Skip to main content
SpringerLink
Log in

A DNA element between At4g28630 and At4g28640 confers companion-cell specific expression following the sink-to-source transition in mature minor vein phloem

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The collection phloem in minor veins is distinct from other vein classes in that the minor veins mature during the sink to source transition and are the primary sites of phloem loading. After maturation, minor vein phloem maintains its character in part through minor-vein specific regulatory cascades; however despite its physiological significance, little of these developmental programs is understood. From an Arabidopsis enhancer trap screen, we identified MATURE MINOR VEIN ELEMENT1 (MMVE1) in the intergenic region between two oppositely oriented genes, the ABC transporter ATM1 (At4g28630) and IAA11 (At4g28640). MMVE1 promotes reporter gene activity in minor vein phloem in a pattern resembling the sink to source transition. Promoter truncation experiments and phylogenetic footprinting demonstrate sequences proximal to ATM1 promote minor vein expression whereas sequences closer to IAA11 repress it. Both orientations of the promoter were used to drive expression of CONSTANS to generate a phloem mobile signal conferring early flowering under non-inductive conditions. Tandem copies of MMVE1 increase minor vein expression strength and specificity. MMVE1 is the first minor vein enhancer characterized from a species that loads from the apoplast, and supports the presence of unique regulatory cascades operating in minor vein phloem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

CO :

CONSTANS

CmGAS1 :

Cucumis melo GALACTINOL SYNTHASE1

GUS:

β-Glucuronidase enzyme

SUC2/SUT :

SUC/H+ symporter

XglcA:

5-Bromo-4-chloro-3-indolyl β-d-glucuronide

uidA :

β-glucuronidase gene

References

  • Abel S, Nguyen MD, Theologis A (1995) The Ps IAA4/5-like family of early auxin-inducible messenger RNAs in Arabidopsis thaliana. J Mol Biol 251:533–549

    Article  PubMed  CAS  Google Scholar 

  • Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 259:89–120

    Article  Google Scholar 

  • Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A, Shimada H, Kadowaki K (2002) Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: Toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32:401–408

    Article  PubMed  CAS  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) (2002) Short protocols in molecular biology: a compendium of methods from current protocols in molecular biology. Wiley, Hoboken

  • Ayre BG, Blair JE, Turgeon R (2003a) Functional and phylogenetic analyses of a conserved regulatory program in the phloem of minor veins. Plant Physiol 133:1229–1239

    Article  PubMed  CAS  Google Scholar 

  • Ayre BG, Keller F, Turgeon R (2003b) Symplastic continuity between companion cells and the translocation stream: Long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol 131:1518–1528

    Article  PubMed  CAS  Google Scholar 

  • Ayre BG, Turgeon R (2004) Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol 135:2271–2278

    Article  PubMed  CAS  Google Scholar 

  • Baskin TI, Busby CH, Fowke LC, Sammut M, Gubler F (1992) Improvements in immunostaining samples embedded in methacrylate—localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187:405–413

    Article  Google Scholar 

  • Becker D, Kemper E, Schell J, Masterson R (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol Biol 20:1195–1197

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Campisi L, Yang Y, Yi Y, Heilig E, Herman B, Cassista AJ, Allen DW, Xiang H, Jack T (1999) Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. Plant J 17:699–707

    Article  PubMed  CAS  Google Scholar 

  • Casson S, Spencer M, Walker K, Lindsey K (2005) Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. Plant J 42:111–123

    Article  PubMed  CAS  Google Scholar 

  • Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Kuhn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Groover A, Fontana JR, Dupper G, Ma C, Martienssen R, Strauss S, Meilan R (2004) Gene and enhancer trap tagging of vascular-expressed genes in poplar trees. Plant Physiol 134:1742–1751

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Mader MT, Kosarev P, Spannagl M, Yang L, Mayer KFX (2006) Large-scale cis-element detection by analysis of correlated expression and sequence conservation between Arabidopsis and Brassica oleracea. Plant Physiol 142:1589–1602

    Article  PubMed  CAS  Google Scholar 

  • Haritatos E, Ayre BG, Turgeon R (2000a) Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter. Plant Physiol 123:929–937

    Article  PubMed  CAS  Google Scholar 

  • Haritatos E, Medville R, Turgeon R (2000b) Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211:105–111

    Article  PubMed  CAS  Google Scholar 

  • He Y, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiol 126:707–716

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Eiguchi M, Kurata N (2004) Establishment of an enhancer trap system with Ds and GUS for functional genomics in rice. Mol Genet Genomics 271:639–650

    Article  PubMed  CAS  Google Scholar 

  • Ivashikina N, Deeken R, Ache P, Kranz E, Pommerrenig B, Sauer N, Hedrich R (2003) Isolation of AtSUC2 promoter-GFP-marked companion cells for patch-clamp studies and expression profiling. Plant J 36:931–945

    Article  PubMed  CAS  Google Scholar 

  • Johnson AAT, Hibberd JM, Gay C, Essah PA, Haseloff J, Tester M, Guiderdoni E (2005) Spatial control of transgene expression in rice (Oryza sativa L.) using the GAL4 enhancer trapping system. Plant J 41:779–789

    Article  PubMed  CAS  Google Scholar 

  • Kerk NM, Ceserani T, Tausta SL, Sussex IM, Nelson TM (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol 132:27–35

    Article  PubMed  CAS  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of Ti-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Kuhn C, Quick WP, Schulz A, Riesmeier JW, Sonnewald U, Frommer WB (1996) Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ 19:1115–1123

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Loots GG, Ovcharenko I, Pachter L, Dubchak I, Rubin EM (2002) rVISTA for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res 12:832–839

    PubMed  Google Scholar 

  • Maniatis T, Goodbourn S, Fischer JA (1987) Regulation of inducible and tissue-specific gene-expression. Science 236:1237–1245

    Article  PubMed  CAS  Google Scholar 

  • Martens HJ, Roberts AG, Oparka KJ, Schulz A (2006) Quantification of plasmodesmatal endoplasmic reticulum coupling between sieve elements and companion cells using fluorescence redistribution after photobleaching. Plant Physiol 142:471–480

    Article  PubMed  CAS  Google Scholar 

  • Matsuda Y, Liang GQ, Zhu YL, Ma FS, Nelson RS, Ding B (2002) The Commelina yellow mottle virus promoter drives companion- cell-specific gene expression in multiple organs of transgenic tobacco. Protoplasma 220:51–58

    Article  PubMed  CAS  Google Scholar 

  • Nagawa S, Sawa S, Sato S, Kato T, Tabata S, Fukuda H (2006) Gene trapping in Arabidopsis reveals genes involved in vascular development. Plant Cell Physiol 47:1394–1405

    Article  PubMed  CAS  Google Scholar 

  • Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596

    Article  PubMed  CAS  Google Scholar 

  • Nelson T (2002) Development of laser-capture microdissection (LCM) for plant tissues. Plant Physiol 129:419–420

    Google Scholar 

  • O’Connor TR, Dyreson C, Wyrick JJ (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21:4411–4413

    Article  PubMed  CAS  Google Scholar 

  • Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pommerrenig B, Papini-Terzi FS, Sauer N (2007) Differential regulation of sorbitol and sucrose loading into the phloem of Plantago major in response to salt stress. Plant Physiol 144:1029–1038

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sieburth LE, Deyholos MK (2006) Vascular development: the long and winding road. Curr Opin Plant Biol 9:48–54

    Article  PubMed  CAS  Google Scholar 

  • Springer PS (2000) Gene traps: tools for plant development and genomics. Plant Cell 12:1007–1020

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40:119–138

    Article  Google Scholar 

  • Turgeon R, Ayre BG (2005) Pathways and mechanisms of phloem loading. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier Academic Press, New York, pp 45–67

    Chapter  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • van Bel AJE (1996) Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with associated physiological software packages in dicotyledons. J Exp Bot 47:1129–1140

    Google Scholar 

  • Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci USA 99:10876–10880

    Article  PubMed  CAS  Google Scholar 

  • Volk GM, Haritatos EE, Turgeon R (2003) Galactinol synthase gene expression in melon. J Am Soc Hort Sci 128:8–15

    CAS  Google Scholar 

  • Weigel D, Glazebrook J (2002) Arabidopsis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Weise A, Barker L, Kuhn C, Lalonde S, Buschmann H, Frommer WB, Ward JM (2000) A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12:1345–1355

    Article  PubMed  CAS  Google Scholar 

  • Windsor AJ, Schranz ME, Formanova N, Gebauer-Jung S, Bishop JG, Schnabelrauch D, Kroymann J, Mitchell-Olds T (2006) Partial shotgun sequencing of the Boechera stricta genome reveals extensive microsynteny and promoter conservation with Arabidopsis. Plant Physiol 140:1169–1182

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Jefferson RA, Huttner E, Moore JM, Gagliano WB, Grossniklaus U (2005) An egg apparatus-specific enhancer of Arabidopsis, identified by enhancer detection. Plant Physiol 139:1421–1432

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama R, Hirose T, Fujii N, Aspuria ET, Kato A, Uchimiya H (1994) The rolC promoter of Agrobacterium rhizogenes Ri plasmid is activated by sucrose in transgenic tobacco plants. Mol Gen Genet 244:15–22

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Robert Turgeon for his support early in this project, and talented undergraduates Kenny Morales, Leslie Reed, Hoon Park, and Bruno Britto for their assistance. This work was supported in part by NSF IOS 0344088 to BGA.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of North Texas, 1504 W. Mulberry, SRB Rm 120, P.O. Box 305220, Denton, TX, 76203 5220, USA

    Roisin C. McGarry & Brian G. Ayre

Authors
  1. Roisin C. McGarry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian G. Ayre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian G. Ayre.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2008_786_MOESM1_ESM.eps

MOESM1 MMVE1 is conserved among the Brassicaceae. (a) rVISTA graphical alignment of the orthologous intergenic regions from Arabis purpurea, Thalaspi arvense, Brassica oleraceae, Brassica rapa, Brassica nigra, Crambe hispanica, Rapistrum rugosum, Sisymbrium irio, and Sinapis alba, relative to the Arabidopsis reference sequence. The sequence similarity is illustrated by pink peaks, with the scale bar (50–100%) shown on the right side (EPS 4997 kb)

425_2008_786_MOESM2_ESM.doc

MOESM2 MMVE1 is conserved among the Brassicaceae. (b) rVISTA nucleotide alignment of (a). The orientation of the Arabidopsis sequence is indicated (−1393 to −1); the orthologous sequences are presented in order of increasing nucleotides (i.e. +1 to x) (DOC 133 kb)

425_2008_786_MOESM3_ESM.eps

MOESM3 IAA11p::CO confers early flowering under non-inductive conditions. (a) Shown is the construction and orientation of the full length intergenic region used to drive CO expression. (b) A representative T1 IAA11p::CO plant flowers earlier than a WT plant when both are grown under non-inductive conditions. Scale bars are 1mm (EPS 1206 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

McGarry, R.C., Ayre, B.G. A DNA element between At4g28630 and At4g28640 confers companion-cell specific expression following the sink-to-source transition in mature minor vein phloem. Planta 228, 839–849 (2008). https://doi.org/10.1007/s00425-008-0786-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0786-1

Keywords

Search

Navigation