Phloem pp 267-287 | Cite as

The AtSUC2 Promoter: A Powerful Tool to Study Phloem Physiology and Development

  • Ruth StadlerEmail author
  • Norbert Sauer
Part of the Methods in Molecular Biology book series (MIMB, volume 2014)


The sucrose carrier AtSUC2 of Arabidopsis thaliana is localized in the phloem, where it catalyzes the uptake of sucrose from the apoplast into companion cells. Imported sucrose moves passively via plasmodesmata from the companion cells into the neighboring sieve elements that distribute this disaccharide to the different sink organs. Phloem loading of sucrose by the AtSUC2 protein is an essential process, and mutants lacking this protein stay tiny, develop no or only few flowers, and have a strongly reduced root system. The promoter of the AtSUC2 gene is active exclusively in companion cells of the phloem. Moreover, it drives very strong expression not only in Arabidopsis, but also in all plant species tested so far, including monocot species. Due to these features, the AtSUC2 promoter has become an important tool in diverse areas of plant research during the last two decades. It was used to study phloem development and function including phloem loading and unloading. Furthermore, it was helpful in analyzing the pathways of posttranscriptional silencing by RNA interference, the regulation of flowering, mechanisms of nutrient withdrawal by phloem-feeding pathogens, and other physiological functions that are related to long distance transport. The present paper gives an overview of different approaches in plant research that utilized the strong and companion cell-specific expression of own or foreign genes driven by the AtSUC2 promoter.

Key words

Arabidopsis thaliana Assimilate transport AtSUC2 promoter Companion cells Phloem Sucrose carrier Sucrose transporter Vascular tissue 


  1. 1.
    Sauer N, Stolz J (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker’s yeast and identification of the histidine-tagged protein. Plant J 6:67–77CrossRefGoogle Scholar
  2. 2.
    Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11:4705–4713CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    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 196:564–570CrossRefGoogle Scholar
  4. 4.
    Stadler R, Sauer N (1996) The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot Acta 109:299–306CrossRefGoogle Scholar
  5. 5.
    Gottwald JR, Krysan PJ, Young JC et al (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci 97:13979–13984CrossRefGoogle Scholar
  6. 6.
    Srivastava AC, Dasgupta K, Ajieren E et al (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 104:1121–1128CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Gould N, Thorpe MR, Pritchard J et al (2012) AtSUC2 has a role for sucrose retrieval along the phloem pathway: evidence from carbon-11 tracer studies. Plant Sci 188–189:97–101CrossRefGoogle Scholar
  8. 8.
    Chalfie M, Tu Y, Euskirchen G et al (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805CrossRefGoogle Scholar
  9. 9.
    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 11:309–322CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Stadler R, Wright KM, Lauterbach C 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 41:319–331CrossRefGoogle Scholar
  12. 12.
    Werner D, Gerlitz N, Stadler R (2011) A dual switch in phloem unloading during ovule development in Arabidopsis. Protoplasma 248:225–235CrossRefGoogle Scholar
  13. 13.
    Wenig U, Meyer S, Stadler R et al (2013) Identification of MAIN, a factor involved in genome stability in the meristems of Arabidopsis thaliana. Plant J 75:469–483CrossRefGoogle Scholar
  14. 14.
    Schneidereit A, Imlau A, Sauer N (2008) Conserved cis-regulatory elements for DNA-binding-with-one-finger and homeo-domain-leucine-zipper transcription factors regulate companion cell-specific expression of the Arabidopsis thaliana SUCROSE TRANSPORTER 2 gene. Planta 228:651–662CrossRefGoogle Scholar
  15. 15.
    Wippel K, Sauer N (2012) Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter. J Exp Bot 63:669–679CrossRefGoogle Scholar
  16. 16.
    Reinders A, Sivitz AB, Ward JM (2012) Evolution of plant sucrose uptake transporters. Front Plant Sci 3:22CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Eom J-S, Nguyen CD, Lee D-W et al (2016) Genetic complementation analysis of rice sucrose transporter genes in Arabidopsis SUC2 mutant atsuc2. J Plant Biol 59:231–237CrossRefGoogle Scholar
  18. 18.
    Dasgupta K, Khadilkar AS, Sulpice 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 165:715–731CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40:119–138CrossRefGoogle Scholar
  20. 20.
    Oparka KJ, Roberts AG, Boevink P et al (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754CrossRefGoogle Scholar
  21. 21.
    Wright KM, Roberts AG, Martens HJ et al (2003) Structural and functional vein maturation in developing tobacco leaves in relation to AtSUC2 promoter activity. Plant Physiol 131:1555–1565CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Roberts IM, Boevink P, Roberts AG et al (2001) Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31–44CrossRefGoogle Scholar
  23. 23.
    Wu X, Huang R, Liu Z et al (2013) Functional characterization of cis-elements conferring vascular vein expression of At4g34880 amidase family protein gene in Arabidopsis. PLoS One 8:e67562CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Kuromori T, Sugimoto E, Shinozaki K (2014) Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiol 164:1587–1592CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ivashikina N, Deeken R, Ache P et al (2003) Isolation of AtSUC2 promoter-GFP-marked companion cells for patch-clamp studies and expression profiling. Plant J 36:931–945CrossRefGoogle Scholar
  26. 26.
    Birnbaum K, Shasha DE, Wang JY et al (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960CrossRefGoogle Scholar
  27. 27.
    Brady SM, Zhang L, Megraw M et al (2011) A stele-enriched gene regulatory network in the Arabidopsis root. Mol Syst Biol 7:459CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Brady SM, Orlando DA, Lee J-Y et al (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806CrossRefGoogle Scholar
  29. 29.
    Cartwright DA, Brady SM, Orlando DA et al (2009) Reconstructing spatiotemporal gene expression data from partial observations. Bioinformatics 25:2581–2587CrossRefGoogle Scholar
  30. 30.
    Zhang C, Barthelson RA, Lambert GM et al (2008) Global characterization of cell-specific gene expression through fluorescence-activated sorting of nuclei. Plant Physiol 147:30–40CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Mustroph A, Zanetti ME, Jang CJH et al (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A 106:18843–18848CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Collum TD, Culver JN (2017) Tobacco mosaic virus infection disproportionately impacts phloem associated translatomes in Arabidopsis thaliana and Nicotiana benthamiana. Virology 510:76–89CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Mähönen AP, Bonke M, Kauppinen L et al (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14:2938–2943CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lucas WJ, Groover A, Lichtenberger R et al (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388CrossRefGoogle Scholar
  35. 35.
    Rodriguez-Villalon A (2016) Wiring a plant: genetic networks for phloem formation in Arabidopsis thaliana roots. New Phytol 210:45–50CrossRefGoogle Scholar
  36. 36.
    Bonke M, Thitamadee S, Mähönen AP et al (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426:181–186CrossRefGoogle Scholar
  37. 37.
    Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Bauby H, Divol F, Truernit E et al (2007) Protophloem differentiation in early Arabidopsis thaliana development. Plant Cell Physiol 48:197–109CrossRefGoogle Scholar
  39. 39.
    Truernit E, Bauby H, Belcram K et al (2012) OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306–1315CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Rodriguez-Villalon A, Gujas B, Kang YH et al (2014) Molecular genetic framework for protophloem formation. Proc Natl Acad Sci U S A 111:11551–11556CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ruiz Sola MA, Coiro M, Crivelli S et al (2017) OCTOPUS-LIKE 2, a novel player in Arabidopsis root and vascular development, reveals a key role for OCTOPUS family genes in root metaphloem sieve tube differentiation. New Phytol 216:1191–1204CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Wallner E-S, López-Salmerón V, Belevich I et al (2017) Strigolactone- and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr Biol 27:1241–1247CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Dettmer J, Ursache R, Campilho A et al (2014) CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication. Nat Commun 5:4276CrossRefGoogle Scholar
  44. 44.
    Furuta KM, Yadav SR, Lehesranta S et al (2014) Plant development. Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345:933–937CrossRefGoogle Scholar
  45. 45.
    Ross-Elliott TJ, Jensen KH, Haaning KS et al (2017) Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. elife 6:e24125CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Viola R, Pelloux J, Van Der Ploeg A et al (2007) Symplastic connection is required for bud outgrowth following dormancy in potato (Solanum tuberosum L.) tubers. Plant Cell Environ 30:973–983CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239:27–38CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Benitez-Alfonso Y, Cilia M, Roman AS et al (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci 106:3615–3620CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Vatén A, Dettmer J, Wu S et al (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Yin H, Yan B, Sun J et al (2012) Graft-union development: a delicate process that involves cell–cell communication between scion and stock for local auxin accumulation. J Exp Bot 63:4219–4232CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Oparka KJ, Cruz SS (2000) THE GREAT ESCAPE: phloem transport and unloading of macromolecules. Annu Rev Plant Physiol Plant Mol Biol 51:323–347CrossRefGoogle Scholar
  52. 52.
    Paultre DSG, Gustin M-P, Molnar A et al (2016) Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–2025CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Spiegelman Z, Ham B-K, Zhang Z et al (2015) A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs. Plant J 83:853–863CrossRefGoogle Scholar
  54. 54.
    Spiegelman Z, Omer S, Mansfeld BN et al (2017) Function of Cyclophilin1 as a long-distance signal molecule in the phloem of tomato plants. J Exp Bot 68:e 953–e 964Google Scholar
  55. 55.
    Kehr J, Kragler F (2018) Long distance RNA movement. New Phytol 218:29–40CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Golan G, Betzer R, Wolf S (2013) Phloem-specific expression of a melon Aux/IAA in tomato plants alters auxin sensitivity and plant development. Front Plant Sci 4:329CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Chen X, Yao Q, Gao X et al (2016) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr Biol 26:640–646CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    An H, Roussot C, Suárez-López P et al (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Corbesier L, Vincent C, Jang S et al (2007) FT Protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033CrossRefGoogle Scholar
  61. 61.
    Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054CrossRefGoogle Scholar
  62. 62.
    Mathieu J, Warthmann N, Küttner F et al (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060CrossRefGoogle Scholar
  63. 63.
    Lu KJ, Huang NC, Liu YS et al (2012) Long-distance movement of Arabidopsis FLOWERING LOCUS T RNA participates in systemic floral regulation. RNA Biol 9:653–662CrossRefGoogle Scholar
  64. 64.
    Ho WWH, Weigel D (2014) structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Liu L, Liu C, Hou X et al (2012) FTIP1 is an essential regulator required for florigen transport. PLoS Biol 10:e1001313CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Serrano G, Herrera-Palau R, Romero JM et al (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr Biol 19:359–368CrossRefGoogle Scholar
  67. 67.
    Kim JJ, Lee JH, Kim W et al (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 159:461–478CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Porri A, Torti S, Romera-Branchat M et al (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 139:2198–2209CrossRefGoogle Scholar
  69. 69.
    Liu L, Zhang J, Adrian J et al (2014) Elevated levels of MYB30 in the phloem accelerate flowering in Arabidopsis through the regulation of FLOWERING LOCUS T. PLoS One 9:e89799CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Tränkner C, Lehmann S, Hoenicka H et al (2010) Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta 232:1309–1324CrossRefGoogle Scholar
  71. 71.
    Chen Q, Payyavula RS, Chen L et al (2018) FLOWERING LOCUS T mRNA is synthesized in specialized companion cells in Arabidopsis and Maryland Mammoth tobacco leaf veins. Proc Natl Acad Sci U S A 115:2830–2835CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Endo M, Yoshida M, Sasaki Y et al (2018) Re-evaluation of florigen transport kinetics with separation of functions by mutations that uncouple flowering initiation and long-distance transport. Plant Cell Physiol.
  73. 73.
    Voogd C, Brian LA, Wang T et al (2017) Three FT and multiple CEN and BFT genes regulate maturity, flowering, and vegetative phenology in kiwifruit. J Exp Bot 68:1539–1553CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Goralogia GS, Liu T-K, Zhao L et al (2017) CYCLING DOF FACTOR 1 represses transcription through the TOPLESS co-repressor to control photoperiodic flowering in Arabidopsis. Plant J 92:244–262CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Hayama R, Sarid-Krebs L, Richter R et al (2017) PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J 36:904–918CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Himber C, Dunoyer P, Moissiard G et al (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22:4523–4533CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360CrossRefGoogle Scholar
  78. 78.
    Smith LM, Pontes O, Searle I et al (2007) An SNF2 Protein Associated with Nuclear RNA Silencing and the Spread of a Silencing Signal between Cells in Arabidopsis. Plant Cell 19:1507–1521CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Haupt S, Oparka KJ, Sauer N et al (2001) Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. J Exp Bot 52:173–177CrossRefGoogle Scholar
  80. 80.
    Nadler-Hassar T, Goldshmidt A, Rubin B et al (2004) Glyphosate inhibits the translocation of green fluorescent protein and sucrose from a transgenic tobacco host to Cuscuta campestris Yunk. Planta 219:790–796CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Birschwilks M, Haupt S, Hofius D et al (2006) Transfer of phloem-mobile substances from the host plants to the holoparasite Cuscuta sp. J Exp Bot 57:911–921CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Aly R, Hamamouch N, Abu-Nassar J et al (2011) Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers. Plant Cell Rep 30:2233–2241CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Juergensen K, Scholz-Starke J, Sauer N et al (2003) The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia. Plant Physiol 131:61–69CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Hoth S, Schneidereit A, Lauterbach C et al (2005) Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiol 138:383–392CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Hoth S, Stadler R, Sauer N et al (2008) Differential vascularization of nematode-induced feeding sites. Proc Natl Acad Sci U S A 105:12617–12622CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Absmanner B, Stadler R, Hammes UZ (2013) Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Front Plant Sci 4:241CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Zhao D, You Y, Fan H et al (2018) The role of sugar transporter genes during early infection by root-knot nematodes. Int J Mol Sci 19:302CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Mondal HA, Louis J, Archer L et al (2018) Arabidopsis ACTIN-DEPOLYMERIZING FACTOR3 is required for controlling aphid feeding from the phloem. Plant Physiol 176:879–890CrossRefGoogle Scholar
  89. 89.
    Mukhtar MS, Deslandes L, Auriac M-C et al (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J 56:935–947CrossRefGoogle Scholar
  90. 90.
    Dutt M, Ananthakrishnan G, Jaromin MK et al (2012) Evaluation of four phloem-specific promoters in vegetative tissues of transgenic citrus plants. Tree Physiol 32:83–93CrossRefGoogle Scholar
  91. 91.
    Dutt M, Barthe G, Irey M et al (2015) Transgenic citrus expressing an Arabidopsis NPR1 gene exhibit enhanced resistance against huanglongbing (HLB; citrus greening). PLoS One 10:e0137134CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Javaid S, Amin I, Jander G et al (2016) A transgenic approach to control hemipteran insects by expressing insecticidal genes under phloem-specific promoters. Sci Rep 6:34706CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Zhao Y, Liu Q, Davis RE (2004) Transgene expression in strawberries driven by a heterologous phloem-specific promoter. Plant Cell Rep 23:224–230CrossRefGoogle Scholar
  94. 94.
    Sun Q, Zhao Y, Sun H et al (2011) High-efficiency and stable genetic transformation of pear (Pyrus communis L.) leaf segments and regeneration of transgenic plants. Acta Physiol Plant 33:383–390CrossRefGoogle Scholar
  95. 95.
    Liu Q, Chen X, Zhao H et al (2016) Phloem-specific expression of β-glucuronidase (GUS) driven by a heterologous AtSUC2 promoter in transgenic cherries. Acta Hortic:77–84Google Scholar
  96. 96.
    Schmülling T, Schell J, Spena A (1989) Promoters of the rolA, B, and C genes of Agrobacterium rhizogenes are differentially regulated in transgenic plants. Plant Cell 1:665–670CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Srivastava AC, Ganesan S, Ismail IO et al (2009) Effective carbon partitioning driven by exotic phloem-specific regulatory elements fused to the Arabidopsis thaliana AtSUC2 sucrose-proton symporter gene. BMC Plant Biol 9:7CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Matsuda Y, Liang G, Zhu Y et al (2002) The Commelina yellow mottle virus promoter drives companion-cell-specific gene expression in multiple organs of transgenic tobacco. Protoplasma 220:51–58CrossRefGoogle Scholar
  99. 99.
    Khadilkar AS, Yadav UP, Salazar C et al (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 170:401–414CrossRefGoogle Scholar
  100. 100.
    Chiou TJ, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci U S A 95:4784–4788CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Pizzio GA, Paez-Valencia J, Khadilkar AS et al (2015) Arabidopsis type I proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiol 167:1541–1553CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Dinant S, Ripoll C, Pieper M et al (2004) Phloem specific expression driven by wheat dwarf geminivirus V-sense promoter in transgenic dicotyledonous species. Physiol Plant 121:108–116CrossRefGoogle Scholar
  103. 103.
    Miyata LY, Harakava R, Stipp LCL et al (2012) GUS expression in sweet oranges (Citrus sinensis L. Osbeck) driven by three different phloem-specific promoters. Plant Cell Rep 31:2005–2013CrossRefGoogle Scholar
  104. 104.
    Koramutla MK, Bhatt D, Negi M et al (2016) Strength, stability, and cis-motifs of in silico identified phloem-specific promoters in Brassica juncea (L.). Front Plant Sci 7:457CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Molecular Plant Physiology, Department of BiologyUniversity of Erlangen-NurembergErlangenGermany

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