Skip to main content
Log in

Fine mapping of fw3.2 controlling fruit weight in tomato

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Tomato (Solanum lycopersicum) is an important crop in the Solanaceae family. One of the key traits selected during domestication is fruit mass which is controlled by many quantitative trait loci. The fruit weight locus fw3.2 is one of the major loci responsible for fruit mass in tomato. Identification of the underlying gene will improve our understanding of the molecular mechanism of fruit development while also providing insights into genes that were selected during domestication. We fine mapped fw3.2 to a 51.4-kb interval corresponding to a region comprising seven candidate genes. Gene action showed that the allele from cultivated tomato was additive to dominant in giving rise to an enlarged fruit. Fruit shape analysis indicated that fw3.2 primarily played a role in controlling fruit weight, with a minor effect on fruit shape. Gene expression and nucleotide diversity were investigated and the likelihood of the genes control fruit mass is discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adamski NM, Anastasiou E, Eriksson S, O’Neill CM, Lenhard M (2009) Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. Proc Natl Acad Sci USA 106:20115–20120

    PubMed  CAS  Google Scholar 

  • Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194

    Article  PubMed  CAS  Google Scholar 

  • Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, Lenhard M (2007) Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13:843–856

    Article  PubMed  CAS  Google Scholar 

  • Aubourg S, Boudet N, Kreis M, Lecharny A (2000) In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol Biol 42:603–613

    Article  PubMed  CAS  Google Scholar 

  • Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–577

    Article  PubMed  CAS  Google Scholar 

  • Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis.The COBRA gene family. Plant Physiol 143:172–187

    Article  PubMed  CAS  Google Scholar 

  • Brewer MT, Moyseenko JB, Monforte AJ, van der Knaap E (2007) Morphological variation in tomato: a comprehensive study of quantitative trait loci controlling fruit shape and development. J Exp Bot 58:1339–1349

    Article  PubMed  CAS  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  PubMed  CAS  Google Scholar 

  • Ching A, Dhugga KS, Appenzeller L, Meeley R, Bourett TM, Howard RJ, Rafalski A (2006) Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls. Planta 224:1174–1184

    Article  PubMed  CAS  Google Scholar 

  • Cong B, Tanksley SD (2006) FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ. Plant Mol Biol 62:867–880

    Article  PubMed  CAS  Google Scholar 

  • Cong B, Liu J, Tanksley SD (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc Natl Acad Sci USA 99:13606–13611

    Article  PubMed  CAS  Google Scholar 

  • Cong B, Barrero LS, Tanksley SD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804

    Article  PubMed  CAS  Google Scholar 

  • Dahan Y, Rosenfeld R, Zadiranov V, Irihimovitch V (2010) A proposed conserved role for an avocado FW2.2-like gene as a negative regulator of fruit cell division. Planta 232:663–676

    Article  PubMed  CAS  Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    Article  PubMed  CAS  Google Scholar 

  • Frary A, Nesbitt TC, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Article  PubMed  CAS  Google Scholar 

  • Gonzalo MJ, van der Knaap E (2008) A comparative analysis into the genetic bases of morphology in tomato varieties exhibiting elongated fruit shape. Theor Appl Genet 116:647–656

    Article  PubMed  Google Scholar 

  • Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987

    Article  CAS  Google Scholar 

  • Guo M, Rupe MA, Dieter JA, Zou J, Spielbauer D, Duncan KE, Howard RJ, Hou Z, Simmons CR (2010) Cell number regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22:1057–1073

    Article  PubMed  CAS  Google Scholar 

  • Hammani K, Gobert A, Hleibieh K, Choulier L, Small I, Giege P (2011) An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23:730–740

    Article  PubMed  CAS  Google Scholar 

  • Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, da Costa e Silva O, Bruce W, Lamkey KR, Wienand U, Schnable PS (2008) The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, van der Knaap E (2011) Tomato fruit weight 11.3 maps close to fasciated on the bottom of chromosome 11. Theor Appl Genet 123:465–474

    Article  PubMed  Google Scholar 

  • Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K, Sato F (2007) Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol 145:668–679

    Article  PubMed  CAS  Google Scholar 

  • Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell 12:1541–1550

    PubMed  CAS  Google Scholar 

  • Kazama T, Ichihashi Y, Murata S, Tsukaya H (2010) The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol 51:1046–1054

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–1458

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003) Brittle culm1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Zhang XC, Govindarajulu M, Qiu J, Ong YT, Brechenmacher L, Berg RH, Hurley-Sommer A, Taylor CG, Stacey G (2010) A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis. Plant J 62:852–864

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Cong B, Tanksley SD (2003) Generation and analysis of an artificial gene dosage series in tomato to study the mechanisms by which the cloned quantitative trait locus fw2.2 controls fruit size. Plant Physiol 132:292–299

    Article  PubMed  CAS  Google Scholar 

  • Miyoshi K, Ahn BO, Kawakatsu T, Ito Y, Itoh J, Nagato Y, Kurata N (2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880

    Article  PubMed  CAS  Google Scholar 

  • Munos S, Ranc N, Botton E, Berard A, Rolland S, Duffe P, Carretero Y, Le Paslier MC, Delalande C, Bouzayen M, Brunel D, Causse M (2011) Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156:2244–2254

    Article  PubMed  CAS  Google Scholar 

  • Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J Exp Bot 58:3841–3852

    Article  PubMed  CAS  Google Scholar 

  • Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638

    Article  PubMed  CAS  Google Scholar 

  • Rao GU, Ben Chaim A, Borovsky Y, Paran I (2003) Mapping of yield-related QTLs in pepper in an interspecific cross of Capsicum annuum and C. frutescens. Theor Appl Genet 106:1457–1466

    PubMed  CAS  Google Scholar 

  • Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis. A new fellowship in expansion. Plant Physiol 130:538–548

    Article  PubMed  CAS  Google Scholar 

  • Salamov AA, Solovyev VV (2000) Ab initio gene finding in drosophila genomic DNA. Genome Res 10:516–522

    Article  PubMed  CAS  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  CAS  Google Scholar 

  • Shchelkunov SN (2010) Interaction of orthopoxviruses with the cellular ubiquitin–ligase system. Virus Genes 41:309–318

    Article  PubMed  CAS  Google Scholar 

  • Sindhu A, Langewisch T, Olek A, Multani DS, McCann MC, Vermerris W, Carpita NC, Johal G (2007) Maize brittle stalk2 encodes a COBRA-like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol 145:1444–1459

    Article  PubMed  CAS  Google Scholar 

  • Small ID, Peeters N (2000) The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed  CAS  Google Scholar 

  • Van der Knaap E, Tanksley SD (2003) The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in yellow stuffer tomato. Theor Appl Genet 107:139–147

    PubMed  Google Scholar 

  • Van der Knaap E, Lippman ZB, Tanksley SD (2002) Extremely elongated tomato fruit controlled by four quantitative trait loci with epistatic interactions. Theor Appl Genet 104:241–247

    Article  Google Scholar 

Download references

Acknowledgments

We thank the members of the Van der Knaap laboratory, in particular Jenny Moyseenko for assistance with greenhouse and field experiments. We thank John Elliot and Lee Duncan for field and greenhouse plant care, respectively. We also thank Dr. Sandy Clifton from Washington University Genome Center for an excellent job on the sequencing of the tomato BAC clone. The research was supported by National Science Foundation grants DBI 0227541 and IOS 0922661.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Esther van der Knaap.

Additional information

Communicated by I. Paran.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2012_1832_MOESM1_ESM.tif

Pedigrees of the materials used in this study. The accession 99T190-94 was an F2 plant from a cross between YS and LA1589. (TIFF 1436 kb)

Supplementary material 2 (XLSX 19.5 kb)

Supplementary material 3 (XLSX 29.0 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, N., Brewer, M.T. & van der Knaap, E. Fine mapping of fw3.2 controlling fruit weight in tomato. Theor Appl Genet 125, 273–284 (2012). https://doi.org/10.1007/s00122-012-1832-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-012-1832-8

Keywords

Navigation