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Increased hexose transport in the roots of tomato plants submitted to prolonged hypoxia

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Abstract

We investigated the effects of prolonged hypoxia on the sugar uptake in tomato (Solanum lycopersicum L. var. MP-1) roots. Hydroponic cultures of whole tomato plants were submitted to hypoxic treatment for 1 week, and the roots were analyzed for sugar concentrations, hexose uptake and hexose transporter expression level. Contrary to what has been observed after anoxic shock or short-term hypoxic treatment, we show that sugar concentrations increase and hexose uptake is up-regulated in the roots after 1 week of hypoxic treatment. Increased hexose transport is concomitant with the induction of the hexose transporter gene LeHT2. These responses may be due either to a direct effect of low O2 supply, or to a secondary effect associated with the increase in sugar concentrations, which, typically, develops in most hypoxic plants.

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Fig. 1
Fig. 2

Abbreviations

HT:

Hexose transporter

References

  • Barker L, Kühn K, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–1164

    Article  PubMed  CAS  Google Scholar 

  • Biemelt S, Hajirezaei MR, Melzer M, Albrecht G, Sonnewald U (1999) Sucrose synthase activity does not restrict glycolysis in roots of transgenic potato plants under hypoxic conditions. Planta 210:41–49

    Article  PubMed  CAS  Google Scholar 

  • Brouquisse R, James F, Pradet A, Raymond P (1991) Study of glucose starvation in excised maize root tips. Plant Physiol 96:619–626

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465:263–274

    Article  PubMed  Google Scholar 

  • Chaudhuri B, Hörmann F, Lalonde S, Brady SM, Orlando DA, Benfey P, Frommer WB (2008) Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J 56:948–962

    Article  PubMed  CAS  Google Scholar 

  • Drew MM (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Article  PubMed  CAS  Google Scholar 

  • Gear ML, McPhillips ML, Patrick JW, McCurdy DW (2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Mol Biol 44:687–697

    Article  PubMed  CAS  Google Scholar 

  • Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256

    Article  PubMed  CAS  Google Scholar 

  • Germain V, Ricard B, Raymond P, Saglio P (1997) The role of sugars, hexokinase, and sucrose synthase in the determination of hypoxically induced tolerance to anoxia in tomato roots. Plant Physiol 114:167–175

    PubMed  CAS  Google Scholar 

  • Gharbi I (2007) Rôle de l’hexokinase et du transporteur d’hexoses dans l’acclimatation à l’hypoxie chez la tomate. PhD thesis, Biology Department, University of Tunis, pp 173

  • Gharbi I, Ricard B, Rolin D, Maucourt M, Andrieu MH, Bizid E, Smiti S, Brouquisse R (2007) Effect of hexokinase activity on tomato root metabolism during prolonged hypoxia. Plant Cell Environ 30:508–517

    Article  PubMed  CAS  Google Scholar 

  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Gibson S (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gout E, Boisson AM, Aubert S, Bligny R (2001) Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. Plant Physiol 125:912–925

    Article  PubMed  CAS  Google Scholar 

  • Gronewald JW, Cheeseman JM, Hanson JB (1979) Comparison of the responses of corn root tissue to fusicoccin and washing. Plant Physiol 63:255–259

    Article  PubMed  CAS  Google Scholar 

  • Hole DJ, Cobb BG, Hole PS, Drew MC (1992) Enhancement of anaerobic respiration in root tips of Zea mays following low-oxygen (hypoxic) acclimation. Plant Physiol 99:213–218

    Article  PubMed  CAS  Google Scholar 

  • Joubès J, Phan TH, Just D, Rothan D, Bergounioux C, Raymond P, Chevalier C (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol 121:857–869

    Article  PubMed  Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540

    Article  PubMed  CAS  Google Scholar 

  • Koch KE, Ying Z, Wu Y, Avigne WT (2000) Multiple paths of sugar-sensing and sugar/oxygen overlap for gene of sucrose and ethanol metabolism. J Exp Bot 51:417–427

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  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 

  • Limpinuntana V, Greenway H (1979) Sugar accumulation in barley and rice grown in solutions with low concentrations of oxygen. Ann Bot 43:373–381

    CAS  Google Scholar 

  • Menu T, Saglio P, Granot D, Dai N, Raymond P, Ricard B (2003) High hexokinase activity in tomato fruit perturbs carbon and energy metabolism and reduces fruit and seed size. Plant Cell Environ 27:89–98

    Article  Google Scholar 

  • Moing A, Maucourt M, Renaud C, Gaudillère M, Brouquisse R, Lebouteiller B, Gousset-Dupont A, Vidal J, Granot D, Denoyes-Rothan B, Lerceteau-Köhler E, Rolin D (2004) Quantitative metabolic profiling by 1-dimensional 1H-NMR analyses; application to plant genetics and functional genomics. Funct Plant Biol 31:889–902

    Article  CAS  Google Scholar 

  • Payne D, Gregory PJ (1988) The soil atmosphere, Chap 9. In: Wild A (ed) Russell’s soil conditions and plant growth, 11th edn. Longman, New York, pp 301–314

    Google Scholar 

  • Price J, Laxmi A, St Martin S, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150

    Article  PubMed  CAS  Google Scholar 

  • Roberts JKM, Andrade FH, Anderson IC (1985) Further evidence that cytoplasmic acidosis is a determinant of flooding tolerance in plants. Plant Physiol 77:492–494

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Thorne JH (1982) Temperature and oxygen effects on 14C-photosynthate unloading and accumulation in developing soybean seeds. Plant Physiol 69:48–53

    Article  PubMed  CAS  Google Scholar 

  • Trought MCT, Drew MC (1980) The development of waterlogging damage in wheat seedlings (Triticum aestivum L.). I. Shoot and root growth in relation to changes in concentrations of dissolved gases and solutes in the soil solution. Plant Soil 54:77–94

    Article  CAS  Google Scholar 

  • van Dongen JT, Roeb GW, Dautzenberg M, Froelich A, Vigeolas H, Minchin PE, Geigenberger P (2004) Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds. Plant Physiol 135:1809–1821

    Article  PubMed  Google Scholar 

  • Verwoerd TC, Dekker BM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17:2362

    Article  PubMed  CAS  Google Scholar 

  • Weise A, Barker L, Kühn 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 

  • Xia JH, Saglio P (1988) Characterization of the hexose transport system in maize root tips. Plant Physiol 88:1015–1020

    Article  PubMed  CAS  Google Scholar 

  • Xia JH, Saglio P (1990) H+ efflux and hexose transport under imposed energy status in maize root tips. Plant Physiol 93:453–459

    Article  PubMed  CAS  Google Scholar 

  • Xia JH, Saglio P, Roberts JKM (1995) Nucleotide levels do not critically determine survival of maize root tips acclimated to a low-oxygen environment. Plant Physiol 108:589–595

    PubMed  CAS  Google Scholar 

  • Zhang Q, Greenway H (1995) Membrane transport in anoxic rice coleoptiles and storage tissues of beet root. Aust J Plant Physiol 22:965–975

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the French Institut National de la Recherche Agronomique and by the Comité Mixte Franco-Tunisien pour la Coopération Universitaire (Grant No. 03G0209). We are sincerely grateful to the referees for their thorough reading of the manuscript, and pertinent suggestions to improve the original manuscript. We also thank Julie Hopkins for language correction.

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Authors and Affiliations

  1. Unité d’Ecologie Végétale, Département des Sciences Biologiques, Faculté des Sciences de Tunis, 2092, El Manar II, Tunisia

    Imène Gharbi, Samira Smiti & Essia Bizid

  2. UMR Physiologie et Biotechnologie Végétales, INRA de Bordeaux, BP 81, 33883, Bordeaux, France

    Bérénice Ricard

  3. UMR1064 Interactions Plantes-Microorganismes and Santé Végétale, INRA, Centre de Recherche de Sophia-Antipolis, 400 route des Chappes, BP 167, 06903, Sophia Antipolis Cedex, France

    Renaud Brouquisse

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  1. Imène Gharbi
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  2. Bérénice Ricard
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  5. Renaud Brouquisse
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Correspondence to Imène Gharbi.

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Gharbi, I., Ricard, B., Smiti, S. et al. Increased hexose transport in the roots of tomato plants submitted to prolonged hypoxia. Planta 230, 441–448 (2009). https://doi.org/10.1007/s00425-009-0941-3

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