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Plant function and evolutionary biology
RESEARCH ARTICLE

The high fruit soluble sugar content in wild Lycopersicon species and their hybrids with cultivars depends on sucrose import during ripening rather than on sucrose metabolism

María E. Balibrea A , Cristina Martínez-Andújar A , Jesús Cuartero B , María C. Bolarín C and Francisco Pérez-Alfocea A D
+ Author Affiliations
- Author Affiliations

A Department of Plant Nutrition, CEBAS-CSIC, PO Box 164, E-30100 Murcia, Spain.

B Department of Plant Breeding, EE La Mayora-CSIC, Algarrobo-Costa, E-29750 Málaga, Spain.

C Department of Stress Biology, CEBAS-CSIC, PO Box 164, E-30100 Murcia, Spain.

D Corresponding author. Email: alfocea@cebas.csic.es

Functional Plant Biology 33(3) 279-288 https://doi.org/10.1071/FP05134
Submitted: 6 June 2005  Accepted: 27 October 2005   Published: 2 March 2006

Abstract

Soluble sugar content has been studied in relation to sucrose metabolism in the hexose-accumulating cultivated tomato Lycopersicon esculentum Mill, the wild relative species Lycopersicon cheesmanii Riley, in the sucrose-accumulating wild relative species Lycopersicon chmielewskii Rick, Kesicky, Fobes & Holle. and in two hexose-accumulating interspecific F1 hybrids (L. esculentum × L. cheesmanii; L. esculentum × L. chmielewskii), cultivated under two irrigation regimes (control: EC = 2.1 and saline: EC = 8.4 dS m–1). Under control conditions the total soluble sugar content (as hexose equivalents) in the ripe fruits of L. cheesmanii was 3-fold higher than in L. esculentum, while L. chmielewskii and both F1 hybrids contained twice as much as the cultivar. With the exception of L. esculentum × L. cheesmanii, salinity increased the sugar content by 1.3 (wild species) and 1.7 times (cultivar and L. esculentum × L. chmielewskii) with respect to control fruits. Wild germplasm or salinity provided two different mechanisms for the increases in fruit sugar content. The hexoses accumulated in ripe fruits were strongly influenced by those accumulated at the start of ripening, but the hydrolysed starch before start of ripening only partially explained the final hexose levels and especially the increase under salinity. The early cell wall acid invertase and the late neutral invertase activities appeared to be related to the amount of hexoses accumulated in ripe fruits. However, no metabolic parameter was positively related to the amount of sugar accumulated (including sucrose). The major differences between genotypes appeared in ripe fruits, in which up to 50% of the total amount of sugars accumulated in the wild species (mainly in L. cheesmanii) and hybrids cannot be explained by the sugars accumulated and the starch hydrolysed before the start of ripening stage. As a consequence, the higher fruit quality of the wild species compared with L. esculentum may depend more on the continuation of sucrose import during ripening than on osmotic or metabolic particularities such as the hexose / sucrose-accumulator character or specific enzyme activities.

Keywords: fructose, fruit quality, glucose, invertases, tomato.


Acknowledgments

The authors thank Mr S Hasler and Dr I Dodd for their help in editing the English version of the manuscript, and research assistant Mrs María Rosa Rojo for her efficient technical assistance. Research supported by CICYT-FEDER (Spain), project AGL01-1530. The authors dedicate this paper to the memory of the late Professors Manuel Caro (CEBAS-CSIC, Spain) and Gilles Guerrier (Université d’Orléans, France).


References


Azanza F, Kim D, Tanksley SD, Juvik JA (1995) Genes from Lycopersicon chmielewskii affecting tomato quality during fruit ripening. Theoretical and Applied Genetics 91, 495–504.
Crossref | GoogleScholarGoogle Scholar | open url image1

Balibrea ME, Cayuela E, Artés F, Pérez-Alfocea F (1997) Salinity effects on some postharvest quality factors in a commercial tomato hybrid. Journal of Horticultural Science 72, 885–892. open url image1

Balibrea ME, Parra M, Bolarín MC, Pérez-Alfocea F (1999) Cytoplasmic sucrolytic activity controls tomato fruit growth under salinity. Australian Journal of Plant Physiology 26, 561–568. open url image1

Balibrea ME, Cuartero J, Bolarín MC, Pérez-Alfocea F (2003) Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity. Physiologia Plantarum 118, 38–46.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baxter CJ, Carrari F, Bauke A, Overy S, Hill SA, Quick PW, Fernie AR, Sweetlove LJ (2005a) Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant & Cell Physiology 46, 425–437.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baxter CJ, Sabar M, Quick PW, Sweetlove LJ (2005b) Comparison of changes in fruit gene expression in tomato introgression lines provides evidence of genome-wide transcriptional changes and reveals links to mapped QTLs and described traits. Journal of Experimental Botany 56, 1591–1604.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Causse M, Duffe P, Gómez MC, Buret M, Damidaux R, Zamir D, Gur A, Chevalier C, Lemarie-Chamley M, Rothan C (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. Journal of Experimental Botany 55, 1671–1685.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chetelat RT, De Verna JW, Bennett AB (1995) Introgression into tomato (Lycopersicon esculentum) of the L. chmielewskii sucrose accumulator gene (sucr) controlling fruit sugar composition. Theoretical and Applied Genetics 91, 327–333. open url image1

D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit settting and the sucrose unloading capacity of young fruits. The Plant Cell 11, 2407–2418.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dibley S, Gear ML, Yang X, Rosche EG, Offler CE, McCurdy DW, Patrick JW (2005) Temporal expression of hexose transporters in developing tomato (Lycopersicon esculentum) fruit. Functional Plant Biology 32, 777–785.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dinar M, Stevens MA (1981) The relationship between starch accumulation and soluble solids content of tomato fruits. Journal of the American Society for Horticultural Science 106, 415–418. open url image1

Doehlert D, Felker F (1987) Characterization and distribution of invertase activity in developing maize (Zea mays) kernels. Physiologia Plantarum 70, 51–57. open url image1

Ehret DL, Ho LC (1986) The effects of salinity on dry matter partitioning and fruit growth in tomatoes grown in nutrient film culture. Journal of Horticultural Science 61, 361–367. open url image1

Eshed Y, Zamir D (1994) Introgressions from Lycopersicon pennellii can improve the soluble solids yield of tomato hybrids. Theoretical and Applied Genetics 88, 891–897.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | open url image1

Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305, 1786–1789.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garvey TC, Hewitt JD (1991) Starch and sugar accumulation in two accessions of Lycopersicon cheesmanii. Journal of the American Society for Horticultural Science 116, 77–79. open url image1

Garvey TC, Hewitt JD (1992) Use of molecular markers to locate quantitative trait loci linked to high soluble solids content in a hybrid of Lycopersicon cheesmanii. Journal of the American Society for Horticultural Science 113, 497–499. open url image1

Gayler KR, Glasziou KT (1972) Physiological functions of acid and neutral invertases in growth and sugar storage in sugar cane. Plant Physiology 27, 25–31. open url image1

Guis M, Botondi R, Ben-Amor M, Ayub R, Bouzayen M, Pech JC, Latché A (1997) Ripening-associated biochemical traits of cantaloupe charentais melons expressing an antisense ACC oxidase transgene. Journal of the American Society for Horticultural Science 122, 748–751. open url image1

Harada S, Fukuta S, Tanaka H, Ishiguro Y, Sato T (1995) Genetic analysis of the trait of sucrose accumulation in tomato fruit using molecular marker. Breeding Science 45, 429–434. open url image1

Hewitt, JD ,  and  Garvey, TC (1987). Wild sources of high soluble solids in tomato. In ‘Tomato biotechnology’. pp. 45–54. (Alan R. Liss, Inc.: New York)

Ho LC (1996a) The mechanism of assimilate partitioning and carbohydrate compartmentation in fruit in relation to the quality and yield of tomato. Journal of Experimental Botany 47, 1239–1244. open url image1

Ho, LC (1996b). Tomato. In ‘Photoassimilate distribution in plants and crops. Source–sink relationships’. b. pp. 709–728. (Marcel Dekker, Inc.: New York)

Husain SE, ap Rees T, Shields R, Foyer CH (1999) The role of invertase in carbohydrate metabolism of tomato fruit. Acta Horticulturae 487, 77–84. open url image1

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 | open url image1

Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiology 103, 863–870.
PubMed |
open url image1

Klann EM, Hall B, Bennett AB (1996) Antisense acid invertases (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiology 112, 1321–1330.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235–246.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McCollum JP, Skok J (1960) Radiocarbon studies on the translocation of organic constituents into ripening tomato fruits. Proceedings of American Society for Horticultural Science 75, 611–616. open url image1

Miron D, Schaffer AA (1991) Sucrose phosphate synthase, sucrose synthase, and invertase activities in developing fruit of Lycopersicon hirsutum Humb. and Bonpl. Plant Physiology 95, 623–627. open url image1

Nguyen-Quoc B, Foyer C (2001) A role for futile cycles involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. Journal of Experimental Botany 52, 881–889.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 | open url image1

Paterson AH, De Verna JW, Lanini B, Tanksley SD (1990) Fine mapping of quantitative trait loci using selective overlapping recombinant chromosomes in an interspecies cross of tomato. Genetics 124, 735–742.
PubMed |
open url image1

Pérez-Alfocea F, Balibrea ME, Bolarín MC, Cuartero J (1997) Efecto de la salinidad sobre el rendimiento y la calidad del fruto en Lycopersicon esculentum, L. pimpinellifolium y en sus híbridos interespecíficos. Actas de Horticultura 16, 243–247. open url image1

Petersen KK, Willumsen J, Kaack K (1998) Composition and taste of tomatoes as affected by increased salinity and different salinity sources. Journal of Horticultural Science & Biotechnology 73, 205–215. open url image1

Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9, 606–613.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. open url image1

Ruan YL, Patrick JW (1995) The cellular pathway of post-phloem sugar transport in developing tomato fruit. Planta 196, 434–444.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schaffer AA, Petreikov M (1997) Sucrose metabolism in young tomato fruit undergoing transient sucrose to starch metabolism. Plant Physiology 113, 739–746.
PubMed |
open url image1

Schaffer AA, Petreikov M, Miron D, Fogelman M, Spiegelman M , et al. (1999) Modification of carbohydrate content in developing tomato fruit. HortScience 34, 1024–1027. open url image1

Stevens MA, Rudich J (1978) Genetic potential for overcoming physiological limitation on adaptability, yield and quality in the tomato. HortScience 13, 673–678. open url image1

Stommel JR (1992) Enzymatic components of sucrose accumulation in the wild tomato species Lycopersicon peruvianum. Plant Physiology 99, 324–328. open url image1

Stommel JR, Haynes KG (1993) Genetic control of fruit sugar accumulation in a Lycopersicon esculentum × L. hirsutum cross. Journal of the American Society for Horticultural Science 118, 859–863. open url image1

Sun JS, Loboda T, Sung SS, Black CC (1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiology 98, 1163–1169. open url image1

Wang F, Sanz A, Brenner ML, Smith A (1993) Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiology 101, 321–327.
PubMed |
open url image1

Yelle S, Hewitt JD, Robinson NL, Damon S, Bennett AB (1988) Sink metabolism in tomato fruit. III. Analysis of carbohydrate assimilation in a wild species. Plant Physiology 87, 737–740. open url image1

Yelle S, Chetelat RT, Dorais M, DeVerna JW, Bennett AB (1991) Sink metabolism in tomato fruit. IV. Genetic and biochemical analysis of sucrose accumulation. Plant Physiology 95, 1026–1035. open url image1

Young TE, Juvik JA, Sullivan JG (1993) Accumulation of the components of total solids in ripening fruits of tomato. Journal of the American Society for Horticultural Science 118, 286–292. open url image1