The Molecular Mechanism of Long-distance Sugar Transport in Plants

doi:10.3724/SP.J.1259.2015.00107

Abstract

Abstract: Abstract Plants use CO₂ to synthesize carbohydrates in plant leaves, sheaths and green stems during photosynthesis. After long-distance transport, carbohydrates are consumed or stored in sink tissues such as developing tissues, pollen and fruits. Sucrose is the main type of long-distance-transported carbohydrate in higher plants. Transport of sucrose from the source to sink includes phloem loading in the source tissues, transport in vascular bundles, and phloem unloading in sink tissues. Genetics and molecular biology experiments showed that sucrose transporters, invertases and monosaccharide transporters play an important role in loading and unloading carbohydrates. We review the current literatures on carbohydrate transport and the molecular mechanisms of regulating transport.

Yi Zhang, Dabing Zhang, Man Liu. The Molecular Mechanism of Long-distance Sugar Transport in Plants[J]. Chinese Bulletin of Botany, 2015, 50(1): 107-121.

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References 123

1	夏国海, 张大鹏 (2000). 葡萄果肉同化物卸载区细胞间的共质体联系与隔离. 植物学报 42, 898-904.
2	张大鹏, 李珉, 王毅 (1997). 葡萄果实发育过程中果肉细胞超微结构的观察. 植物学报 39, 389-396.
3	Andriunas FA, Zhang HM, Xia X, Patrick JW, Offler CE (2013). Intersection of transfer cells with phloem biology- broad evolutionary trends, function, and induction. Front Plant Sci 4, 221.
4	Antony G, Zhou JH, Huang S, Li T, Liu B, White F, Yang B (2010). Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3.Plant Cell 22, 3864-3876.
5	Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003). The sucrose transporter gene family in rice.Plant Cell Physiol 44, 223-232.
6	Barth I, Meyer S, Sauer N (2003). PmSUC3: characteriza- tion of a SUT2/SUC3-type sucrose transporter from Plantago major.Plant Cell 15, 1375-1385.
7	Batashev DR, Pakhomova MV, Razumovskaya AV, Voitsekhovskaja OV, Gamalei YV (2013). Cytology of the minor-vein phloem in 320 species from the subclass Asteridae suggests a high diversity of phloem-loading modes.Front Plant Sci 4, 312.
8	Baud S, Wuillème S, Lemoine R, Kronenberger J, Caboche M, Lepiniec L, Rochat C (2005). The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis.Plant J 43, 824-836.
9	Boorer KJ, Loo DDF, Wright EM (1994). Steady-state and presteady-state kinetics of the H+/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes.J Biol Chem 269, 20417-20424.
10	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.
11	Büttner M (2007). The monosaccharide transporter(-like) gene family in Arabidopsis.FEBS Lett 581, 2318-2324.
12	Büttner M (2010). The Arabidopsis sugar transporter (AtSTP) family: an update.Plant Biol 12(Suppl 1), 35-41.
13	Büttner M, Truernit E, Baier K, Scholz-Starke J, Sontheim M, Lauterbach C, Huss VAR, Sauer N (2000). AtSTP3, a green leaf-speciﬁc, low affinity mono- saccharide-H+ symporter of Arabidopsis thaliana.Plant Cell Environ 23, 175-184.
14	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, 21437-21443.
15	Chandran D, Reinders A, Ward JM (2003). Substrate specificity of the Arabidopsis thaliana sucrose transporter AtSUC2.J Biol Chem 278, 44320-44325.
16	Chen LQ (2014). SWEET sugar transporters for phloem transport and pathogen nutrition.New Phytol 201, 1150-1155.
17	Chen LQ, 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, 527-532.
18	Chen LQ, Qu XQ, Hou BH, 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.
19	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.
20	Clement C, Burrus M, Audran JC (1996). Floral organ growth and carbohydrate content during pollen development in Lilium.Am J Bot 83, 459-469.
21	Davidson A, Keller F, Turgeon R (2011). Phloem loading, plant growth form, and climate.Protoplasma 248, 153-163.
22	Dinant S, Lemoine R (2010). The phloem pathway: new issues and old debates.C R Biol 333, 307-319.
23	Ding B, Parthasarathy MV, Niklas K, Turgeon R (1988). A morphometric analysis of the phloem-unloading pathway in developing tobacco leaves. Planta 176, 307-318.
24	Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG (2006). Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach.Plant Physiol 141, 196-207.
25	Eom JS, Cho JI, Reinders A, Lee SW, Yoo Y, Tuan PQ, Choi SB, Bang G, Park YI, Cho MH, Bhoo SH, An G, Hahn TR, Ward JM, Jeon JS (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, 109-119.
26	Eom JS, Choi SB, Ward JM, Jeon JS (2012). The mechanism of phloem loading in rice (Oryza sativa).Mol Cells 33, 431-438.
27	Fan RC, Peng CC, Xu YH, Wang XF, Li Y, Shang Y, Du SY, Zhao R, Zhang XY, Zhang LY, Zhang DP (2009). Apple sucrose transporter SUT1 and sorbitol transporter SOT6 interact with cytochrome b5 to regulate their affinity for substrate sugars.Plant Physiol 150, 1880-1901.
28	Feuerstein A, Niedermeier M, Bauer K, Engelmann S, Hoth S, Stadler R, Sauer N (2010). Expression of the AtSUC1 gene in the female gametophyte, and ecotype- specific expression differences in male reproductive organs. Plant Biol 12(Suppl 1), 105-114.
29	Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003). The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum.Plant Physiol 132, 821-829.
30	Gamalei Y (1989). Structure and function of leaf minor veins in trees and herbs.Trees 3, 96-110.
31	Garchery C, Gest N, Do PT, Alhagdow M, Baldet P, Menard G, Rothan C, Massot C, Gautier H, Aarrouf J, Fernie AR, Stevens R (2013). A diminution in ascorbate oxidase activity affects carbon allocation and improves yield in tomato under water deficit.Plant Cell Environ 36, 159-175.
32	Giaquinta RT, Lin W, Sadler NL, Franceschi VR (1983). Pathway of phloem unloading of sucrose in corn roots.Plant Physiol 72, 362-367.
33	Godt DE, Roitsch T (1997). Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism.Plant Physiol 115, 273-282.
34	Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001). Induction of male sterility in plants by metabolic engineering of the carbohydrate supply.Proc Natl Acad Sci USA 98, 6522-6527.
35	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 USA 97, 13979-13984.
36	Haupt S, Duncan GH, Holzberg S, Oparka KJ (2001). Evidence for symplastic phloem unloading in sink leaves of barley.Plant Physiol 125, 209-218.
37	Hirose T, Zhang ZJ, 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, 3639-3646.
38	Hofmann J, Wieczorek K, Blöchl A, Grundler FMW (2007). Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways.J Exp Bot 58, 1591-1601.
39	Ibraheem O, Botha CE, Bradley G, Dealtry G, Roux S (2014). Rice sucrose transporter1 (OsSUT1) up-regula- tion in xylem parenchyma is caused by aphid feeding on rice leaf blade vascular bundles.Plant Biol 16, 783-791.
40	Juergensen K, Scholz-Starke J, Sauer N, Hess P, van Bel AJE, Grundler FMW (2003). The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia.Plant Physiol 131, 61-69.
41	Kocal N, Sonnewald U, Sonnewald S (2008). Cell wall- bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148, 1523-1536.
42	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.
43	Kühn C, Barker L, Bürkle L, Frommer WB (1999). Update on sucrose transport in higher plants. J Exp Bot 50, 935-953.
44	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.
45	Kühn C, Grof CPL (2010). Sucrose transporters of higher plants.Curr Opin Plant Biol 13, 288-298.
46	Kühn C, Hajirezaei MR, Fernie AR, Roessner-Tunali U, Czechowski T, Hirner B, Frommer WB (2003). The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development.Plant Physiol 131, 102-113.
47	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.
48	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, 341-372.
49	Lin W, Schmitt MR, Hitz WD, Giaquinta RT (1984). Sugar transport in isolated corn root protoplasts.Plant Physiol 76, 894-897.
50	Lu C, Tej SS, Luo SJ, Haudenschild CD, Meyers BC, Green PJ (2005). Elucidation of the small RNA com- ponent of the transcriptome.Science 309, 1567-1569.
51	Maddison AL, Hedley PE, Meyer RC, Aziz N, Davidson D, Machray GC (1999). Expression of tandem invertase genes associated with sexual and vegetative growth cycles in potato. Plant Mol Biol 41, 741-751.
52	Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG (2006). Effects of chilling on male gametophyte develop- ment in rice.Cell Biol Int 30, 583-591.
53	McCaskill A, Turgeon R (2007). Phloem loading in Verbascum phoeniceum L. depends on the synthesis of raffinose-family oligosaccharides.Proc Natl Acad Sci USA 104, 19619-19624.
54	Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004). Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues.Plant Physiol 134, 684-693.
55	Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck R, Stadler R, Sauer N (2000). AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer.Plant J 24, 869-882.
56	Miller ME, Chourey PS (1992). The maize invertase- deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4, 297-305.
57	Miyazaki M, Araki M, Okamura K, Ishibashi Y, Yuasa T, Iwaya-Inoue M (2013). Assimilate translocation and expression of sucrose transporter, OsSUT1, contribute to high-performance ripening under heat stress in the heat-tolerant rice cultivar Genkitsukushi. J Plant Physiol 170, 1579-1584.
58	Ngampanya B, Sobolewska A, Takeda T, Toyofuku K, Narangajavana J, Ikeda A, Yamaguchi J (2003). Characterization of rice functional monosaccharide trans- porter, OsMST5.Biosci Biotechnol Biochem 67, 556-562.
59	Niittylä T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX (2007). Temporal analysis of sucrose- induced phosphorylation changes in plasma membrane proteins of Arabidopsis.Mol Cell Proteomics 6, 1711-1726.
60	Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2013). Assimilate transport in phloem sets conditions for leaf gas exchange.Plant Cell Environ 36, 655-669.
61	Norholm MHH, Nour-Eldin HH, Brodersen P, Mundy J, Halkier BA (2006). Expression of the Arabidopsis high-affinity hexose transporter STP13 correlates with programmed cell death.FEBS Lett 580, 2381-2387.
62	Nour-Eldin HH, Nørholm MH, Halkier BA (2006). Screening for plant transporter function by expressing a normalized Arabidopsis full-length cDNA library in Xenopus oocytes.Plant Methods 2, 17-25.
63	Nühse TS, Stensballe A, Jensen ON, Peck SC (2004). Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database.Plant Cell 16, 2394-2405.
64	Oliver SN, Dennis ES, Dolferus R (2007). ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48, 1319-1330.
65	Oparka KJ, Duckett CM, Prior DAM, Fisher DB (1994). Real-time imaging of phloem unloading in the root tip of Arabidopsis.Plant J 6, 759-766.
66	Pate JS, Gunning BES (1969). Vascular transfer cells in angiosperm leaves—a taxonomic and morphological survey.Protoplasma 68, 135-156.
67	Patrick JW (1997). Phloem unloading: sieve element unloading and post-sieve element transport.Annu Rev Plant Physiol Plant Mol Biol 48, 191-222.
68	Patrick JW (2013). Does Don Fisher's high-pressure manifold model account for phloem transport and resource partitioning?Front Plant Sci 4, 184.
69	Patrick JW, Botha FC, Birch RG (2013). Metabolic engineering of sugars and simple sugar derivatives in plants.Plant Biotechnol J 11, 142-156.
70	Patrick JW, Offler CE (1995). Post-sieve element transport of sucrose in developing seeds. Aust J Plant Physiol 22, 681-702.
71	Patrick JW, Offler CE (1996). Post-sieve element transport of photoassimilates in sink regions.J Exp Bot 47, 1165-1177.
72	Pomper KW, Breen PJ (1995). Levels of apoplastic solutes in developing strawberry fruit.J Exp Bot 46, 743-752.
73	Poschet G, Hannich B, Buttner M (2010). Identification and characterization of AtSTP14, a novel galactose trans- porter from Arabidopsis.Plant Cell Physiol 51, 1571-1580.
74	Reidel EJ, Rennie EA, Amiard V, Cheng LL, Turgeon R (2009). Phloem loading strategies in three plant species that transport sugar alcohols.Plant Physiol 149, 1601-1608.
75	Reinders A, Schulze W, Kühn C, Barker L, Schulz A, Ward JM, Frommer WB (2002). Protein-protein inter- actions between sucrose transporters of different affinities colocalized in the same enucleate sieve element.Plant Cell 14, 1567-1577.
76	Rennie EA, Turgeon R (2009). A comprehensive picture of phloem loading strategies.Proc Natl Acad Sci USA 106, 14162-14167.
77	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.
78	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, 4705-4713.
79	Roblin G, Sakr S, Bonmort J, Delrot S (1998). Regulation of a plant plasma membrane sucrose transporter by phosphorylation.FEBS Lett 424, 165-168.
80	Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010). Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat.Mol Plant 3, 942-955.
81	Ruan YL, Patrick JW (1995). The cellular pathway of post- phloem sugar transport in developing tomato fruit.Planta 196, 434-444.
82	Sauer N, Friedländer K, Gräml-Wicke U (1990). Primary structure, genomic organization and .1990bdländer K.heterologous ex- pression of a glucose transporter from Arabidopsis thaliana.EMBO J 9, 3045-3050.
83	Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M, Klebl F (2004). AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. Plant J 40, 120-130.
84	Schmalstig JG, Geiger DR (1985). Phloem unloading in developing leaves of sugar beet. I. Evidence for pathway through the symplast. Plant Physiol 79, 237-241.
85	Schneider S, Hulpke S, Schulz A, Yaron I, Höll J, Imlau A, Schmitt B, Batz S, Wolf S, Hedrich R, Sauer N (2012). Vacuoles release sucrose via tonoplast-localised SUC4- type transporters.Plant Biol 14, 325-336.
86	Schneidereit A, Scholz-Starke J, Büttner M (2003). Functional characterization and expression analyses of the glucose-specific AtSTP9 monosaccharide transporter in pollen of Arabidopsis.Plant Physiol 133, 182-190.
87	Schneidereit A, Scholz-Starke J, Sauer N, Büttner M (2005). AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis.Planta 221, 48-55.
88	Scholz-Starke J, Büttner M, Sauer N (2003). AtSTP6, a new pollen-specific H+-monosaccharide symporter from Arabidopsis.Plant Physiol 131, 70-77.
89	Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, Poschet G, Büttner M, Schneider S, Sauer N, Hedrich R (2011). Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2.Plant J 68, 129-136.
90	Schulze W, Weise A, Frommer WB, Ward JM (2000). Function of the cytosolic N-terminus of sucrose trans- porter AtSUT2 in substrate affinity.FEBS Lett 485, 189-194.
91	Scofield GN, Aoki N, Hirose T, Takano M, Jenkins CLD, Furbank RT (2007a). The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants.J Exp Bot 58, 483-495.
92	Scofield GN, Hirose T, Aoki N, Furbank RT (2007b). Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice.J Exp Bot 58, 3155-3169.
93	Sherson SM, Hemmann G, Wallace G, Forbes S, Germain V, Stadler R, Bechtold N, Sauer N, Smith SM (2000). Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J 24, 849-857.
94	Sivitz AB, Reinders A, Johnson ME, Krentz AD, Grof CPL, Perroux JM, Ward JM (2007). Arabidopsis sucrose transporter AtSUC9. High-affinity transport activity, intra- genic control of expression, and early flowering mutant phenotype.Plant Physiol 143, 188-198.
95	Sivitz AB, Reinders A, Ward JM (2008). Arabidopsis sucrose transporter AtSUC1 is important for pollen germi- nation and sucrose-induced anthocyanin accumulation. Plant Physiol 147, 92-100.
96	Sonnewald U, Hajirezaei MR, Kossmann J, Heyer A, Trethewey RN, Willmitzer L (1997). Increased potato tuber size resulting from apoplastic expression of a yeast invertase.Nat Biotechnol 15, 794-797.
97	Srivastava AC, Dasgupta K, Ajieren E, Costilla G, McGarry RC, Ayre BG (2009). Arabidopsis plants har- bouring 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, 1121-1128.
98	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.
99	Stadler R, Büttner M, Ache P, Hedrich R, Ivashikina N, Melzer M, Shearson SM, Smith SM, Sauer N (2003). Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis.Plant Physiol 133, 528-537.
100	Stadler R, Truernit E, Gahrtz M, Sauer N (1999). The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis.Plant J 19, 269-278.
101	Sturm A, Chrispeels MJ (1990). cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection.Plant Cell 2, 1107-1119.
102	Sturm A, Tang GQ (1999). The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning.Trends Plant Sci 4, 401-407.
103	Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996). The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a mono- saccharide transporter by wounding, elicitors, and patho- gen challenge.Plant Cell 8, 2169-2182.
104	Truernit E, Stadler R, Baier K, Sauer N (1999). A male gametophyte-specific monosaccharide transporter in Ara- bidopsis.Plant J 17, 191-201.
105	Turgeon R (2010). The role of phloem loading reconsidered. Plant Physiol 152, 1817-1823.
106	Tymowska-Lalanne Z, Kreis M (1998). Expression of the Arabidopsis thaliana invertase gene family.Planta 207, 259-265.
107	van Bel AJE (1993). Strategies of phloem loading.Annu Rev Plant Physiol Plant Mol Biol 44, 253-281.
108	van Bel AJE (1996). Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with asso- ciated physiological software packages in dicotyledons.J Exp Bot 47, 1129-1140.
109	van Bel AJE, Knoblauch M (1987). Phloem unloading in tobacco sink leaves insensitivity to anoxia indicates a symplastic pathway.Planta 171, 73-81.
110	van Bel AJE, Knoblauch M (2000). Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse.Aust J Plant Physiol 27, 477-487.
111	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.
112	Wang ET, Wang JJ, Zhu XD, Hao W, Wang LY, Li Q, Zhang LX, He W, Lu BR, Lin HX, Ma H, Zhang GQ, He ZH (2008a). Control of rice grain-filling and yield by a gene with a potential signature of domestication.Nat Genet 40, 1370-1374.
113	Wang RK, Cao ZH, Hao YJ (2014). Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples.Physiol Plant 150, 76-87.
114	Wang YQ, Xiao YG, Zhang Y, Chai CL, Wei G, Wei XL, Xu HL, Wang M, Ouwerkerk PBF, Zhu Z (2008b). Molecular cloning, functional characterization and expression analysis of a novel monosaccharide transporter gene OsMST6 from rice (Oryza sativa L.).Planta 228, 525-535.
115	Wang YQ, Xu HL, Wei XL, Chai CL, Xiao YG, Zhang Y, Chen B, Xiao GF, Ouwerkerk PBF, Wang M, Zhu Z (2007). Molecular cloning and expression analysis of a monosaccharide transporter gene OsMST4 from rice (Oryza sativa L.).Plant Mol Biol 65, 439-451.
116	Werner T, Holst K, Pörs Y, Guivarc'h A, Mustroph A, Chriqui D, Grimm B, Schmülling T (2008). Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots.J Exp Bot 59, 2659-2672.
117	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 mono- saccharide transporter TMT1 alters cellular sugar par- titioning, sugar signaling, and seed yield in Arabidopsis.Plant Physiol 154, 665-677.
118	Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006). Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18, 3476-3490.
119	Wu GL, Zhang XY, Zhang LY, Pan QH, Shen YY, Zhang DP (2004). Phloem unloading in developing walnut fruit is symplasmic in the seed pericarp and apoplasmic in the fleshy pericarp.Plant Cell Physiol 45, 1461-1470.
120	Yuan M, Zhao JW, Huang RY, Li XH, Xiao JH, Wang SP (2014). Rice MtN3/saliva/SWEET gene family: evolution, expression profiling, and sugar transport.J Integr Plant Biol 56, 559-570.
121	Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpice R, Zhou YH, Fernie AR (2009). RNA inter- ference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the impor- tance of sucrose cleavage for normal fruit development and fertility.Plant Physiol 150, 1204-1218.
122	Zhang CK, Turgeon R (2009). Downregulating the sucrose transporter VpSUT1 in verbascum phoeniceum does not inhibit phloem loading.Proc Natl Acad Sci USA 106, 18849-18854.
123	Zhou YC, Qu HX, Dibley KE, Offler CE, Patrick JW (2007). A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators.Plant J 49, 750-764.

物种	基因	表达部位	功能
玉米 Zea mays	ZmSUT1	成熟叶片、叶鞘、花梗、种子	将源中的蔗糖运输进韧皮部, 再将韧皮部蔗糖卸载到库(Carpaneto et al., 2005)
	ZmSUT2-6	未知	未知
拟南芥 Arabidopsis thaliana	AtSUC1	花粉管质膜、根	介导幼苗中蔗糖诱导的花青素积累; 参与花粉管发育过程中对蔗糖的吸收(Stadler et al., 1999; Sivitz et al., 2008; Feuerstein et al., 2010)
	AtSUC2	韧皮部伴胞	第1个被发现的由病原菌激活的二糖转运蛋白, 可以吸收韧皮部运输中泄漏的蔗糖(Chandran et al., 2003; Juer- gensen et al., 2003; Srivastava et al., 2008, 2009)
	AtSUC3	库细胞: 保卫细胞、根尖、托叶、毛状体、花粉粒、花粉管	为正在发育的心皮运输蔗糖, 可向植物受伤部位运输蔗糖, 促进植物恢复, 或者从受伤部位移去蔗糖避免感染(Meyer et al., 2000, 2004)
	AtSUC4	合胞体(syncytia)、感染区域附近的根、叶肉细胞液泡膜	为分化早期的合胞体运输蔗糖, 从液泡向外运输蔗糖(Hofmann et al., 2007; Schulz et al., 2011; Schneider et al., 2012)
	AtSUC5	胚乳	参与种子发育早期的蔗糖运输(Baud et al., 2005)
	AtSUC6, 7	假基因(Sauer et al., 2004)
	AtSUC8	珠柄、花柱引导组织	未知(Sauer et al., 2004)
	AtSUC9	库细胞质膜	通过保持细胞间低浓度的蔗糖防止早花(Sivitz et al., 2007)
	AtSWEET10, 13, 14, 15	未知	未知
	AtSWEET11, 12	韧皮部薄壁细胞质膜	将蔗糖从韧皮部薄壁细胞运出(Chen et al., 2012)
水稻 Oryza sativa	OsSUT1	内子叶伴胞、筛管、胚芽鞘	从胚芽鞘、第1、2片真叶中的质外体回收泄露的蔗糖(Scofield et al., 2007a, 2007b; Ibraheem et al., 2014)
	OsSUT2	叶肉细胞、新生侧根、受精颖花花梗、种皮横细胞层液泡膜上	将蔗糖从液泡内运输到胞质(Eom et al., 2011)
	OsSUT3	花粉	参与花粉发育过程中淀粉的积累过程(Hirose et al., 2010)
	OsSUT4	叶、叶鞘、根、小穗(Aoki et al., 2003)	未知
	OsSUT5	同OsSUT4(Aoki et al., 2003)	未知
	OsSWEET14	未知	在293T细胞中表达能运输蔗糖(Chen et al., 2012)
	OsSWEET14	未知	参与蔗糖到种子的运输(Antony et al., 2010; Yuan et al., 2014)

物种	基因	表达部位	功能
玉米 Zea mays	ZmSUT1	成熟叶片、叶鞘、花梗、种子	将源中的蔗糖运输进韧皮部, 再将韧皮部蔗糖卸载到库(Carpaneto et al., 2005)
	ZmSUT2-6	未知	未知
拟南芥 Arabidopsis thaliana	AtSUC1	花粉管质膜、根	介导幼苗中蔗糖诱导的花青素积累; 参与花粉管发育过程中对蔗糖的吸收(Stadler et al., 1999; Sivitz et al., 2008; Feuerstein et al., 2010)
	AtSUC2	韧皮部伴胞	第1个被发现的由病原菌激活的二糖转运蛋白, 可以吸收韧皮部运输中泄漏的蔗糖(Chandran et al., 2003; Juer- gensen et al., 2003; Srivastava et al., 2008, 2009)
	AtSUC3	库细胞: 保卫细胞、根尖、托叶、毛状体、花粉粒、花粉管	为正在发育的心皮运输蔗糖, 可向植物受伤部位运输蔗糖, 促进植物恢复, 或者从受伤部位移去蔗糖避免感染(Meyer et al., 2000, 2004)
	AtSUC4	合胞体(syncytia)、感染区域附近的根、叶肉细胞液泡膜	为分化早期的合胞体运输蔗糖, 从液泡向外运输蔗糖(Hofmann et al., 2007; Schulz et al., 2011; Schneider et al., 2012)
	AtSUC5	胚乳	参与种子发育早期的蔗糖运输(Baud et al., 2005)
	AtSUC6, 7	假基因(Sauer et al., 2004)
	AtSUC8	珠柄、花柱引导组织	未知(Sauer et al., 2004)
	AtSUC9	库细胞质膜	通过保持细胞间低浓度的蔗糖防止早花(Sivitz et al., 2007)
	AtSWEET10, 13, 14, 15	未知	未知
	AtSWEET11, 12	韧皮部薄壁细胞质膜	将蔗糖从韧皮部薄壁细胞运出(Chen et al., 2012)
水稻 Oryza sativa	OsSUT1	内子叶伴胞、筛管、胚芽鞘	从胚芽鞘、第1、2片真叶中的质外体回收泄露的蔗糖(Scofield et al., 2007a, 2007b; Ibraheem et al., 2014)
	OsSUT2	叶肉细胞、新生侧根、受精颖花花梗、种皮横细胞层液泡膜上	将蔗糖从液泡内运输到胞质(Eom et al., 2011)
	OsSUT3	花粉	参与花粉发育过程中淀粉的积累过程(Hirose et al., 2010)
	OsSUT4	叶、叶鞘、根、小穗(Aoki et al., 2003)	未知
	OsSUT5	同OsSUT4(Aoki et al., 2003)	未知
	OsSWEET14	未知	在293T细胞中表达能运输蔗糖(Chen et al., 2012)
	OsSWEET14	未知	参与蔗糖到种子的运输(Antony et al., 2010; Yuan et al., 2014)

物种	基因	表达部位	功能
拟南芥 Arabidopsis thaliana	AtSTP1	子叶保卫细胞、莲座叶、萼片、子房、茎	吸收胚和幼苗细胞间的单糖; 晚上可将单糖运输进保卫细胞, 白天调控渗透势(Sherson et al., 2000; Stadler et al., 2003)
	AtSTP2	发育和成熟的花粉粒	吸收胼胝质降解产生的葡萄糖(Davidson et al., 2011)
	AtSTP3	子叶、莲座叶、叶茎、萼片(Büttner et al., 2000)	未知
	AtSTP4	根、白粉菌(Erysipheci choracearum)感染后的成熟叶维管组织	将更多的葡萄糖运输进感染区附近的叶片参与植物防御(Fotopoulos et al., 2003)
	AtSTP5, 7	未知	在酿酒酵母中表达对常见的糖类无转运活性(Büttner, 2010)
	AtSTP6	花药发育11、12期及之后的花粉粒	可能参与花粉成熟及花粉管发育过程(Scholz-Starke et al., 2003)
	AtSTP8, 10, 12	未知	未知
	AtSTP9, AtSTP11	花粉粒、花粉管	将单糖运输进发育中的花粉粒或花粉管(Schneid- ereit et al., 2003, 2005)
	AtSTP13	新生花瓣维管组织	参与细胞程序性死亡(programmed cell death, PCD)(Norholm et al., 2006; Nour-Eldin et al., 2006)
	AtSTP14	胚乳、子叶、莲座叶、根尖	参与细胞壁产生的半乳糖循环(Poschet et al., 2010)
	TMT1	蛋白定位于液泡膜	将单糖运输进液泡, 响应胁迫, 参与拟南芥的生长发育(Wormit et al., 2006; Wingenter et al., 2010)
	TMT2	根、茎(Wormit et al., 2006)	未知
	TMT3	蛋白定位于液泡膜(Wormit et al., 2006)	未知
水稻	OsMST1, 2, 3, 7	未知	未知
Oryza sativa	OsMST4	叶鞘、茎尖、根	参与种子发育过程中单糖的运输(Wang et al., 2007)
	OsMST5	授粉前的小穗	参与花粉发育(Ngampanya et al., 2003)
	OsMST6	种子发育早期的胚乳、横细胞、维管束薄壁细胞	参与种子发育过程(Wang et al., 2008b)
	OsMST8	绒毡层、小孢子、维管束	将胼胝质降解产生的葡萄糖运输到绒毡层和小孢子(Mamun et al., 2006)

物种	基因	表达部位	功能
拟南芥 Arabidopsis thaliana	AtSTP1	子叶保卫细胞、莲座叶、萼片、子房、茎	吸收胚和幼苗细胞间的单糖; 晚上可将单糖运输进保卫细胞, 白天调控渗透势(Sherson et al., 2000; Stadler et al., 2003)
	AtSTP2	发育和成熟的花粉粒	吸收胼胝质降解产生的葡萄糖(Davidson et al., 2011)
	AtSTP3	子叶、莲座叶、叶茎、萼片(Büttner et al., 2000)	未知
	AtSTP4	根、白粉菌(Erysipheci choracearum)感染后的成熟叶维管组织	将更多的葡萄糖运输进感染区附近的叶片参与植物防御(Fotopoulos et al., 2003)
	AtSTP5, 7	未知	在酿酒酵母中表达对常见的糖类无转运活性(Büttner, 2010)
	AtSTP6	花药发育11、12期及之后的花粉粒	可能参与花粉成熟及花粉管发育过程(Scholz-Starke et al., 2003)
	AtSTP8, 10, 12	未知	未知
	AtSTP9, AtSTP11	花粉粒、花粉管	将单糖运输进发育中的花粉粒或花粉管(Schneid- ereit et al., 2003, 2005)
	AtSTP13	新生花瓣维管组织	参与细胞程序性死亡(programmed cell death, PCD)(Norholm et al., 2006; Nour-Eldin et al., 2006)
	AtSTP14	胚乳、子叶、莲座叶、根尖	参与细胞壁产生的半乳糖循环(Poschet et al., 2010)
	TMT1	蛋白定位于液泡膜	将单糖运输进液泡, 响应胁迫, 参与拟南芥的生长发育(Wormit et al., 2006; Wingenter et al., 2010)
	TMT2	根、茎(Wormit et al., 2006)	未知
	TMT3	蛋白定位于液泡膜(Wormit et al., 2006)	未知
水稻	OsMST1, 2, 3, 7	未知	未知
Oryza sativa	OsMST4	叶鞘、茎尖、根	参与种子发育过程中单糖的运输(Wang et al., 2007)
	OsMST5	授粉前的小穗	参与花粉发育(Ngampanya et al., 2003)
	OsMST6	种子发育早期的胚乳、横细胞、维管束薄壁细胞	参与种子发育过程(Wang et al., 2008b)
	OsMST8	绒毡层、小孢子、维管束	将胼胝质降解产生的葡萄糖运输到绒毡层和小孢子(Mamun et al., 2006)