Temporal and spatial expression of hexose transporters in developing tomato (Lycopersicon esculentum) fruit
Stephen J. Dibley A , Michael L. Gear A B , Xiao Yang A , Elke G. Rosche A C , Christina E. Offler A , David W. McCurdy A and John W. Patrick A DA School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia.
B Current address: Office of the Gene Technology Regulator, MDP-54, PO Box 100, Woden, ACT 2606, Australia.
C Current address: Molecular Plant Physiology Group, Research School of Biological Sciences, Australian National University, PO Box 475, Canberra, ACT 2601, Australia.
D Corresponding author. Email: John.Patrick@newcastle.edu.au
Functional Plant Biology 32(9) 777-785 https://doi.org/10.1071/FP04224
Submitted: 30 November 2004 Accepted: 25 May 2005 Published: 26 August 2005
Abstract
Correlative physiological evidence suggests that membrane transport into storage parenchyma cells is a key step in determining hexose levels accumulated in tomato (Lycopersicon esculentum Mill.) fruit (Ruan et al. 1997). Expression of three previously identified hexose transporter genes (LeHT1, 2 and 3) demonstrated that LeHT3, and to a lesser extent LeHT1, are the predominant transporters expressed in young fruit (10 d after anthesis; DAA). Expression of both transporters dropped sharply until 24 DAA, after which only LeHT3 expression remained at detectable levels through to fruit ripening. LeHT2 was not expressed substantially until the onset of fruit ripening. For fruit at both 10 and 30 DAA, LeHT3 transcripts were detected in storage parenchyma cells of the outer pericarp tissue, but not in vascular bundles or the first layer of parenchyma cells surrounding these bundles. In contrast to LeHT gene expression, hexose transporter protein levels were maximal between 20 and 30 DAA, which corresponded to the period of highest hexose accumulation. The delayed appearance of transporter protein is consistent with some form of post-transcriptional regulation. Based on these analyses, LeHT3 appears to be responsible for the rapid hexose accumulation in developing tomato fruit.
Keywords: fruit, gene expression, hexose transporters, membrane transport, tomato, sugar accumulation.
Acknowledgments
This study was supported by an Australian Research Council Grant awarded to JWP and DWMcC. SJD and MLG are grateful for the support of ARC-funded postgraduate scholarships. We thank Louise Hetherington and Dr Xin-Ding Wang for assistance with the in situ hybridisation experiments, Prof. S. Delrot (Université de Poitiers) for the anti-VvHT1 antibody, and Kevin Stokes for glasshouse assistance.
Brown MM,
Hall JL, Ho LC
(1997) Sugar uptake by protoplasts isolated from tomato fruit tissues during various stages of fruit growth. Physiologia Plantarum 101, 533–539.
| Crossref | GoogleScholarGoogle Scholar |
Büttner M,
Truernit E,
Baier K,
Scholz-Starke J,
Sontheim M,
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 |
Carey AT,
Smith DL,
Harrison E,
Bird CR,
Gross KC,
Seymour GB, Tucker GA
(2001) Down-regulation of a ripening-related β-galactosidase gene (TBG1) in transgenic tomato fruits. Journal of Experimental Botany 52, 663–668.
| PubMed |
Chengappa S,
Guilleroux M,
Phillips W, Shields R
(1999) Transgenic tomato plants with decreased sucrose synthase are unaltered in starch and sugar accumulation in the fruit. Plant Molecular Biology 40, 213–221.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
D’Aoust MA,
Yelle S, Nguyen-Quoc B
(1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. The Plant Cell 11, 2407–2418.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Damon S,
Hewitt J,
Nieder M, Bennett AB
(1988) Sink metabolism in tomato fruit. II. Phloem unloading and sugar uptake. Plant Physiology 87, 731–736.
Davies JW, Cocking EC
(1965) Changes in carbohydrates, proteins and nucleic acids during cellular development in tomato fruit locule tissue. Planta 67, 242–253.
| Crossref | GoogleScholarGoogle Scholar |
Delrot S,
Atanassova R, Maurousset L
(2000) Regulation of sugar, amino acid and peptide plant membrane transporters. Biochimica et Biophysica Acta — Biomembranes 1465, 281–306.
| Crossref | GoogleScholarGoogle Scholar |
Droillard M-J,
Rauet-Mayer M-A,
Bureau J-M, Laurière C
(1993) Membrane-associated and soluble lipoxygenase isoforms in tomato pericarp: characterization and involvement in membrane alterations. Plant Physiology 103, 1211–1219.
| PubMed |
Eshed Y, Zamir D
(1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141, 1147–1162.
| PubMed |
Fieuw S, Willenbrink J
(1991) Isolation of protoplasts from tomato fruit (Lycopersicon esculentum): first uptake studies. Plant Science 76, 9–17.
| Crossref | GoogleScholarGoogle Scholar |
Fillion L,
Ageorges A,
Picaud S,
Coutos-Thévenot P,
Lemoine R,
Romieu C, Delrot S
(1999) Cloning and expression of a hexose transporter gene expressed during the ripening of grape berry. Plant Physiology 120, 1083–1093.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fridman E,
Pleban T, Zamir D
(2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proceedings of the National Academy of Sciences USA 97, 4718–4723.
| Crossref | GoogleScholarGoogle Scholar |
Gear ML,
McPhillips ML,
Patrick JW, McCurdy DW
(2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Molecular Biology 44, 687–697.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gillaspy G,
Ben-David H, Gruissem W
(1993) Fruits: a developmental perspective. The Plant Cell 5, 1439–1451.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Physiology 115, 273–282.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grierson, D ,
and
Kader, AA (1986). Fruit ripening and quality. In ‘The tomato crop. A scientific basis for improvement’. pp. 241–280. (Cambridge University Press, Chapman and Hall Ltd: Cambridge, UK)
Harrington GN,
Nussbaumer Y,
Wang X-D,
Tegeder M,
Franceschi VR,
Frommer WB,
Patrick JW, Offler CE
(1997) Spatial and temporal expression of sucrose transport-related genes in developing cotyledons of Vicia faba L. Protoplasma 200, 35–50.
| Crossref | GoogleScholarGoogle Scholar |
Ho, LC ,
and
Hewitt, JD (1986). Fruit development. In ‘The tomato crop. A scientific basis for improvement’. pp. 202–226. (Cambridge University Press, Chapman and Hall Ltd: Cambridge, UK)
Husain SE,
James C,
Shields R, Foyer CH
(2001) Manipulation of fruit sugar composition but not content in Lycopersicon esculentum fruit by introgression of an acid invertase gene from Lycopersicon pimpinellifolium.
New Phytologist 150, 65–72.
| Crossref | GoogleScholarGoogle Scholar |
Johnson C,
Hall JL, Ho LC
(1988) Pathways of uptake and accumulation of sugars in tomato fruit. Annals of Botany 61, 593–603.
Klann EM,
Hall B, Bennett AB
(1996) Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiology 112, 1321–1330.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lashbrook CC,
Gonzalez-Bosch C, Bennett AB
(1994) Two divergent endo-β-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. The Plant Cell 6, 1485–1493.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Milner ID,
Ho LC, Hall JL
(1995) Properties of proton and sugar transport at the tonoplast of tomato (Lycopersicon esculentum) fruit. Physiologia Plantarum 94, 399–410.
| Crossref | GoogleScholarGoogle Scholar |
Mohr WP, Stein M
(1969) Fine structure of fruit development in tomato. Canadian Journal of Plant Science 49, 549–553.
N’Tchobo H,
Dali N,
Nguyen-Quoc B,
Foyer CH, Yelle S
(1999) Starch synthesis in tomato remains constant throughout fruit development and is dependent on sucrose supply and sucrose synthase activity. Journal of Experimental Botany 50, 1457–1463.
| Crossref | GoogleScholarGoogle Scholar |
Offler CE, Horder BE
(1992) The cellular pathway of short distance transfer of photosynthates in developing tomato fruit. Plant Physiology 99, S-41.
Ohyama A,
Ito H,
Sato T,
Nishimura S,
Imai T, Hirai M
(1995) Suppression of acid invertase activity by antisense RNA modifies the sugar composition of the tomato fruit. Plant & Cell Physiology 36, 369–376.
Patrick JW
(1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology and Plant Molecular Biology 48, 191–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Patrick JW, Offler CE
(1996) Post-sieve element transport of photoassimilates in sink regions. Journal of Experimental Botany 47, 1165–1177.
Qi C, Pekala PH
(1999) The influence of mRNA stability on glucose transporter (GLUT1) gene expression. Biochemical and Biophysical Research Communications 263, 265–269.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roitsch T,
Ehness R,
Goetz M,
Hause B,
Hofmann M, Sinha AK
(2000) Regulation and function of extracellular invertase from higher plants in relation to assimilate partitioning, stress responses and sugar signalling. Australian Journal of Plant Physiology 27, 815–825.
Ruan Y-L, Patrick JW
(1995) The cellular pathway of postphloem sugar transport in developing tomato fruit. Planta 196, 434–444.
| Crossref | GoogleScholarGoogle Scholar |
Ruan Y-L,
Patrick JW, Brady CJ
(1997) Protoplast hexose carrier activity is a determinate of genotypic difference in hexose storage in tomato fruit. Plant, Cell & Environment 20, 341–349.
| Crossref | GoogleScholarGoogle Scholar |
Sun J,
Loboda T,
Sung SS, Black CC
(1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiology 98, 1163–1169.
Truernit E,
Stadler R,
Baier K, Sauer N
(1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. The Plant Journal 17, 191–201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Volchuk A,
Narine S,
Foster LJ,
Grabs D,
De Camilli P, Klip A
(1998) Perturbation of dynamin II with an amphiphysin SH3 domain increases GLUT4 glucose transporters at the plasma membrane in 3T3–L1 adipocytes — dynamin II participates in GLUT4 endocytosis. Journal of Biological Chemistry 273, 8169–8176.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walker AJ, Ho LC
(1977) Carbon translocation in the tomato: carbon import and fruit growth. Annals of Botany 41, 813–823.
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 plant cells. The Plant Cell 12, 1345–1355.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yelle S,
Hewitt JD,
Robinson NL,
Damon S, Bennett AB
(1988) Sink metabolism in tomato fruit. III Analysis of carbohydrate assimilation in wild species. Plant Physiology 87, 737–740.
Zhang LY,
Peng YB,
Pelleschi-Travier S,
Fan Y,
Lu YF,
Lu YM,
Gao XP,
Shen YY,
Delrot S, Zhang DP
(2004) Evidence for apoplasmic phloem unloading in developing apple fruit. Plant Physiology 135, 574–586.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
