Skip to main content
SpringerLink
Log in

Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves

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

Abstract

Magnesium deficiency has been reported to affect plant growth and biomass partitioning between root and shoot. The present work aims to identify how Mg deficiency alters carbon partitioning in sugar beet (Beta vulgaris L.) plants. Fresh biomass, Mg and sugar contents were followed in diverse organs over 20 days under Mg-sufficient and Mg-deficient conditions. At the end of the treatment, the aerial biomass, but not the root biomass, of Mg-deficient plants was lower compared to control plants. A clear inverse relationship between Mg and sugar contents in leaves was found. Mg deficiency promoted a marked increase in sucrose and starch accumulation in the uppermost expanded leaves, which also had the lowest content of Mg among all the leaves of the rosette. The oldest leaves maintained a higher Mg content. [14C]Sucrose labelling showed that sucrose export from the uppermost expanded leaves was inhibited. In contrast, sucrose export from the oldest leaves, which are close to, and export mainly to, the roots, was not restricted. In response to Mg deficiency, the BvSUT1 gene encoding a companion cell sucrose/H+ symporter was induced in the uppermost expanded leaves, but without further enhancement of sucrose loading into the phloem. The observed increase in BvSUT1 gene expression supports the idea that sucrose loading into the phloem is defective, resulting in its accumulation in the leaf.

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. 1a,b
Fig. 2
Fig. 3
Fig. 4a,b
Fig. 5a–c
Fig. 6a,b

Similar content being viewed by others

References

  • Aoki N, Hirose T, Takahashi S, Ono K, Ishimaru K, Oshugi R (1999) Molecular cloning and expression analysis of a gene for a sucrose transporter in maize (Zea mays L.). Plant Cell Physiol 40:99–112

    Google Scholar 

  • Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232

    Article  CAS  PubMed  Google Scholar 

  • Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365

    CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore D, Seidman JG, Smith JA, Struhl K, eds (1998) Current protocols in molecular biology. Greene Publishing Associates & Wiley-Interscience, New York

  • Bennett WF, ed (1997) Nutrients deficiencies & toxicities in crop plants. The American Phythopathological Society Press, St Paul, MN

  • Bonnemain JL (1964) Transport du 14C assimilé chez les Solanacées. Rev Gen Bot 75:579–610

    Google Scholar 

  • Bouché-Pillon S, Fleurat-Lessard P, Fromont JC, Serrano R, Bonnemain JL (1994) Immunolocalization of the plasma membrane H+-ATPase in minor veins of Vicia faba in relation to phloem loading. Plant Physiol 105:691–697

    Google Scholar 

  • Bürkle L, Hibberd JM, Quick WP, Kühn C, Hirner B, Frommer WB (1998) The H+-sucrose cotransporter NtSUT1 is essential for sucrose export from tobacco leaves. Plant Physiol 118:59–68

    Google Scholar 

  • Bush DR (1989) Proton-coupled sucrose transport in plasmalemma vesicles isolated from sugar beet (Beta vulgaris L. cv Great Western) leaves. Plant Physiol 89:1318–1323

    Google Scholar 

  • Bush DR (1993) Proton-coupled sugar and amino acid transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 44:513–542

    Article  CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994a) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250

    CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994b) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45:1251–1257

    CAS  Google Scholar 

  • Chiou T-J, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 95:4784–4788

    Article  CAS  PubMed  Google Scholar 

  • Cowan JA (2002) Structural and catalytic chemistry of magnesium-dependent enzymes. Biometals 15:225–235

    Article  CAS  PubMed  Google Scholar 

  • Delrot S, Bonnemain J-L (1981) Involvement of protons as a substrate for the sucrose carrier during phloem loading in Vicia faba leaves. Plant Physiol 67:560–564

    CAS  Google Scholar 

  • Dewitt ND, Sussman MR (1995) Immunocytological localization of an epitope-tagged plasma membrane proton pump (H+-ATPase) in phloem companion cells. Plant Cell 7:2053–2067

    Article  CAS  PubMed  Google Scholar 

  • Ericsson T, Kahr M (1995) Growth and nutrition of birch seedlings at varied relative addition rates of magnesium. Tree Physiol 15:85–93

    CAS  PubMed  Google Scholar 

  • Fisher ES, Bremer E (1993) Influence of magnesium deficiency on rates of leaf expansion, starch and sucrose accumulation and net assimilation in Phaseolus vulgaris. Physiol Plant 89:271–276

    Article  CAS  Google Scholar 

  • Fisher ES, Lohaus G, Heineke D, Heldt HW (1998) Magnesium deficiency results in accumulation of carbohydrates and amino acids in source and sink leaves of spinach. Physiol Plant 102:16–20

    Article  CAS  Google Scholar 

  • Foyer CH (1988) Feedback inhibition of photosynthesis through source–sink regulation in leaves. Plant Physiol Biochem 26:483–492

    CAS  Google Scholar 

  • Giaquinta R (1976) Evidence for phloem loading from the apoplast. Chemical modification of membrane sulfhydryl groups. Plant Physiol 57:872–875

    CAS  Google Scholar 

  • Gifford RM, Evans LT (1981) Photosynthesis, carbon partitioning and yield. Annu Rev Plant Physiol 32:485–509

    Article  CAS  Google Scholar 

  • Grusak MA, Delrot S, Ntsika G (1990) Short-term effect of heat-girdles on source leaves of Vicia faba: analysis of phloem loading and carbon partitioning parameters. J Exp Bot 41:1371–1377

    Google Scholar 

  • Harms K, Wöhner RV, Schulz B, Frommer WB (1994) Regulation of two p-type H+-ATPase genes from potato. Plant Mol Biol 26:979–988

    CAS  PubMed  Google Scholar 

  • Kühn 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

    Google Scholar 

  • Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Molecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300

    Article  PubMed  Google Scholar 

  • Lemoine R, Delrot S (1989) Proton-motive-force-driven sucrose uptake in sugar-beet plasma-membrane vesicles. FEBS Lett 249:129–133

    Article  CAS  Google Scholar 

  • Lemoine R, Kühn C, Thiele N, Delrot S, Frommer WB (1996) Antisense and sense expression of the sucrose transporter in potato: effects on amount and activity. Plant Cell Environ 19:1124–1131

    Google Scholar 

  • Lerchl J, Geigenberger P, Stitt M, Sonnewald U (1995) Impaired photoassimilate partitioning caused by phloem-specific removal of pyrophosphate can be complemented by a phloem-specific cytosolic yeast-derived invertase in transgenic plants. Plant Cell 7:259–270

    Article  CAS  PubMed  Google Scholar 

  • López-Buico J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  Google Scholar 

  • Mengel K, Kirkby EA (1987) Principles of plant nutrition. International Potash Institute, Worblaufen-Bern, Switzerland, pp 481–492

  • Mitchell AD, Loganathan P, Payn TW, Tillman RW (1999) Effect of calcined magnesite on soil and Pinus radiata foliage magnesium in pumice soils of New Zealand. Aust J Soil Res 37:545–560

    CAS  Google Scholar 

  • Noiraud N, Delrot S, Lemoine R (2000) The sucrose transporter of celery. Identification and expression during salt stress. Plant Physiol 122:1447–1455

    Google Scholar 

  • Ntsika G, Delrot S (1986) Changes in apoplastic and intracellular leaf sugars induced by the blocking of export in Vicia faba. Physiol Plant 68:145–153

    CAS  Google Scholar 

  • Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975:384–394

    CAS  Google Scholar 

  • Ransom-Hodgkins WD, Vaughn MW, Bush DR (2003) Protein phosphorylation plays a key role in sucrose-mediated transcriptional regulation of a phloem-specific proton–sucrose symporter. Planta 217:483–489

    Article  CAS  PubMed  Google Scholar 

  • Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J 26:421–433

    Article  CAS  PubMed  Google Scholar 

  • Shakya R, Sturm A (1998) Characterization of source- and sink-specific sucrose/H+ symporters from carrot. Plant Physiol 118:1473–1480

    Google Scholar 

  • Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323

    Article  CAS  PubMed  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038

    Article  CAS  PubMed  Google Scholar 

  • Sokolov LN, Déjardin A, Kleczkowski LA (1998) Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochem J 336:681–687

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Weber H, Borisjuk L, Heim U, Sauer N, Wobus U (1997) A role for sugar transporters during seed development: molecular characterisation of a hexose and a sucrose carrier in faba bean seeds. Plant Cell 9:895–908

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson SR, Welch RM, Mayland HF, Grunes DL (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. Metal Ions Biol Syst 26:33–56

    CAS  Google Scholar 

  • Zhao R, Dielen V, Kinet J-M, Boutry M (2000) Cosuppression of a plasma membrane H+-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth and male fertility. Plant Cell 12:535–546

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

C Hermans was supported by an FRIA grant (Fond pour la Formation de la Recherche dans l’Industrie et dans l’Agriculture, Belgium). This research was supported by a grant from the Interuniversity Attraction Pole Program—Belgian Science Policy (Project V/13). We thank Prof. D.R. Bush, P. Tocquin and L. Corbesier for valuable advice. Access to the spectrometer equipment was provided by Prof. C. Buess, Laboratoire de Chimie Analytique, Université Libre de Bruxelles.

Author information

Author notes

  1. Christian Hermans

    Present address: Biology Department, Colorado State University, Fort Collins, CO 80523, USA

  2. Fabienne Bourgis

    Present address: Centre IRD de Montpellier, Avenue Agropolis, BP 64501, 34394, Montpellier Cedex 5, France

Authors and Affiliations

  1. Laboratoire de Physiologie et de Génétique Moléculaire des Plantes, Université Libre de Bruxelles, 1050, Brussels, Belgium

    Christian Hermans, Fabienne Bourgis & Nathalie Verbruggen

  2. Bioenergetics Laboratory, University of Geneva, 1254, Geneva, Switzerland

    Christian Hermans & Reto J. Strasser

  3. Laboratoire de Physiologie, Biochimie et Biologie Moléculaire Végétales, Unité Mixte de Recherches Centre National de la Recherche Scientifique 6161, Université de Poitiers, 86022, Poitiers Cedex, France

    Mireille Faucher & Serge Delrot

Authors
  1. Christian Hermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabienne Bourgis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mireille Faucher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reto J. Strasser
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Serge Delrot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nathalie Verbruggen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Hermans.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hermans, C., Bourgis, F., Faucher, M. et al. Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220, 541–549 (2005). https://doi.org/10.1007/s00425-004-1376-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1376-5

Keywords

Search

Navigation