Hexose uptake by developing cotyledons of Vicia faba: physiological evidence for transporters of differing affinities and specificities
Gregory N. Harrington A B , Katherine E. Dibley A , Raymond J. Ritchie C , Christina E. Offler A and John W. Patrick A DA School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia.
B Present address: Department of Integrated Natural Sciences, Arizona State University, at the West campus, Glendale, AZ 85306, USA.
C Biology A-08, University of Sydney, Sydney, NSW 2006, Australia.
D Corresponding author. Email: john.patrick@newcastle.edu.au
Functional Plant Biology 32(11) 987-995 https://doi.org/10.1071/FP05081
Submitted: 4 April 2005 Accepted: 31 May 2005 Published: 28 October 2005
Abstract
Cotyledons of broad bean (Vicia faba L.) develop in an apoplasmic environment that shifts in composition from one dominated by hexoses to one dominated by sucrose. During the latter phase of development, sucrose / H+ symporter activity and expression is restricted to cotyledon epidermal transfer cell complexes that support sucrose fluxes that are 8.5-fold higher than those exhibited by the storage parenchyma. In contrast, the flux difference between these cotyledon tissues is only 1.7-fold for hexoses. Glucose and fructose uptake was shown to be sensitive to PCMBS and phloridzin, both of which slow H+-sugar transport. A low Km (or high affinity transporter, HAT) mechanism transports glucose and glucose-analogues exclusively. No HAT system for fructose could be found. A high Km (low affinity transporter, LAT) mechanism transports a broader range of hexoses, including glucose and fructose. Consistent with glucose and fructose transport being H+-coupled, their uptake was inhibited by dissipating the proton motive force (pmf) by treating cotyledons with carbonyl cyanide m-chlorophenol hydrazone, propionic acid or tetraphenylphosphonium ion. Erythrosin B inhibited hexose uptake, indicating a role for the P-type H+-ATPase in establishing the pmf. It is concluded that H+-coupled glucose and fructose transport mechanisms occur at plasma membranes of dermal transfer cell complexes and storage parenchyma cells. These transport mechanisms are active during pre- and storage phases of cotyledon development. However, hexose symport only makes a quantitative contribution to cotyledon biomass gain during the pre-storage stage of development.
Keywords: fructose; glucose; hexose; plasma membrane transport; seed development; Vicia faba cotyledons.
Acknowledgments
This study was supported by a large Australian Research Council grant awarded to JWP and CEO. GNH is grateful for the support offered by an Australian Postgraduate Research Award. We are indebted to Louise Hetherington for technical assistance and Mr Kevin Stokes for a continuous supply of healthy plant material.
Beffagna N, Romani G
(1988) Effects of two plasmalemma ATPase inhibitors on H+ extrusion and intracellular pH in Elodea densa leaves. Journal of Experimental Botany 39, 1033–1043.
Borisjuk L,
Rolletschek H,
Wobus U, Weber H
(2003) Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. Journal of Experimental Botany 54, 503–512.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Buckhout, TJ ,
and
Tübbe, A (1996). Structure, mechanisms of catalysis, and regulation of sugar transporters in plants. In ‘Photoassimilate distribution in plants and crops: source–sink relationships’ pp. 229–260. (Marcel Dekker Inc.: New York)
Bush DR
(1993) Inhibitors of the proton–sucrose symport. Archives of Biochemistry and Biophysics 307, 355–360.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Büttner M, Sauer N
(2000) Monosaccharide transporters in plants: structure function and physiology. Biochimica et Biophysica Acta 1465, 263–274.
| PubMed |
Büttner M,
Truernit E,
Baier K,
Scholz-Starke J,
Sontheim M,
Lauterbach C,
Huss VAR, Sauer N
(2000) AtSTP3, a green leaf-specific, low affinity monosaccharide-H+ symporter of Arabidopsis thaliana. Plant, Cell & Environment 23, 175–184.
| Crossref | GoogleScholarGoogle Scholar |
Cameron-Mills V, Duffus CM
(1979) Hexose transport in isolated barley embryos. Annals of Botany 44, 485–494.
Darussalam
,
Cole MA, Patrick JW
(1998) Auxin control of photoassimilate transport to and within developing grains of wheat. Australian Journal of Plant Physiology 25, 69–77.
Diettrich B, Keller F
(1991) Carbohydrate transport in discs of storage parenchyma of celery petioles: I. Uptake of glucose and fructose. New Phytologist 117, 413–422.
Harrington GN
(2000) Plasma membrane transport of photoassimilates in developing cotyledons of Vicia faba L.: pathways, mechanisms and regulation. PhD Thesis
(The University of Newcastle:
Australia)
Harrington GN,
Franceschi VR,
Offler CE,
Patrick JW,
Tegeder M,
Frommer WB,
Harper JF, Hitz WD
(1997a) Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Vicia faba seed. Protoplasma 197, 160–173.
| Crossref | GoogleScholarGoogle Scholar |
Harrington GN,
Nussbaumer Y,
Wang X-D,
Tegeder M,
Franceschi VR,
Frommer WB,
Patrick JW, Offler CE
(1997b) Spatial and temporal expression of sucrose transport-related genes in developing cotyledons of Vicia faba L. Protoplasma 200, 35–50.
| Crossref | GoogleScholarGoogle Scholar |
Lalonde S,
Wipf D, Frommer WB
(2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology 55, 341–372.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Leterrier M,
Atanassova R,
Laquitaine L,
Gaillard C,
Coutos-Thévenot P, Delrot S
(2003) Expression of a putative grapevine hexose transporter in tobacco alters morphogenesis and assimilate partitioning. Journal of Experimental Botany 54, 1193–1204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McDonald R
(1991) Transfer cells and sugar transport in the developing cotyledon of Vicia faba L. PhD Thesis
(The University of Newcastle:
Australia)
McDonald R,
Wang HL,
Patrick JW, Offler CE
(1995) Cellular pathway of sucrose transport in developing cotyledons of Vicia faba L. and Phaseolus vulgaris L. A physiological assessment. Planta 196, 659–667.
| Crossref | GoogleScholarGoogle Scholar |
McDonald R,
Fieuw S, Patrick JW
(1996a) Sugar uptake by the dermal transfer cells of developing cotyledons of Vicia faba L. 1. Experimental systems and general transport properties. Planta 198, 54–63.
McDonald R,
Fieuw S, Patrick JW
(1996b) Sugar uptake by the dermal transfer cells of developing cotyledons of Vicia faba L. II. Mechanism of energy coupling. Planta 198, 502–509.
Murray, DR (1988).
Offler CE,
Liet E, Sutton EG
(1997) Transfer cell induction in cotyledons of Vicia faba L. Protoplasma 200, 51–64.
| Crossref | GoogleScholarGoogle Scholar |
Patrick, JW ,
van Bel, AJE ,
and
Offler, CE (2003). Seed development — nutrient loading. In ‘Encyclopedia of applied plant sciences’. pp. 1240–1249. (Academic Press: London)
Penning de Vries, FWT (1975). Use of assimilates in higher plants. In ‘Photosynthesis and productivity in different environments’. pp. 459–480. (Cambridge University Press: London)
Rausch T
(1991) The hexose transporters at the plasma membrane and the tonoplast of higher plants. Physiologia Plantarum 82, 134–142.
| Crossref | GoogleScholarGoogle Scholar |
Ritchie R,
Fieuw-Makaroff S, Patrick JW
(2003) Sugar retrieval by coats of developing seeds of Phaseolus vulgaris L. and Vicia faba L. Plant & Cell Physiology 44, 163–172.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ross HA, Davies HV
(1992) Purification and characterization of sucrose synthase from the cotyledons of Vicia faba L. Plant Physiology 100, 1008–1013.
Sherson SM,
Hemmann G,
Wallace G,
Forbes S,
Germain V,
Stadler R,
Bechtold N,
Sauer N, Smith SM
(2000) Monosaccharide / proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. The Plant Journal 24, 849–857.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Slone JH,
Buckhout TJ, VanDerWoude WJ
(1991) Symport of proton and sucrose in plasma membrane vesicles isolated from spinach leaves. Plant Physiology 96, 615–618.
Thomas PA,
Felker FC, Crawford CG
(1992) Sugar uptake and metabolism in the developing endosperm of Tassel-seed Tunicat (Ts-5Tu). Plant Physiology 99, 1540–1546.
Weber H,
Borisjuk L,
Heim U,
Buchner P, Wobus U
(1995) Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell-type specific expression. The Plant Cell 7, 1835–1846.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weber H,
Borisjuk L,
Heim U,
Sauer N, Wobus U
(1997) A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seed. The Plant Cell 9, 895–908.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weschke W,
Panitz R,
Gubatz S,
Wang Q,
Radchuk R,
Weber H, Wobus U
(2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. The Plant Journal 33, 395–411.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xia J-H, Saglio PH
(1988) Characterisation of the hexose transport system in maize root tips. Plant Physiology 88, 1015–1020.
