–95
    [Google Scholar]
  42. 42.
    Evert RF, Eschrich W, Heyser W 1977. Distribution and structure of the plasmodesmata in mesophyll and bundle sheath cells of Zea mays L. Planta 136:77–89
    [Google Scholar]
  43. 43.
    Evert RF, Eschrich W, Heyser W 1978. Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138:279–94
    [Google Scholar]
  44. 44.
    Evert RF, Russin WA, Bosabalidis AM. 1996. Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. Int. J. Plant Sci. 157:247–61
    [Google Scholar]
  45. 45.
    Ewing EE, Wareing PF. 1978. Shoot, stolon, and tuber formation on potato (Solanum tuberosum L.) cuttings in response to photoperiod. Plant Physiol 61:348–53
    [Google Scholar]
  46. 46.
    Fei H, Yang Z, Lu Q, Wen X, Zhang Y et al. 2021. OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice. Plant Sci 306:110851
    [Google Scholar]
  47. 47.
    Fritz E, Evert RF, Heyser W. 1983. Microautoradiographic studies of phloem loading and transport in the leaf of Zea mays L. Planta 159:193–206
    [Google Scholar]
  48. 48.
    Fritz E, Evert RF, Nasse H. 1989. Loading and transport of assimilates in different maize leaf bundles: digital image analysis of 14C-microautoradiographs. Planta 178:1–9
    [Google Scholar]
  49. 49.
    Gamalei Y. 1989. Structure and function of leaf minor veins in trees and herbs: a taxonomic review. Trees 3:96–110
    [Google Scholar]
  50. 50.
    Garg V, Kühn C. 2020. What determines the composition of the phloem sap? Is there any selectivity filter for macromolecules entering the phloem sieve elements?. Plant Physiol. Biochem. 151:284–91
    [Google Scholar]
  51. 51.
    Geiger D, Giaquinta R, Sovonick S, Fellows R 1973. Solute distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol 52:585–89
    [Google Scholar]
  52. 52.
    Gersony JT, McClelland A, Holbrook NM. 2021. Raman spectroscopy reveals high phloem sugar content in leaves of canopy red oak trees. New Phytol 232:418–24
    [Google Scholar]
  53. 53.
    Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR. 2000. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. PNAS 97:13979–84
    [Google Scholar]
  54. 54.
    Grant JE, Ninan A, Cripps-Guazzone N, Shaw M, Song J et al. 2021. Concurrent overexpression of amino acid permease AAP1(3a) and SUT1 sucrose transporter in pea resulted in increased seed number and changed cytokinin and protein levels. Funct. Plant Biol. 48:889–904
    [Google Scholar]
  55. 55.
    Guo W-J, Nagy R, Chen H-Y, Pfrunder S, Yu Y-C et al. 2013. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol 164:777–89
    [Google Scholar]
  56. 56.
    Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kühn C. 2006. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45:180–92
    [Google Scholar]
  57. 57.
    Haritatos E, Ayre BG, Turgeon R. 2000. Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter. Plant Physiol 123:929–37
    [Google Scholar]
  58. 58.
    Haritatos E, Medville R, Turgeon R 2000. Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211:105–11
    [Google Scholar]
  59. 59.
    Haupt S, Duncan GH, Holzberg S, Oparka KJ 2001. Evidence for symplastic phloem unloading in sink leaves of barley. Plant Physiol 125:209–18
    [Google Scholar]
  60. 60.
    Heyser W, Evert RF, Fritz E, Eschrich W 1978. Sucrose in the free space of translocating maize leaf bundles. Plant Physiol 62:491–94
    [Google Scholar]
  61. 61.
    Hirose T, Zhang Z, Miyao A, Hirochika H, Ohsugi R, Terao T 2010. Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. J. Exp. Bot. 61:3639–46
    [Google Scholar]
  62. 62.
    Hunter K. 2020. CBL2-CIPK6-TST2-mediated regulation of sugar homeostasis. Plant Physiol 183:21–22
    [Google Scholar]
  63. 63.
    Ishimaru K, Hirose T, Aoki N, Takahashi S, Ono K et al. 2001. Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant Cell Physiol. 42:1181–85
    [Google Scholar]
  64. 64.
    Jeannette E, Reyss A, Grégory N, Gantet P, Prioul J-L 2000. Carbohydrate metabolism in a heat-girdled maize source leaf. Plant Cell Environ 23:61–69
    [Google Scholar]
  65. 65.
    Jones AM, Xuan Y, Xu M, Wang R-S, Ho C-H et al. 2014. Border control—a membrane-linked interactome of Arabidopsis. Science 344:711–16
    [Google Scholar]
  66. 66.
    Julius BT, Leach KA, Tran TM, Mertz RA, Braun DM. 2017. Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol 58:1442–60
    [Google Scholar]
  67. 67.
    Julius BT, Slewinski TL, Baker RF, Tzin V, Zhou S et al. 2018. Maize Carbohydrate partitioning defective1 impacts carbohydrate distribution, callose accumulation, and phloem function. J. Exp. Bot. 69:3917–31
    [Google Scholar]
  68. 68.
    Jung B, Ludewig F, Schulz A, Meißner G, Wöstefeld N et al. 2015. Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat. Plants 1:14001
    [Google Scholar]
  69. 69.
    Kaiser G, Heber U. 1984. Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 161:562–68
    [Google Scholar]
  70. 70.
    Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T et al. 2016. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat. Commun. 7:13245
    [Google Scholar]
  71. 71.
    Kim J-Y, Symeonidi E, Pang TY, Denyer T, Weidauer D et al. 2021. Distinct identities of leaf phloem cells revealed by single cell transcriptomics. Plant Cell 33:511–30Performed single-cell RNA sequencing; identified cell-specific expression patterns in Arabidopsis leaves and two types of phloem parenchyma cells.
    [Google Scholar]
  72. 72.
    Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA et al. 2016. Testing the Münch hypothesis of long distance phloem transport in plants. eLife 5:e15341Demonstrated anatomical changes to leaf sieve elements with increasing distance from sink tissues, supporting the Münch hypothesis.
    [Google Scholar]
  73. 73.
    Knoblauch M, Peters WS. 2017. What actually is the Münch hypothesis? A short history of assimilate transport by mass flow. J. Int. Plant Biol. 59:292–310
    [Google Scholar]
  74. 74.
    Knoblauch M, Vendrell M, de Leau E, Paterlini A, Knox K et al. 2015. Multispectral phloem-mobile probes: properties and applications. Plant Physiol 167:1211–20
    [Google Scholar]
  75. 75.
    Knox K, Paterlini A, Thomson S, Oparka K. 2018. The coumarin glucoside, esculin, reveals rapid changes in phloem-transport velocity in response to environmental cues. Plant Physiol 178:795–807
    [Google Scholar]
  76. 76.
    Koch K. 2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7:235–46
    [Google Scholar]
  77. 77.
    Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J et al. 2008. Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification. Plant Cell 20:2497–513
    [Google Scholar]
  78. 78.
    Kurihara D, Mizuta Y, Sato Y, Higashiyama T. 2015. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142:4168–79
    [Google Scholar]
  79. 79.
    Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW. 2003. Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26:37–56
    [Google Scholar]
  80. 80.
    Lalonde S, Wipf D, Frommer WB 2004. Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu. Rev. Plant Biol. 55:341–72
    [Google Scholar]
  81. 81.
    Le Hir R, Spinner L, Klemens PA, Chakraborti D, de Marco F et al. 2015. Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular development and freezing tolerance in Arabidopsis. Mol. Plant 8:1687–90
    [Google Scholar]
  82. 82.
    Leach KA, Tran TM, Slewinski TL, Meeley RB, Braun DM. 2017. Sucrose transporter2 contributes to maize growth, development, and crop yield. J. Int. Plant Biol. 59:390–408
    [Google Scholar]
  83. 83.
    Leggewie G, Kolbe A, Lemoine R, Roessner U, Lytovchenko A et al. 2003. 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. Planta 217:158–67
    [Google Scholar]
  84. 84.
    Liu DD, Chao WM, Turgeon R. 2012. Transport of sucrose, not hexose, in the phloem. J. Exp. Bot. 63:4315–20
    [Google Scholar]
  85. 85.
    Liu L, Liu C, Hou X, Xi W, Shen L et al. 2012. FTIP1 is an essential regulator required for florigen transport. PLOS Biol 10:e1001313
    [Google Scholar]
  86. 86.
    Lu MZ, Snyder R, Grant J, Tegeder M 2020. Manipulation of sucrose phloem and embryo loading affects pea leaf metabolism, carbon and nitrogen partitioning to sinks as well as seed storage pools. Plant J 101:217–36Used push–pull strategy to simultaneously increase source and sink strengths to improve yield in pea.
    [Google Scholar]
  87. 87.
    Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav S-R et al. 2013. The plant vascular system: evolution, development and functions. J. Int. Plant Biol. 55:294–388
    [Google Scholar]
  88. 88.
    Ma Q-J, Sun M-H, Lu J, Kang H, You C-X, Hao Y-J. 2019. An apple sucrose transporter MdSUT2.2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought. Plant Biotech. J. 17:625–37
    [Google Scholar]
  89. 89.
    McCubbin TJ, Braun DM. 2020. Unraveling the puzzle of phloem parenchyma transfer cell wall ingrowth. J. Exp. Bot. 71:4617–20
    [Google Scholar]
  90. 90.
    McCubbin TJ, Braun DM. 2021. Phloem anatomy and function as shaped by the cell wall. J. Plant Phys. 266:153526
    [Google Scholar]
  91. 91.
    Milne RJ, Grof CP, Patrick JW. 2018. Mechanisms of phloem unloading: shaped by cellular pathways, their conductances and sink function. Curr. Opin. Plant Biol. 43:8–15
    [Google Scholar]
  92. 92.
    Münch E. 1930. Die Stoffbewegungen in der Pflanze Jena, Ger: Gustav Fischer
  93. 93.
    Offler CE, McCurdy DW, Patrick JW, Talbot MJ 2003. Transfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54:431–54
    [Google Scholar]
  94. 94.
    Ohshima T, Hayashi H, Chino M. 1990. Collection and chemical composition of pure phloem sap from Zea mays L. Plant Cell Physiol 31:735–37
    [Google Scholar]
  95. 95.
    Oparka K, Duckett C, Prior D, Fisher D. 1994. Real-time imaging of phloem unloading in the root tip of Arabidopsis. Plant J 6:759–66
    [Google Scholar]
  96. 96.
    Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts L et al. 1999. Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–54
    [Google Scholar]
  97. 97.
    Pate J, Gunning B. 1972. Transfer cells. Annu. Rev. Plant Physiol. 23:173–96
    [Google Scholar]
  98. 98.
    Patrick JW. 1997. Phloem unloading: sieve element unloading and post-sieve element transport. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:191–222
    [Google Scholar]
  99. 99.
    Patrick JW, Botha FC, Birch RG. 2013. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotech. J. 11:142–56
    [Google Scholar]
  100. 100.
    Paultre DSG, Gustin M-P, Molnar A, Oparka KJ. 2016. Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–25
    [Google Scholar]
  101. 101.
    Ransom-Hodgkins W, Vaughn M, Bush D 2003. Protein phosphorylation plays a key role in sucrose-mediated transcriptional regulation of a phloem-specific proton-sucrose symporter. Planta 217:483–89
    [Google Scholar]
  102. 102.
    Reidel EJ, Rennie EA, Amiard V, Cheng L, Turgeon R. 2009. Phloem loading strategies in three plant species that transport sugar alcohols. Plant Physiol 149:1601–8
    [Google Scholar]
  103. 103.
    Reinders A, Sivitz AB, Ward JM. 2012. Evolution of plant sucrose uptake transporters. Front. Plant Sci. 3:22
    [Google Scholar]
  104. 104.
    Ren Y, Li M, Guo S, Sun H, Zhao J et al. 2021. Evolutionary gain of oligosaccharide hydrolysis and sugar transport enhanced carbohydrate partitioning in sweet watermelon fruits. Plant Cell 33:1554–73
    [Google Scholar]
  105. 105.
    Rennie EA, Turgeon R 2009. A comprehensive picture of phloem loading strategies. PNAS 106:14162–67
    [Google Scholar]
  106. 106.
    Riesmeier JW, Willmitzer L, Frommer WB. 1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11:4705–13
    [Google Scholar]
  107. 107.
    Riesmeier JW, Willmitzer L, Frommer WB. 1994. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13:1–7
    [Google Scholar]
  108. 108.
    Rosche EG, Blackmore D, Offler CE, Patrick JW. 2005. Increased capacity for sucrose uptake leads to earlier onset of protein accumulation in developing pea seeds. Funct. Plant Biol. 32:997–1007
    [Google Scholar]
  109. 109.
    Rosche EG, Blackmore D, Tegeder M, Richardson T, Schroeder H et al. 2002. Seed-specific overexpression of a potato sucrose transporter increases sucrose uptake and growth rates of developing pea cotyledons. Plant J 30:165–75
    [Google Scholar]
  110. 110.
    Ross-Elliott TJ, Jensen KH, Haaning KS, Wager BM, Knoblauch J et al. 2017. Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife 6e24125Characterized phloem unloading in developing protophloem sieve elements; determined that unloading was occurring into phloem pole pericycle cells through funnel plasmodesmata.
  111. 111.
    Ruan Y-L. 2014. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu. Rev. Plant Biol. 65:33–67
    [Google Scholar]
  112. 112.
    Russell SH, Evert RF. 1985. Leaf vasculature in Zea mays L. Planta 164:448–58
    [Google Scholar]
  113. 113.
    Sauer N. 2007. Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–17
    [Google Scholar]
  114. 114.
    Scofield G, Hirose T, Gaudron J, Upadhyaya N, Ohsugi R, Furbank RT 2002. Antisense suppression of the rice sucrose transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Funct. Plant Biol. 29:815–26
    [Google Scholar]
  115. 115.
    Slewinski TL, Braun DM. 2010. Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Sci 178:341–49
    [Google Scholar]
  116. 116.
    Slewinski TL, Braun DM. 2010. The psychedelic genes of maize redundantly promote carbohydrate export from leaves. Genetics 185:221–32
    [Google Scholar]
  117. 117.
    Slewinski TL, Garg A, Johal GS, Braun DM. 2010. Maize SUT1 functions in phloem loading. Plant Signal. Behav. 5:687–90
    [Google Scholar]
  118. 118.
    Slewinski TL, Meeley R, Braun DM. 2009. Sucrose transporter1 functions in phloem loading in maize leaves. J. Exp. Bot. 60:881–92
    [Google Scholar]
  119. 119.
    Slewinski TL, Zhang C, Turgeon R. 2013. Structural and functional heterogeneity in phloem loading and transport. Front. Plant Sci. 4:244
    [Google Scholar]
  120. 120.
    Smith AM, Zeeman SC. 2020. Starch: a flexible, adaptable carbon store coupled to plant growth. Annu. Rev. Plant Biol. 71:217–45
    [Google Scholar]
  121. 121.
    Srivastava AC, Dasgupta K, Ajieren E, Costilla G, McGarry RC, Ayre BG. 2009. 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. 104:1121–28
    [Google Scholar]
  122. 122.
    Srivastava AC, Ganesan S, Ismail IO, Ayre BG 2008. Functional characterization of the Arabidopsis thaliana AtSUC2 Suc/H+ symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 147:200–11
    [Google Scholar]
  123. 123.
    Stadler R, Sauer N. 2019. The AtSUC2 promoter: a powerful tool to study phloem physiology and development. Methods Mol. Biol. 2014:267–87
    [Google Scholar]
  124. 124.
    Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M et al. 2005. 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. Plant J 41:319–31
    [Google Scholar]
  125. 125.
    Tegeder M, Tan Q, Grennan AK, Patrick JW. 2007. Amino acid transporter expression and localisation studies in pea (Pisum sativum). Funct. Plant Biol. 34:1019–28
    [Google Scholar]
  126. 126.
    Tegeder M, Wang X-D, Frommer WB, Offler CE, Patrick JW. 1999. Sucrose transport into developing seeds of Pisum sativum L. Plant J 18:151–61
    [Google Scholar]
  127. 127.
    Tran TM, McCubbin TJ, Bihmidine S, Julius B, Baker RF et al. 2019. Maize Carbohydrate partitioning defective33 encodes a MCTP protein and functions in sucrose export from leaves. Mol. Plant 12:1278–93
    [Google Scholar]
  128. 128.
    Turgeon R 1991. Symplastic phloem loading and the sink-source transition in leaves: a model. Recent Advances in Phloem Transport and Assimilate Compartmentation J-L Bonnemain, S Delrot, WJ Lucas, J Dainty 18–22 Nantes, Fr: Quest Editions
    [Google Scholar]
  129. 129.
    Turgeon R. 2006. Phloem loading: how leaves gain their independence. BioScience 56:15–24
    [Google Scholar]
  130. 130.
    Turgeon R, Wolf S. 2009. Phloem transport: cellular pathways and molecular trafficking. Annu. Rev. Plant Biol. 60:207–21
    [Google Scholar]
  131. 131.
    Vaddepalli P, Herrmann A, Fulton L, Oelschner M, Hillmer S et al. 2014. The C2-domain protein QUIRKY and the receptor-like kinase STRUBBELIG localize to plasmodesmata and mediate tissue morphogenesis in Arabidopsis thaliana. Development 141:4139–48
    [Google Scholar]
  132. 132.
    van Bel AJE. 2003. Phloem, a miracle of ingenuity. Plant Cell Environ 26:125–49
    [Google Scholar]
  133. 133.
    van Bel AJE, Knoblauch M. 2000. Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Funct. Plant Biol. 27:477–87
    [Google Scholar]
  134. 134.
    Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD et al. 2001. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13:385–98
    [Google Scholar]
  135. 135.
    Voitsekhovskaja OV, Rudashevskaya EL, Demchenko KN, Pakhomova MV, Batashev DR et al. 2009. Evidence for functional heterogeneity of sieve element-companion cell complexes in minor vein phloem of Alonsoa meridionalis. J. Exp. Bot. 60:1873–83
    [Google Scholar]
  136. 136.
    Von Schaewen A, Stitt M, Schmidt R, Sonnewald U, Willmitzer L. 1990. 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. EMBO J 9:3033–44
    [Google Scholar]
  137. 137.
    Wang G, Wu Y, Ma L, Lin Y, Hu Y et al. 2021. Phloem loading in rice leaves depends strongly on the apoplastic pathway. J. Exp. Bot. 72:3723–38
    [Google Scholar]
  138. 138.
    Wang L, Lu Q, Wen X, Lu C 2015. Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–62
    [Google Scholar]
  139. 139.
    Warmbrodt RD. 1985. Studies on the root of Hordeum vulgare L.– ultrastructure of the seminal root with special reference to the phloem. Am. J. Bot. 72:414–32
    [Google Scholar]
  140. 140.
    Wei X, Nguyen ST, Collings DA, McCurdy DW 2020. Sucrose regulates wall ingrowth deposition in phloem parenchyma transfer cells in Arabidopsis via affecting phloem loading activity. J. Exp. Bot. 71:4690–702
    [Google Scholar]
  141. 141.
    Weichert N, Saalbach I, Weichert H, Kohl S, Erban A et al. 2010. Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol 152:698–710
    [Google Scholar]
  142. 142.
    Wingenter K, Trentmann O, Winschuh I, Hörmiller II, Heyer AG et al. 2011. A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J 68:890–900
    [Google Scholar]
  143. 143.
    Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J et al. 2006. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476–90
    [Google Scholar]
  144. 144.
    Wright K, Oparka KJ 1996. The fluorescent probe HPTS as a phloem-mobile, symplastic tracer: an evaluation using confocal laser scanning microscopy. J. Exp. Bot. 47:439–45
    [Google Scholar]
  145. 145.
    Wu Y, Lee S-K, Yoo Y, Wei J, Kwon S-Y et al. 2018. Rice transcription factor OsDOF11 modulates sugar transport by promoting expression of Sucrose Transporter and SWEET genes. Mol. Plant 11:833–45
    [Google Scholar]
  146. 146.
    Xu Q, Chen S, Yunjuan R, Chen S, Liesche J 2018. Regulation of sucrose transporters and phloem loading in response to environmental cues. Plant Physiol 176:930–45
    [Google Scholar]
  147. 147.
    Xu Q, Liesche J. 2021. Sugar export from Arabidopsis leaves: actors and regulatory strategies. J. Exp. Bot. 72:5275–84
    [Google Scholar]
  148. 148.
    Xu Q, Yin S, Ma Y, Song M, Song Y et al. 2020. Carbon export from leaves is controlled via ubiquitination and phosphorylation of sucrose transporter SUC2. PNAS 117:6223–30
    [Google Scholar]
  149. 149.
    Xue X, Wang J, Shukla D, Cheung LS, Chen L-Q. 2022. When SWEETs turn tweens: updates and perspectives. Annu. Rev. Plant Biol. 73:379403
    [Google Scholar]
  150. 150.
    Yadav UP, Evers JF, Shaikh MA, Ayre BG. 2021. Cotton phloem loads from the apoplast using a single member of its nine-member sucrose transporter gene family. J. Exp. Bot. 73:84859
    [Google Scholar]
  151. 151.
    Yamada K, Saijo Y, Nakagami H, Takano Y. 2016. Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science 354:1427–30
    [Google Scholar]
  152. 152.
    Zhang C, Han L, Slewinski TL, Sun J, Zhang J et al. 2014. Symplastic phloem loading in poplar. Plant Physiol 166:306–13
    [Google Scholar]
  153. 153.
    Zhang C, Li Y, Wang J, Xue X, Beuchat G, Chen L-Q. 2021. Two evolutionarily duplicated domains individually and post-transcriptionally control SWEET expression for phloem transport. New Phytol 232:1793–807Mapped regulatory sequences controlling phloem parenchyma cell–specific expression of AtSWEET11; determined that proteins binding AtSWEET11 transcript were involved.
    [Google Scholar]
  154. 154.
    Zhang C, Turgeon R. 2018. Mechanisms of phloem loading. Curr. Opin. Plant Biol. 43:71–75
    [Google Scholar]
  155. 155.
    Zhang L, Garneau MG, Majumdar R, Grant J, Tegeder M 2015. Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids. Plant J 81:134–46
    [Google Scholar]
  156. 156.
    Zhou Y, Chan K, Wang TL, Hedley CL, Offler CE, Patrick JW. 2009. Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons. J. Exp. Bot. 60:71–85
    [Google Scholar]
  157. 157.
    Zhu L, Li B, Wu L, Li H, Wang Z et al. 2021. MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato. PNAS 118:e2022788118
    [Google Scholar]
  158. 158.
    Zierer W, Rüscher D, Sonnewald U, Sonnewald S. 2021. Tuber and tuberous root development. Annu. Rev. Plant Biol. 72:551–80
    [Google Scholar]
  159. 159.
    Zimmermann M, Ziegler H. 1975. List of sugars and sugar alcohols in sieve-tube exudates. Encycl. Plant Physiol. 1:480–503
    [Google Scholar]
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