Skip to main content
SpringerLink
Log in

The Role and Regulation of Sugar Transporters in Plants with Crassulacean Acid Metabolism

  • Chapter
Progress in Botany

Part of the book series: Progress in Botany ((BOTANY,volume 70))

The photosynthetic specialisation of Crassulacean acid metabolism (CAM) operates via a diel separation of carboxylation processes mediated by phosphoenolpyruvate carboxylase (PEPC) and Rubisco which optimise photosynthetic performance and carbon gain in potentially limiting environments. Carbohydrates are a key limiting factor for nocturnal CO2 uptake in CAM plants, and the partitioning of sugars towards providing substrate for dark carboxylation must be balanced with the requirements of other competing sinks that include growth and export. Sugar transporters have been recognised previously as key targets for regulatory roles in the long-distance and subcellular distribution and partitioning of assimilates in plants. Thus, in CAM plants, sugar transporters may represent a strategic checkpoint for regulating the partitioning of photosynthetically fixed carbon between provision of substrate for nocturnal carboxylation and export for growth. In this review, we examine the major pathways underpinning sugar flux in CAM plants and describe the requirements for sugar transport across the chloroplastic and vacuolar membranes as well as for long-distance transport in the phloem. We review current knowledge on the structure, function and regulation of plant sugar transporters and highlight candidate sugar transporters that could play cardinal roles in regulating carbohydrate partitioning between the potentially conflicting fates of storage for CAM and for growth and productivity.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Antony E (2007) Cloning localisation and expression analysis of sugar transporters in CAM plants. PhD Thesis, Newcastle University

    Google Scholar 

  • Antony E, Taybi T, Courbot M, Mugford S, Smith JAC, Borland AM (2008) Cloning, localisation and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). J Exp Bot, accepted for publication

    Google Scholar 

  • Atanassova R, Leterrier M, Gaillard C, Agasse A, Sagot E, Coutos-Thevenot P, Delrot S (2003) Sugar-regulated expression of a putative hexose transport gene in grape. Plant Physiol 131: 326–334

    Article  PubMed  CAS  Google Scholar 

  • Bartholomew D, Kadzimin S (1977) Pineapple. In: Alvim P de T, TT Kozolowski TT (eds) Ecophysiology of Tropical Crops. Academic Press, New York, pp. 113–156

    Google Scholar 

  • Black CC, Chen JQ, Doong RL, Angelov MN, Sung SJS (1996) Alternative carbohydrate reserves used in the daily cycle of Crassulacean acid metabolism. In: Winter K, Smith, JAC (eds) Crassulacean Acid Metabolism; Biochemistry, Ecophysiology and Evolution. Springer, Berlin, pp. 31–43

    Google Scholar 

  • Borland AM (1996) A model for the partitioning of photosynthetically fixed carbon during the C3-CAM transition in Sedum telephium. New Phytol 134: 433–444

    Article  CAS  Google Scholar 

  • Borland AM, Dodd AN (2002) Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Fun Plant Biol 29: 707–716

    Article  CAS  Google Scholar 

  • Borland AM, Griffiths H (1989) The regulation of citric acid accumulation and carbon recycling during CAM in Ananas comosus. J Exp Bot 40: 53–60

    Article  CAS  Google Scholar 

  • Borland AM, Taybi T (2004) Synchronization of metabolic processes in plants with Crassulacean acid metabolism. J Exp Botany 55: 1255–1265

    Article  CAS  Google Scholar 

  • Borland AM, Griffiths H, Broadmeadow MSJ, Fordham MC, Maxwell C (1994) Carbon-isotope composition of biochemical fractions and the regulation of carbon balance in leaves of the C3-Crassulacean acid metabolism intermediate Clusia minor L growing in Trinidad. Plant Physiol 106: 493–501

    PubMed  CAS  Google Scholar 

  • Borland AM, Hartwell J, Jenkins GI, Wilkins MB, Nimmo HG (1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in Crassulacean acid metabolism. Plant Physiol 121: 889–896

    Article  PubMed  CAS  Google Scholar 

  • Borland AM, Maxwell K, Griffiths H (2000) Ecophysiology of the CAM pathway. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism. Kluwer, The Netherlands, pp. 583–605.

    Google Scholar 

  • Büttner M (2007) The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Letts 581: 2318–2324

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Christopher JT, Holtum JAM (1996) Patterns of carbon partitioning in leaves of Crassulacean acid metabolism species during deacidification. Plant Physiol 112: 393–399

    PubMed  CAS  Google Scholar 

  • Christopher JT, Holtum JAM (1998) Carbohydrate partitioning in the leaves of Bromeliaceae performing C3 photosynthesis or Crassulacean acid metabolism. Aus J Plant Physiol 25: 371–376

    Article  CAS  Google Scholar 

  • Deléens E, Garnierdardart J, Queiroz O (1979) Carbon isotope composition of intermediates of the starch-malate sequence and level of Crassulacean acid metabolism in leaves of Kalanchoë blossfeldiana Tom Thumb. Planta 146: 441–449

    Article  Google Scholar 

  • Delrot S, Atanassova R, Maurousset L (2003) Regulation of sugar, amino acid and peptide plant membrane transporters. Biochim Biophys Acta 1465: 281–306

    Google Scholar 

  • Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002) Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53: 569–580

    Article  PubMed  CAS  Google Scholar 

  • Echeverria E (2000) Vesicle-mediated solute transport between the vacuole and the plasma membrane. Plant Physiol 123: 1217–1226

    Article  PubMed  CAS  Google Scholar 

  • 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 thaliana mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141: 196–207

    Article  PubMed  CAS  Google Scholar 

  • Giegé P, Heazlewood JL, Roessner-Tunali U, Millar AH, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15: 2140–2151

    Article  PubMed  CAS  Google Scholar 

  • Gouws LM, Osmond CB, Schurr U, Walter A (2005) Distinctive diel growth cycles in leaves and cladodes of CAM plants: differences from C3 plants and putative interactions with substrate availability, turgor and cytoplasmic pH. Fun Plant Biol 32: 421–428

    Article  CAS  Google Scholar 

  • Häusler RE, Baur B, Scharte J, Teichmann T, Eicks M, Fischer KL, Flugge UI, Schubert S, Weber A, Fischer K (2000) Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum. Plant J 24: 285–296

    Article  PubMed  Google Scholar 

  • Hartwell J (2005) The co-ordination of central plant metabolism by the circadian clock. Biochem Soc Trans 33: 945–948

    Article  PubMed  CAS  Google Scholar 

  • Hirose T, Imaizumi N, Scofield GN, Furbank RT, Ohsugi R (1997) cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol 38: 1389–1396

    Google Scholar 

  • Holtum JAM, Smith JAC, Neuhaus HE (2005) Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Fun Plant Biol 32: 429–450

    Article  CAS  Google Scholar 

  • Kenyon WH, Severson RF, Black CC (1985) Maintenance carbon cycle in Crassulacean acid metabolism plant leaves: source and compartmentation of carbon for nocturnal malate synthesis. Plant Physiol 77: 183–189

    Article  PubMed  CAS  Google Scholar 

  • Kiyosue T, Abe H, Yamaguchi-Shinozaki K, Shinozaki K (1998) ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochim Biophys Acta 1370: 187–191

    Article  Google Scholar 

  • Kluge M (1969) Veränderliche Markierungsmuster bei 14CO2 Fütterung von Bryophyllum tubiflorum zu verschiedenen Zeipunkten der Hell-Dunkel-Periode. I. Die Fütterung unter Belichtung Planta 88: 113–129

    CAS  Google Scholar 

  • Kore-eda S, Kanai R (1997) Induction of glucose 6-phosphate transport activity in chloroplasts of Mesembryanthemum crystallinum by the C3-CAM transition Plant Cell Physiol 38: 895–901

    Google Scholar 

  • Kore-eda S, Noake C, Ohishi M, Ohnishi J-I, Cushman JC (2005) Transcriptional regulation of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum. Fun Plant Biol 32: 451–466

    Article  CAS  Google Scholar 

  • Kuhn 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

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Ann Rev Plant Biol 55: 341–372

    Article  CAS  Google Scholar 

  • Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochim Biophys Acta 1465: 246–262

    Article  PubMed  CAS  Google Scholar 

  • Lüttge U (1988) Day–night changes of citric acid levels in CAM: phenomenon and ecophysiological significance. Plant Cell Environ 11: 445–451

    Article  Google Scholar 

  • McRae SR, Christopher JT, Smith JAC, Holtum JAM (2002) Sucrose transport across the vacuolar membrane of Ananas comosus. Fun Plant Biol 29: 717–726

    Article  CAS  Google Scholar 

  • Miao Y, Yan PK, Kim H, Hwang I, Jiang L (2006) Localization of green fluorescent protein fusions with the seven arabidopsis vacuolar sorting receptors to prevacuolar compartments in tobacco BY-2 cells. Plant Physiol 142: 945–962

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus HE, Schulte N (1996) Starch degradation in chloroplasts isolated from C3 or CAM (crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. Biochem J 318: 945–953

    PubMed  CAS  Google Scholar 

  • Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87–89

    Article  PubMed  CAS  Google Scholar 

  • Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5: 75–80

    Article  PubMed  CAS  Google Scholar 

  • Nobel PS (1996) High productivity of certain agronomic CAM species. In: Winter K, Smith JAC (eds) Crassulacean Acid Metabolism. Biochemistry, Ecophysiology and Evolution. Springer, Berlin, pp. 255–265

    Google Scholar 

  • Osmond CB (1978) Crassulacean acid metabolism – curiosity in context. Ann Rev Plant Phys Plant Mol Biol 29: 379–414

    CAS  Google Scholar 

  • Osmond CB, Holtum JAM (1982) Crassulacean acid metabolism. In: Hatch MD, Boardman NK (eds) The Biochemistry of Plants, Vol 8. Academic Press, New York, pp. 283–370

    Google Scholar 

  • Paul MJ, Loos K, Stitt M, Ziegler P (1993) Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum. Plant Cell Environ 16: 531–538

    Article  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  PubMed  CAS  Google Scholar 

  • Roblin G, Sakr S, Bonmort J, Delrot S (1998) Regulation of a plant plasma membrane sucrose transporter by phosphorylation. FEBS Lett 424: 165–168

    Article  PubMed  CAS  Google Scholar 

  • Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581: 2309–2317

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schulze W, Weise A, Frommer WB, Ward JM (2000) Function of the cytosolic N-terminus of sucrose transporter AtSUT2 in substrate affinity. FEBS Lett 485: 189–194

    Article  PubMed  CAS  Google Scholar 

  • Smith JAC, Bryce JH (1992) Metabolic compartmentation and transport in CAM plants. In: Tobin A (ed) Plant Organelles: Compartmentation of Metabolism in Photosynthetic Cells. Cambridge University Press, Cambridge, pp. 141–167

    Google Scholar 

  • Taybi T, Nimmo HG, Borland AM (2004) Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes: implications for genotypic capacity and phenotypic plasticity in the expression of Crassulacean acid metabolism. Plant Physiol 135: 587–598

    Article  PubMed  CAS  Google Scholar 

  • Tse YC, Mo BX, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang LW (2004) Identification of multi-vesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16: 672–693

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Walter A, Schurr U (2005) Dynamics of leaf and root growth: endogenous control versus environmental impact. Ann Bot 95: 891–900

    Google Scholar 

  • Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 141: 879–886

    Article  PubMed  CAS  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants – a diversity of roles and complex regulation. Trend Plant Sci 5: 283–290

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zeeman SC, Smith SM, Smith AM (2004) The breakdown of starch in leaves. New Phytol 163: 247–261

    Article  CAS  Google Scholar 

  • Zeeman SC, Delatte T, Messerli G, Umhang M, Stettler M, Mettler T, Streb S, Reinhold H, Kotting O (2007) Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Fun Plant Biol 34: 465–473

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Water Technology Centre for Eastern Region, Chandrasehkarpur, Von-Esmarchstrasse 58, 751023, Bhubangewar, India

    E. Antony

  2. Institute for Research on Environment and Sustainability, Devonshire Building, Newcastle University, NE1 7RU, UK

    A. M. Borland

Authors
  1. E. Antony
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. M. Borland
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. M. Borland .

Editor information

Ulrich Lüttge Wolfram Beyschlag Burkhard Büdel Dennis Francis

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Antony, E., Borland, A.M. (2009). The Role and Regulation of Sugar Transporters in Plants with Crassulacean Acid Metabolism. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany. Progress in Botany, vol 70. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-68421-3_6

Download citation

Publish with us

Policies and ethics

Search

Navigation