Summary
Mature leaves export approximately 80% of the carbon they fix by photosynthesis. Although most attention has been devoted to studying export of recently synthesized sugar, this is only one source of nutrients that enter the export stream. The mesophyll also supplies amino acids and other chemical species; ions and compounds are rerouted from the xylem, and companion cells have the capacity to reconfigure metabolites as they pass along the sieve tubes. The extent to which each of these channels contributes to the complexity of sieve tube content is not easy to estimate, an analytical problem made especially acute by the difficulty in obtaining authentic phloem sap.
Prior to export, the products of photosynthesis, primarily sucrose and, in some plants, sugar alcohol, must be transferred from mesophyll cells to the phloem. To date, three phloem-loading mechanisms are known. Two are metabolically active in the sense that energy is used to increase the concentration in the phloem relative to the mesophyll. One of these involves sucrose transfer into the apoplast (cell walls) and subsequent transporter-mediated uptake by phloem cells. The second is an oligomerization or “polymer trap” mechanism in which sucrose enters the phloem through plasmodesmata where it is converted to larger sugars that cannot pass back into the mesophyll cells and are thus vectored out of the leaf. The third loading mechanism is also symplastic (through plasmodesmata) but is passive in the sense that it occurs down the concentration gradient. Polymer trap plants also load apoplastically to a lesser degree and it is possible that heterogeneous patterns of loading are more common in plants than presently realized. The adaptive advantages conferred by the three loading mechanisms are not fully understood. One advantage to active loading is that it allows leaves to maintain overall reduced carbohydrate status, thus freeing up fixed carbon for transport to sinks and increasing growth potential. Symplastic loading mechanisms allow compounds in addition to carbohydrates direct access to the phloem without having to traverse the apoplast.
Export from source leaves needs to be regulated consistent with the dynamic needs of storage and sink organs and with environmental conditions that influence hydrostatic pressure gradients throughout the plant. In principle, export can be regulated at every structure along the path, including chloroplasts, tonoplasts, plasma membranes, plasmodesmata, and sieve plate pores. These regulatory steps could involve transporters as well as biochemical interactions in the phloem and/or in the flanking cells along the phloem path. Examples of control at each of these steps have been described. Notwithstanding, how these diverse processes work together to influence resource partitioning on a whole-plant scale is poorly understood. We present such a model based on sucrose concentration and associated turgor pressure.
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Abbreviations
- CC:
-
companion cell
- RFO:
-
raffinose-family oligosaccharide
- SE:
-
sieve element
- Suc:
-
sucrose
- SUT:
-
sucrose uptake transporter
- SWEET:
-
sucrose will eventually be exported transporter
References
Adams WW III, Cohu CM, Amiard V, Demmig-Adams B (2014) Associations between the acclimation of phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate. Front Plant Sci 5:24
Adams WW III, Stewart JJ, Polutchko SK, Demmig-Adams B (2018) Leaf structure, vasculature, and the upper limit of photosynthesis, pp 27–54
Aloni B, Wyse RE, Griffith S (1986) Sucrose transport and phloem unloading in stem of Vicia faba - possible involvement of a sucrose carrier and osmotic regulation. Plant Physiol 81:482–486
Amiard V, Mueh KE, Demmig-Adams B, Ebbert V, Turgeon R, Adams WWIII (2005) Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proc Natl Acad Sci U S A 102:12968–12973
Amiard V, Demmig-Adams B, Mueh KE, Turgeon R, Combs AF, Adams WW III (2007) Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development. New Phytol 173:722–731
Aoki N, Hirose T, Takahashi S, Ono K, Ishimaru K, Ohsugi R (1999) Molecular cloning and expression analysis of a gene for a sucrose transporter in maize (Zea mays L.). Plant Cell Physiol 40:1072–1078
Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232
Atkins CA (2013) Mechanism of long-distance solute transport in phloem elements. In: Sokoloska K, Sowiński P (eds) Symplasmic transport in vascular plants. Springer, New York, pp 165–181
Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394
Baker RF, Braun DM (2008) Tie-dyed2 functions with tie-dyed1 to promote carbohydrate export from maize leaves. Plant Physiol 146:1085–1097
Beebe DU, Evert RF (1992) Photoassimilate pathway(s) and phloem loading in the leaf of Moricandia arvensis (L.) DC. (Brassicaceae). Inter J Plant Sci 153:61–77
Beebe DU, Turgeon R (1992) Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves. Planta 188:354–361
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
Braun DM, Ma Y, Inada N, Muszynski MG, Baker RF (2006) Tie-dyed1 regulates carbohydrate accumulation in maize leaves. Plant Physiol 142:1511–1522
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 65:1713–1735
Bush DR (1993) Proton-coupled sugar and amino acid transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 44:513–542
Cao T, Lahiri I, Singh V, Louis J, Shah J, Ayre BG (2013) Metabolic engineering of raffinose-family oligosaccharides in the phloem reveals alterations in carbon partitioning and enhances resistance to green peach aphid. Front Plant Sci 4:263
Chen L-Q (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155
Chen L-Q, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–534
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 335:207–211
Chen L-Q, Lin IWN, Qu XQ, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619
Chincinska IA, Liesche J, Krügel U, Michalska J, Geigenberger P, Grimm B, Kühn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528
Chiou TJ, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci U S A 95:4784–4788
Cohu CM, Muller O, Adams WW III, Demmig-Adams B (2014) Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals. Physiol Plantarum 152:164–173
Comtet J, Jensen KH, Turgeon R, Stroock AD, Hosoi AE (2017a) Passive phloem loading and long-distance transport in a synthetic tree-on-a-chip. Nature Plants 3: 17032
Comtet J, Turgeon R, Stroock AD (2017b) Phloem loading through plasmodesmata: a biophysical analysis. Plant Physiol 175(2):904–915
Cuellar-Ortiz SM, Arrieta-Montiel MDLP, Acosta-Gallegos J, Covarrubias AA (2008) Relationship between carbohydrate partitioning and drought resistance in common bean. Plant Cell Environ 31:1399–1409
Daie J (1996) Metabolic adjustments, assimilate partitioning, and alterations in source-sink relations in drought-stressed plants. In: Zamski E, Schaffer AA (eds) Photoassimilate distribution in plants and crops: source -sink relationships. Marcel Dekker, New York, pp 407–420
Dasgupta K, Khadilkar AS, Sulpice R, Pant B, Scheible W-R, Fisahn J, Stitt M, Ayre BG (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 165:715–731
Davidson A, Keller F, Turgeon R (2011) Phloem loading, plant growth form, and climate. Protoplasma 248:153–163
De Schepper V, De Swaef T, Bauweraerts I, Steppe K (2013) Phloem transport: a review of mechanisms and controls. J Exp Bot 64:4839–4850
De Storme N, Geelen D (2014) Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front Plant Sci 5:138
Dechadilok P, Deen WM (2006) Hindrance factors for diffusion and convection in pores. Indus Eng Chem Res 45:6953–6959
Dinant S, Kehr J (2013) Sampling and analysis of phloem sap. In: Maathuis FJM (ed) Plant mineral nutrients: methods and protocols. Springer, New York, pp 185–194
Dölger J, Rademaker H, Liesche J, Schulz A, Bohr T (2014) Diffusion and bulk flow in phloem loading: a theoretical analysis of the polymer trap mechanism for sugar transport in plants. Phys Rev E 90:042704
Eom J-S, Choi S-B, Ward JM, Jeon J-S (2012) The mechanism of phloem loading in rice (Oryza sativa). Mol Cells 33:431–438
Eom JS, Chen LQ, Sosso D, Julius BT, Lin IW, Qu XQ, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol 25:53–62
Fisher D (1986) Ultrastructure, plasmodesmatal frequency, and solute concentration in green areas of variegated Coleus blumei Benth. leaves. Planta 169:141–152
Flora LL, Madore MA (1993) Stachyose and mannitol transport in olive (Olea europaea L.). Planta 189:484–490
Fu Q, Cheng L, Guo Y, Turgeon R (2011) Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol 157:1518–1527
Gamalei Y (1989) Structure and function of leaf minor veins in trees and herbs. Trees 3:96–110
Gamalei Y (1991) Phloem loading and its development related to plant evolution from trees to herbs. Trees 5:50–64
Gamalei YV, van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194:443–453
Gao Z, Maurousset L, Lemoine R, Yoo S-D, van Nocker S, Loescher W (2003) Cloning, expression, and characterization of sorbitol transporters from developing sour cherry fruit and leaf sink tissues. Plant Physiol 131:1566–1575
Gaxiola RA, Sanchez CA, Paez-Valencia J, Ayre BG, Elser JJ (2012) Genetic manipulation of a “vacuolar” H+-PPase: from salt tolerance to yield enhancement under phosphorus-deficient soils. Plant Physiol 159:3–11
Geiger DR (1976) Phloem loading in source leaves. In: Wardlaw IF, Passioura JB (eds) Transport and transfer processes in plants. Academic, New York, pp 167–183
Geiger DR, Giaquinta RT, Sovonick SA, Felows RJ (1973) Solute distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol 52:585–589
Giaquinta RT (1977) Phloem loading of sucrose. pH dependence and selectivity. Plant Physiol 59:750–753
Giaquinta RT (1979) Phloem loading of sucrose: involvement of membrane ATPase and proton transport. Plant Physiol 63:744–748
Giaquinta RT (1983) Phloem loading of sucrose. Annu Rev Plant Physiol Plant Mol Biol 34:347–387
Gil L, Yaron I, Shalitin D, Sauer N, Turgeon R, Wolf S (2011) Sucrose transporter plays a role in phloem loading in CMV-infected melon plants that are defined as symplastic loaders. Plant J 66:366–374
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. Proc Natl Acad Sci U S A 97:13979–13984
Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci U S A 107:9458–9463
Grennan AK (2006) Genevestigator. Facilitating web-based gene-expression analysis. Plant Physiol 141:1164–1166
Gunning BES, Pate JS, Briarty LG (1968) Specialized “transfer cells” in minor veins of leaves and their possible significance in phloem translocation. J Cell Biol 37:C7–C12
Hannah MA, Zuther E, Buchel K, Heyer AG (2006) Transport and metabolism of raffinose family oligosaccharides in transgenic potato. J Exp Bot 57:3801–3811
Haritatos E, Turgeon R (1995) Symplastic phloem loading by polymer trapping. In: Pontis H, Salerno G, Echeverria E (eds) Sucrose metabolism, biochemistry, physiology and molecular biology. American Society of Plant Physiologists, Rockville, pp 216–224
Haritatos E, Medville R, Turgeon R (2000a) Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211:105–111
Haritatos E, Ayre BG, Turgeon R (2000b) Identification of phloem involved in assimilate loading in leaves by the activity of the GALACTINOL SYNTHASE promoter. Plant Physiol 123:929–937
Haydon MJ, Bell LJ, Webb AAR (2011) Interactions between plant circadian clocks and solute transport. J Exp Bot 62:2333–2348
Heineke D, Wildenberger K, Sonnewald U, Willmitzer L, Heldt HW (1994) Accumulation of hexoses in leaf vacuoles: studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194:29–33
Hoffmann-Thoma G, van Bel AJE, Ehlers K (2001) Ultrastructure of minor-vein phloem and assimilate export in summer and winter leaves of the symplasmically loading evergreens Ajuga reptans L., Aucuba japonica Thunb., and Hedera helix L. Planta 212:231–242
Holthaus U, Schmitz K (1991) Distribution and immunolocalization of stachyose synthase in Cucumis melo L. Planta 185:479–486
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322
Jensen KH, Lee J, Bohr T, Bruus H (2009) Osmotically driven flows in microchannels separated by a semipermeable membrane. Lab Chip 9:2093–2099
Jensen KH, Lee J, Bohr T, Bruus H, Holbrook NM, Zwieniecki M (2011) Optimality of the Münch mechanism for translocation of sugars in plants. J Royal Soc Interf 8:1155–1165
Jensen KH, Liesche J, Bohr T, Schulz A (2012) Universality of phloem transport in seed plants. Plant Cell Environ 35:1065–1076
Kalttorres W, Kerr PS, Usuda H, Huber SC (1987) Diurnal changes in maize leaf photosynthesis. 1. Carbon exchange-rate, assimilate export rate, and enzyme-activities. Plant Physiol 83:283–288
Kempers R, van Bel AJE (1997) Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201:195–201
Khadilkar AS, Yadav UP, Salazar C, Shulaev V, Paez-Valencia J, Pizzio GA, Gaxiola RA, Ayre BG (2016) Constitutive and companion cell-specific overexpression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport. Plant Physiol 170:401–414
Knoblauch M, Peters W (2010) Münch, morphology, microfluidics-our structural problem with the phloem. Plant Cell Environ 33:1439–1452
Knoblauch M, Peters WS (2013) Long-distance translocation of photosynthates: a primer. Photosynth Res 117:189–196
Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10:35–50
Krügel U, Kühn C (2013) Post-translational regulation of sucrose transporters by direct protein-protein interactions. Front Plant Sci 4:237
Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B, Kühn C (2008) Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification. Plant Cell 20:2497–2513
Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B, Kühn C (2009) Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification (correction). Plant Cell 21:4059–4060
Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300
Liesche J, Schulz A (2012a) Quantification of plant cell coupling with three-dimensional photoactivation microscopy. J Microsc 247:2–9
Liesche J, Schulz A (2012b) In vivo quantification of cell coupling in plants with different phloem-loading strategies. Plant Physiol 159:355–365
Liesche J, Schulz A (2013a) Symplasmic transport in phloem loading and unloading. In: Sokoloska K, Sûwiński P (eds) Symplasmic transport in vascular plants. Springer, New York, pp 133–163
Liesche J, Schulz A (2013b) Modeling the parameters for plasmodesmal sugar filtering in active symplasmic phloem loaders. Front Plant Sci 4:207
Liesche J, He H-X, Grimm B, Schulz A, Kühn C (2010) Recycling of Solanum sucrose transporters expressed in yeast, tobacco, and in mature phloem sieve elements. Mol Plant 3:1064–1074
Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232
Lucas WJ, Groover A, Lichtenberer R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388
McCaskill A, Turgeon R (2007) Phloem loading in Verbascum phoeniceum L. depends on the synthesis of raffinose-family oligosaccharides. Proc Natl Acad Sci U S A 104:19619–19624
McCurdy DW, Hueros G (2014) Transfer cells. Front Plant Sci 5:672
Mitchell DE, Gadus MV, Madore MA (1992) Patterns of assimilate production and translocation in muskmelon (Cucumis melo L.) I. Diurnal patterns. Plant Physiol 99:959–965
Münch E (1930) Die Stoffbewegungen in Der Pflanze. Gustav Fischer, Jena
Nikinmaa E, Sievänen R, Hölttä T (2014) Dynamics of leaf gas exchange, xylem and phloem transport, water potential and carbohydrate concentration in a realistic 3-D model tree crown. Ann Bot 114:653–666
Noiraud N, Maurousset L, Lemoine R (2001) Identification of a mannitol transporter, AgMaT1, in celery phloem. Plant Cell 13:695–705
Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161
Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454
Oparka K, Turgeon R (1999) Sieve elements and companion cells - traffic control centers of the phloem. Plant Cell 11:739–750
Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts L, Pradel KS, Imlau A, Kotlizky G, Sauer N, Epel B (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754
Orlich G, Hofbrückl M, Schulz A (1998) A symplasmic flow of sucrose contributes to phloem loading in Ricinus cotyledons. Planta 206:108–116
Otero S, Helariutta Y, Benitez-Alfonso Y (2016) Symplastic communication in organ formation and tissue patterning. Curr Opin Plant Biol 29:21–28
Pate JS, Gunning BES (1969) Vascular transfer cells in angiosperm leaves. A taxanomic and morphological survey. Protoplasma 68:135–156
Pizzio GA, Paez-Valencia J, Khadilkar AS, Regmi K, Patron-Soberano A, Zhang S, Sanchez-Lares J, Furstenau T, Li J, Sanchez-Gomez C, Valencia-Mayoral P, Yadav UP, Ayre BG, Gaxiola RA (2015) Arabidopsis type I proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiol 167:1541–1553
Regmi KC, Zhang S, Gaxiola RA (2016) Apoplasmic loading in the rice phloem supported by the presence of sucrose synthase and plasma membrane-localized proton pyrophosphatase. Ann Bot 117:257–268
Reidel EJ, Rennie EA, Amiard V, Cheng L, Turgeon R (2009) Phloem loading strategies in three plant species that transport sugar alcohols. Plant Physiol 149:1601–1608
Reinders A, Schulze W, Kühn C, Barker L, Schulz A, Ward JM, Frommer WB (2002) Protein-protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell 14:1567–1577
Reinders A, Sivitz AB, Ward JM (2012) Evolution of plant sucrose uptake transporters. Front Plant Sci 3:22
Rennie E, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proc Natl Acad Sci U S A 106:14162–14167
Riesmeier JW, Hirner B, Frommer WB (1993) Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5:1591–1598
Russin WA, Evert RF (1985) Studies on the leaf of Populus deltoides (Salicaceae): ultrastructure, plasmodesmatal frequency, and solute concentrations. Amer J Bot 72:1232–1247
Russin WA, Evert RF, Vanderveer PJ, Sharkey TD, Briggs SP (1996) Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. Plant Cell 8:645–658
Ryan MG, Asao S (2014) Phloem transport in trees. Tree Physiol 34:1–4
Savage JA, Clearwater MJ, Haines DF, Klein T, Mencuccini M, Sevanto S, Turgeon R, Zhang C (2016) Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology? Plant Cell Environ 39:709–725
Schulz A (2015) Diffusion or bulk flow: how plasmodesmata facilitate pre-phloem transport of assimilates. J Plant Res 128:49–61
Schulze WX, Reinders A, Ward J, Lalonde S, Frommer WB (2003) Interactions between co-expressed Arabidopsis sucrose transporters in the split-ubiquitin system. BMC Biochem 4:3
Shabala S, White RG, Djordjevic MA, Ruan Y-L, Mathesius U (2016) Root-to-shoot signalling: integration of diverse molecules, pathways and functions. Funct Plant Biol 43:87–104
Sivitz AB, Reinders A, Ward JM (2005) Analysis of the transport activity of barley sucrose transporter HvSUT1. Plant Cell Physiol 46:1666–1673
Sjolund RD (1997) The phloem sieve element: a river runs through it. Plant Cell 9:1137–1146
Slewinski TL, Braun DM (2010) The PSYCHEDELIC genes of maize redundantly promote carbohydrate export from leaves. Genetics 185:221–232
Slewinski TL, Baker RF, Stubert A, Braun DM (2012) Tie-dyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves. Plant Physiol 160:1540–1550
Slewinski TL, Zhang C, Turgeon R (2013) Structural and functional heterogeneity in phloem loading and transport. Front Plant Biol 4:244
Smith JAC, Milburn JA (1980) Phloem turgor and the regulation of sucrose loading in Ricinus communis L. Planta 148:42–48
Sosso D, Luo DP, Li QB, Sasse J, Yang JL, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM, Ross-Ibarra J, Yang B, Frommer WB (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47:1489–1493
Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) 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. Plant Physiol 148:200–211
Srivastava AC, Dasgupta K, Ajieren E, Costilla G, McGarry RC, Ayre BG (2009a) Arabidopsis plants harbouring a mutation in AtSUC2, encodoing the predominant sucrose/proton symporter necessay for efficient phloem transport, are able to complete their life cycle and produce viable seed. Ann Bot 104:1121–1128
Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2009b) Effective carbon partitioning driven by exotic phloem-specific regulatory elements fused to the Arabidopsis thaliana AtSUC2 sucrose-proton symporter gene. BMC Plant Biol 9:7
Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M, Feuerstein A, Oparka KJ, Sauer N (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 41:319–331
Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake. Plant J 61:1067–1091
Stroock AD, Pagay VV, Zwieniecki MA, Holbrook NM (2014) The physicochemical hydrodynamics of vascular plants. Annu Rev Fluid Mech 46:615–642
Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155
Sung FJM, Krieg DR (1979) Relative sensitivity of photosynthetic assimilation and translocation of 14Carbon to water stress. Plant Physiol 64:852–856
Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J Exp Bot 65:1865–1878
Thompson MV (2006) Phloem: the long and the short of it. Trends Plant Sci 11:26–32
Truernit E, Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196:564–570
Turgeon R (1984) Termination of nutrient import and development of vein loading capacity in albino tobacco leaves. Plant Physiol 76:45–48
Turgeon R (1996) Phloem loading and plasmodesmata. Trends Plant Sci 1:418–423
Turgeon R (2006) Phloem loading: how leaves gain their independence. Bioscience 56:15–24
Turgeon R (2010a) The role of phloem loading reconsidered. Plant Physiol 152:1817–1823
Turgeon R (2010b) The puzzle of phloem pressure. Plant Physiol 154:578–581
Turgeon R, Gowan E (1990) Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiol 94:1244–1249
Turgeon R, Hepler PK (1989) Symplastic continuity between mesophyll and companion cells in minor veins of mature Cucurbita pepo L. leaves. Planta 179:24–31
Turgeon R, Medville R (1998) The absence of phloem loading in willow leaves. Proc Natl Acad Sci U S A 95:12055–12060
Turgeon R, Medville R (2004) Phloem loading. A reevaluation of the relationship between plasmodesmatal frequencies and loading strategies. Plant Physiol 136:3795–3803
Turgeon R, Medville R (2011) Amborella trichopoda, plasmodesmata, and the evolution of phloem loading. Protoplasma 248:173–180
Turgeon R, Webb J (1973) Leaf development and phloem transport in Cucurbita pepo: transition from import to export. Planta 113:179–191
Turgeon R, Webb JA (1976) Leaf development and phloem trnsport in Cucurbita pepo: maturation of the minor veins. Planta 129:265–269
Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221
Turgeon R, Webb JA, Evert RF (1975) Ultrastructure of minor veins in Cucurbita pepo leaves. Protoplasma 83:217–232
Turgeon R, Beebe DU, Gowan E (1993) The intermediary cell: minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta 191:446–456
Turgeon R, Medville R, Nixon KC (2001) The evolution of minor vein phloem and phloem loading. Am J Bot 88:1331–1339
van Bel AJE (1993) Stategies of phloem loading. Annu Rev Plant Biol Plant Mol Biol 44:253–281
van Bel AJE, Gamalei YV, Ammerlaan A, Bik LP (1992) Dissimilar phloem loading in leaves with symplasmic or apoplasmic minor-vein configurations. Planta 186:518–525
van Bel AJE, Helariutta Y, Thompson GA, Ton J, Dinant S, Ding B, Patrick JW (2013) Phloem: the integrative avenue for resource distribution, signaling, and defense. Front Plant Sci 4:471
Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci U S A 99:10876–10880
Voitsekhovskaja OV, Koroleva OA, Batashev DR, Knop C, Tomos AD, Gamalei YV, Heldt H-W, Lohaus G (2006) Phloem loading in two Scrophulariaceae species. What can drive symplastic flow via plasmodesmata? Plant Physiol 140:383–395
Voitsekhovskaja OV, Rudashevskaya EL, Demchenko KN, Pakhomova MV, Batashev DR, Gamalei YV, Lohaus G, Pawlowski K (2009) Evidence for functional heterogeneity of sieve element-companion cell complexes in minor vein phloem of Alonsoa meridionalis. J Exp Bot 60:1873–1883
Volk GM, Turgeon R, Beebe DU (1996) Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta 199:425–432
Volk GM, Haritatos EE, Turgeon R (2003) Galactinol synthase gene expression in melon. J Am Soc Hortic Sci 128:8–15
Weisberg LA, Wimmers LE, Turgeon R (1988) Photoassimilate-transport characteristics of nonchlorophyllous and green tissue in variegated leaves of Coleus blumei Benth. Planta 175:1–8
Wimmers LE, Turgeon R (1991) Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta 186:2–12
Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O, Hoermiller II, Heyer AG, Marten I, Hedrich R, Neuhaus HE (2010) Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield in Arabidopsis. Plant Physiol 154:665–677
Winter H, Lohaus G, Heldt HW (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996–1004
Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191:180–190
Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193:530–535
Wippel K, Sauer N (2012) Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter. J Exp Bot 63:669–679
Wright KM, Roberts AG, Martens HJ, Sauer N, Oparka KJ (2003) Structural and functional vein maturation in developing tobacco leaves in relation to AtSUC2 promoter activity. Plant Physiol 131:1555–1565
Yadav UP, Ayre BG, Bush DR (2015) Transgenic approaches to altering carbon and nitrogen partitioning in whole plants: assessing the potential to improve crop yields and nutritional quality. Front Plant Sci 6:275
Yamaji N, Ma JF (2014) The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci 19:556–563
Zhang C, Turgeon R (2009) Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading. Proc Natl Acad Sci U S A 106:18849–18854
Zhang W-H, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Nutrient loading of developing seeds. Funct Plant Biol 34:314–331
Zhang C, Han L, Slewinski TL, Sun J, Zhang J, Wang Z-Y, Turgeon R (2014) Symplastic phloem loading in poplar. Plant Physiol 166:306–313
Zhou YC, 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
Zimmermann MH (1957) Translocation of organic substances in trees. II. On the translocation mechanism in the phloem of white ash (Fraxinus americana L.). Plant Physiol 32:399–404
Acknowledgments
This work was supported by the National Science Foundation – Integrative Organismal Systems grant 1354718 to R.T. and grant 1558012 to B.G.A.
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Ayre, B.G., Turgeon, R. (2018). Export of Photosynthates from the Leaf. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_3
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