Histological and molecular investigation of the basis for variation in tomato fruit size in response to fruit load and genotype
Julienne Fanwoua A B C F , Pieter H. B. de Visser A , Ep Heuvelink B , Gerco Angenent D E , Xinyou Yin C , Leo F. M. Marcelis A B and Paul C. Struik C
+ Author Affiliations
- Author Affiliations
A Wageningen UR Greenhouse Horticulture, PO Box 644, 6700 AP Wageningen, The Netherlands.
B Horticultural Supply Chains, Wageningen University, PO Box 630, 6700 AP Wageningen, The Netherlands.
C Centre for Crop Systems Analysis, Wageningen University, PO Box 430, 6700 AK Wageningen, The Netherlands.
D Plant Research International, Business Unit Bioscience, PO Box 16, 6700 AA Wageningen, The Netherlands.
E Centre for BioSystems Genomics (CBSG), PO Box 16, 6700 AA Wageningen, The Netherlands.
F Corresponding author. Email: julienne.fanwoua@wur.nl
Functional Plant Biology 39(9) 754-763 https://doi.org/10.1071/FP12093
Submitted: 22 March 2012 Accepted: 10 July 2012 Published: 15 August 2012
Abstract
Understanding the molecular mechanisms and cellular dynamics that cause variation in fruit size is critical for the control of fruit growth. The aim of this study was to investigate how both genotypic factors and carbohydrate limitation cause variation in fruit size. We grew a parental line (Solanum lycopersicum L.) and two inbred lines from Solanum chmielewskii (C.M.Rick et al.; D.M.Spooner et al.) producing small or large fruits under three fruit loads (FL): continuously two fruits/truss (2&2F) or five fruits/truss (5&5F) and a switch from five to two fruits/truss (5&2F) 7 days after anthesis (DAA). Final fruit size, sugar content and cell phenotypes were measured. The expression of major cell cycle genes 7 DAA was investigated using quantitative PCR. The 5&5F treatment resulted in significantly smaller fruits than the 5&2F and 2&2F treatments. In the 5&5F treatment, cell number and cell volume contributed equally to the genotypic variation in final fruit size. In the 5&2F and 2&2F treatment, cell number contributed twice as much to the genotypic variation in final fruit size than cell volume did. FL treatments resulted in only subtle variations in gene expression. Genotypic differences were detected in transcript levels of CycD3 (cyclin) and CDKB1 (cyclin-dependent-kinase), but not CycB2. Genotypic variation in fruit FW, pericarp volume and cell volume was linked to pericarp glucose and fructose content (R2 = 0.41, R2 = 0.48, R2 = 0.11 respectively). Genotypic variation in cell number was positively correlated with pericarp fructose content (R2 = 0.28). These results emphasise the role of sugar content and of the timing of assimilate supply in the variation of cell and fruit phenotypes.
Additional keywords: assimilates, cell cycle genes, histology, Solanum lycopersicum, variety.
References
Anastasiou E, Lenhard M (2008) Control of plant organ size. In ‘Plant growth signaling’. (Eds L Bögre, G Beemster) pp. 25–45. (Springer: Berlin)Archdeacon TJ (1994) ‘Correlation and regression analysis: a historian’s guide.’ (University of Wisconsin Press: Madison, WI)
Baldet P, Devaux C, Chevalier C, Brouquisse R, Just D, Raymond P (2002) Contrasted responses to carbohydrate limitation in tomato fruit at two stages of development. Plant, Cell & Environment 25, 1639–1649.
| Contrasted responses to carbohydrate limitation in tomato fruit at two stages of development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislCjtg%3D%3D&md5=ecd32d91223b5fa8f5c94bc690e7ebecCAS |
Baldet P, Hernould M, Laporte F, Mounet F, Just D, Mouras A, Chevalier C, Rothan C (2006) The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants. Journal of Experimental Botany 57, 961–970.
| The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVOqt7s%3D&md5=37c569b7308198a54ff3d70fa5c55ae1CAS |
Bertin N (2005) Analysis of the tomato fruit growth response to temperature and plant fruit load in relation to cell division, cell expansion and DNA endoreduplication. Annals of Botany 95, 439–447.
| Analysis of the tomato fruit growth response to temperature and plant fruit load in relation to cell division, cell expansion and DNA endoreduplication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVamtrc%3D&md5=a397027551bea7f86689795fbe936033CAS |
Bertin N, Borel C, Brunel B, Cheniclet C, Causse M (2003) Do genetic make-up and growth manipulation affect tomato fruit size by cell number, or cell size and DNA endoreduplication? Annals of Botany 92, 415–424.
| Do genetic make-up and growth manipulation affect tomato fruit size by cell number, or cell size and DNA endoreduplication?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szptlWrsQ%3D%3D&md5=aea7cce5ab83740c0cbe74679b4aeb4bCAS |
Bertin N, Lecomte A, Brunel B, Fishman S, Génard M (2007) A model describing cell polyploidization in tissues of growing fruit as related to cessation of cell proliferation. Journal of Experimental Botany 58, 1903–1913.
| A model describing cell polyploidization in tissues of growing fruit as related to cessation of cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeisL0%3D&md5=c4d734f086b7454ed54b70d1ecb8c087CAS |
Bohner J, Bangerth F (1988a) Cell number, cell size and hormone levels in semi-isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size. Physiologia Plantarum 72, 316–320.
| Cell number, cell size and hormone levels in semi-isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1CrurY%3D&md5=948f6c2de1a4a91c59c38aa8116c952fCAS |
Bohner J, Bangerth F (1988b) Effects of fruit set sequence and defoliation on cell number, cell size and hormone levels of tomato fruits (Lycopersicon esculentum Mill.) within a truss. Plant Growth Regulation 7, 141–155.
Bourdon M, Frangne N, Mathieu-Rivet E, Nafati M, Cheniclet C, Renaudin JP, Chevalier C (2010) Endoreduplication and growth of fleshy fruits. In ‘Progress in botany 71’. (Eds U Lüttge, W Beyschlag, B Büdel, D Francis) pp. 101–132. (Springer: Berlin)
Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiology 139, 1984–1994.
| Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlGmsbzM&md5=d0ad138fbff8f0fadfa027436749f71aCAS |
Chevalier C (2007) Cell cycle control and fruit development. In ‘Cell cycle control and plant development’. (Ed. D Inzé) pp. 269–293. (Blackwell Publishing: Oxford)
de Koning ANM (1994) Development and dry matter distribution in glasshouse tomato: a quantitative approach. PhD thesis, Wageningen University, The Netherlands.
Do PT, Prudent M, Sulpice R, Causse M, Fernie AR (2010) The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiology 154, 1128–1142.
| The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2ntr7N&md5=75f4c8c70297db5c08790f29da45da93CAS |
Doerner P (2008) Signals and mechanisms in the control of plant growth. In ‘Plant growth signaling’. (Eds L Bögre, G Beemster) pp. 1–23. (Springer: Berlin)
Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE (1993) Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Molecular Biology 21, 515–524.
| Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Oit7o%3D&md5=82168030b628ec3888c6fe218ccb4baeCAS |
Expósito-Rodríguez M, Borges A, Borges-Pérez A, Pérez J (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biology 8, 131–143.
| Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process.Crossref | GoogleScholarGoogle Scholar |
Francis D (2007) The plant cell cycle 15 years on. New Phytologist 174, 261–278.
| The plant cell cycle 15 years on.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls12ltb4%3D&md5=6286e9cf1e5363a1f185ac147be0a6e1CAS |
Génard M, Bertin N, Borel C, Bussières P, Gautier H, Habib R, Léchaudel M, Lecomte A, Lescourret F, Lobit P, Quilot B (2007) Towards a virtual fruit focusing on quality: modelling features and potential uses. Journal of Experimental Botany 58, 917–928.
| Towards a virtual fruit focusing on quality: modelling features and potential uses.Crossref | GoogleScholarGoogle Scholar |
Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. The Plant Cell 5, 1439–1451.
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. The Plant Cell 16, S170–S180.
| Genetic regulation of fruit development and ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWltb8%3D&md5=8e0af5a01d52fab5fc36bd9160fff543CAS |
Hajjaj H, Blanc PJ, Goma G, François J (1998) Sampling techniques and comparative extraction procedures for quantitative determination of intra- and extracellular metabolites in filamentous fungi. FEMS Microbiology Letters 164, 195–200.
| Sampling techniques and comparative extraction procedures for quantitative determination of intra- and extracellular metabolites in filamentous fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFKnsb8%3D&md5=c30fd151e54727138dce3b2ec96f8668CAS |
Heuvelink E (2005) Developmental processes. In ‘Tomatoes’. (Ed. E Heuvelink) pp. 53–83. (CABI Publishing: Oxfordshire)
Higashi K, Hosoya K, Ezura H (1999) Histological analysis of fruit development between two melon (Cucumis melo L. reticulatus) genotypes setting a different size of fruit. Journal of Experimental Botany 50, 1593–1597.
Ho LC (1992) Fruit growth and sink strength. In ‘Fruit and seed production. Aspects of development, environmental physiology and ecology’. (Eds C Marshall, J Grace) pp. 101–124. (Cambridge University Press: Cambridge)
Joubès J, Walsh D, Raymond P, Chevalier C (2000) Molecular characterization of the expression of distinct classes of cyclins during the early development of tomato fruit. Planta 211, 430–439.
| Molecular characterization of the expression of distinct classes of cyclins during the early development of tomato fruit.Crossref | GoogleScholarGoogle Scholar |
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.
| Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntVags78%3D&md5=b96154ad81049b1c4b353d5521b2dd31CAS |
Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? Current Opinion in Plant Biology 3, 488–492.
| Plant cell-size control: growing by ploidy?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FmtFaquw%3D%3D&md5=507fbb5f84c9622e5175acb2d2bdfde2CAS |
Kultur F, Harrison HC, Staub JE, Palta JP (2001) Spacing and genotype affect fruit sugar concentration, yield, and fruit size of muskmelon. HortScience 36, 274–278.
Kwon HK, Wang MH (2011) The D-type cyclin gene (Nicta;CycD3;4) controls cell cycle progression in response to sugar availability in tobacco. Journal of Plant Physiology 168, 133–139.
| The D-type cyclin gene (Nicta;CycD3;4) controls cell cycle progression in response to sugar availability in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2jurvJ&md5=e2e902fcd5ec113c584d347e379218b6CAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=86e5fd6e2b10f00206b12a43a671f6c8CAS |
Luengwilai K, Fiehn OE, Beckles DM (2010) Comparison of leaf and fruit metabolism in two tomato (Solanum lycopersicum L.) genotypes varying in total soluble solids. Journal of Agricultural and Food Chemistry 58, 11790–11800.
| Comparison of leaf and fruit metabolism in two tomato (Solanum lycopersicum L.) genotypes varying in total soluble solids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGkt7vN&md5=8b4ff1b3467de4bb5869c461ccfb7e38CAS |
Marcelis LFM (1993) Effect of assimilate supply on the growth of individual cucumber fruits. Physiologia Plantarum 87, 313–320.
| Effect of assimilate supply on the growth of individual cucumber fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVGjtrg%3D&md5=b9eca12a1eb07d5f025e4c0006f0c0adCAS |
Massot C, Génard M, Stevens R, Gautier H (2010) Fluctuations in sugar content are not determinant in explaining variations in vitamin C in tomato fruit. Plant Physiology and Biochemistry 48, 751–757.
| Fluctuations in sugar content are not determinant in explaining variations in vitamin C in tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVersbrO&md5=db893effe6f6dc30e08854db1a64bd50CAS |
Prudent M, Causse M, Génard M, Tripodi P, Grandillo S, Bertin N (2009) Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection. Journal of Experimental Botany 60, 923–937.
| Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSmtrs%3D&md5=e694fd11a2d87219af7457689c2ea48dCAS |
Prudent M, Bertin N, Génard M, Munos S, Rolland S, Garcia V, Petit J, Baldet P, Rothan C, Causse M (2010) Genotype-dependent response to carbon availability in growing tomato fruit. Plant, Cell & Environment 33, 1186–1204.
Richings EW, Cripps RF, Cowan AK (2000) Factors affecting ‘Hass’ avocado fruit size: carbohydrate, abscisic acid and isoprenoid metabolism in normal and phenotypically small fruit. Physiologia Plantarum 109, 81–89.
| Factors affecting ‘Hass’ avocado fruit size: carbohydrate, abscisic acid and isoprenoid metabolism in normal and phenotypically small fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs1GgsLo%3D&md5=2ae1b41a55246df8e9661edbac2a52d2CAS |
Riou-Khamlichi C, Menges M, Healy JMS, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Molecular and Cellular Biology 20, 4513–4521.
| Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksVOjtLk%3D&md5=9c8ca987d5a9fdd2fc6530d4d1e715f2CAS |
Smith AM (1988) Major differences in isoforms of starch-branching enzyme between developing embryos of round- and wrinkled-seeded peas (Pisum sativum L.). Planta 175, 270–279.
| Major differences in isoforms of starch-branching enzyme between developing embryos of round- and wrinkled-seeded peas (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlt1Kjs78%3D&md5=3794edbebb76b2ae1279b62f78c76803CAS |
Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. The Plant Cell 16, S181–S189.
| The genetic, developmental, and molecular bases of fruit size and shape variation in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWltbw%3D&md5=1ee6432d5c5181c79cf827f6e44e14b4CAS |
Vlieghe K, Inzé D, De Veylder L (2007) Physiological relevance and molecular control of the endocycle in plants. In ‘Cell cycle control and plant development’. (Ed. D Inzé) pp. 227–248. (Blackwell Publishing: Oxford)
Yin X, Struik PC, Kropff MJ (2004) Role of crop physiology in predicting gene-to-phenotype relationships. Trends in Plant Science 9, 426–432.
| Role of crop physiology in predicting gene-to-phenotype relationships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVOjt70%3D&md5=73ed4c0985b5393ad61c638ef222e598CAS |
Zhang C, Tanabe K, Wang S, Tamura F, Yoshida A, Matsumoto K (2006) The impact of cell division and cell enlargement on the evolution of fruit size in Pyrus pyrifolia. Annals of Botany 98, 537–543.
| The impact of cell division and cell enlargement on the evolution of fruit size in Pyrus pyrifolia.Crossref | GoogleScholarGoogle Scholar |
