Skip to main content
SpringerLink
Log in

Identification of Solanum habrochaites loci that quantitatively influence tomato fruit ripening-associated ethylene emissions

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

Abstract

The phytohormone ethylene is essential for ripening of climacteric fruits such as tomato. While many of the genes responsible for ethylene synthesis and perception have been identified, the regulatory network controlling autocatalytic climacteric ethylene synthesis is not well understood. In order to better understand the regulation of ripening-associated ethylene, we have exploited the genetic variation within Solanum Sect. Lycopersicon. In particular, we have used a near-isogenic population of S. habrochaites introgression lines to identify chromosome segments affecting ethylene emissions during ripening. S. habrochaites fruits produce much larger quantities of ethylene during ripening than do cultivated S. lycopersicum tomatoes. A total of 17 segments were identified; 3 had emissions more than twice the level of the tomato parent, 11 had less than a twofold increase and 3 had significantly reduced emissions at one or more ripening stages. While several of these segments co-segregate with known ethylene-related genes, many do not correspond to known genes. Thus, they may identify novel modes of regulation. These results illustrate the utility of wild relatives and their introgression lines to understand regulation of fruit ripening-related processes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Regul 26:143–159

    Article  CAS  Google Scholar 

  • Barry C, Blume B, Bouzayen M, Cooper W, Hamilton A, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9:525–535

    Article  PubMed  CAS  Google Scholar 

  • Bernacchi D, Tanksley SD (1997) An interspecific backcross of Lycopersicon esculentum × L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147:861–877

    PubMed  CAS  Google Scholar 

  • Bernacchi D, Beck-Bunn T, Eshed J, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley SD (1998) Advanced backcross QTL analysis of tomato. I. Identification of QTLs for traits of agronomic importance from Lycopersicon hirsutum. Theor Appl Genet 97:381–397

    Article  CAS  Google Scholar 

  • Cameron AC, Fenton CAL, Yu YB, Adams DO, Yang SF (1979) Increased production of ethylene by plant tissues treated with l-aminocyclopropane-l-carboxylic acid. Hortscience 14:178–180

    CAS  Google Scholar 

  • Causse M, Chaıb J, Lecomte L, Buret M, de′ric Hospital F (2007) Both additivity and epistasis control the genetic variation for fruit quality traits in tomato. Theor Appl Genet 115:429–442

    Article  PubMed  CAS  Google Scholar 

  • Dal Cin V, Galla G, Ramina A (2007) MdACO expression during abscission: the use of 33P labeled primers in transcript quantitation. Mol Biotechnol 36:9–13

    Article  PubMed  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

  • Foolad MR, Zhang LP, Khan AA, Ni˜no-Liu D, Lin GY (2002) Identification of QTLs for early blight (Alternaria solani) resistance in tomato using backcross populations of a Lycopersicon esculentum Xl. hirsutum cross. Theor Appl Genet 104:945–958

    Article  PubMed  CAS  Google Scholar 

  • Frary A, Fritz LA, Tanksley SD (2004) A comparative study of the genetic bases of natural variation in tomato leaf, sepal, and petal morphology. Theor Appl Genet 109:523–533

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fulton T, van der Hoeven R, Eannetta N, Tanksley S (2002) Identification, analysis and utilization of a conserved ortholog set (COS) markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Giegerich R, Meyer F, Schleiermacher C (1996) GeneFisher: software support for the detection of postulated genes. Proc Int Conf Intell Syst Mol Biol 4:68–77

    PubMed  CAS  Google Scholar 

  • Giovannoni J, Yen H, Shelton B, Miller S, Kannan P, Vrebalov J, Tieman D, Hackett R, Grierson D, Klee H (1999) Genetic mapping of ripening and ethylene-related loci in tomato. Theor Appl Genet 98:1005–1013

    Article  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, Tanksley SD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92:935–951

    Article  CAS  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 

  • Grumet R, Fobes J, Herner R (1981) Ripening behavior of wild tomato species. Plant Physiol 68:1428–1432

    Article  PubMed  CAS  Google Scholar 

  • Hovav R, Chehanovsky N, Moy M, Jetter R, Schaffer AA (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J 52:627–639

    Article  PubMed  CAS  Google Scholar 

  • Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3:1187–1194

    Article  PubMed  CAS  Google Scholar 

  • Lippman Z, Tanksley SD (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics 158:413–422

    PubMed  CAS  Google Scholar 

  • Liu YS, Gur A, Ronen G, Causse M, Damidaux R, Buret M, Hirschberg J, Zamir D (2003) There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnol J 1:195–207

    Article  PubMed  CAS  Google Scholar 

  • Mathieu S, Dal Cin V, Fei Z, Li H, Bliss P, Taylor MG, Klee HJ, Tieman DM (2008) Flavor compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition. J Exp Bot doi:10.1093/jxb/ern294

  • McMurchie EJ, McGlasson WB, Eaks IL (1972) Treatment of fruit with propylene gives information about biogenesis of ethylene. Nature 237:235–236

    Article  PubMed  CAS  Google Scholar 

  • Monforte AJ, Tanksley SD (2000a) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43:803–813

    Article  PubMed  CAS  Google Scholar 

  • Monforte AJ, Tanksley SD (2000b) Fine mapping of a quantitative trait locus (QTL) from Lycopersicon hirsutum chromosome 1 affecting fruit characteristics and agronomic traits: breaking linkage among QTLs affecting different traits and dissection of heterosis for yield. Theor Appl Genet 100:471–479

    Article  CAS  Google Scholar 

  • Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305

    Article  PubMed  CAS  Google Scholar 

  • Oeller PW, Min Wong L, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437–439

    Article  PubMed  CAS  Google Scholar 

  • Picton S, Barton SL, Bouzayen M, Hamilton AJ, Grierson D (1993) Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3:469–481

    CAS  Google Scholar 

  • Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, Nagy BP, Taylor LP, Campbell AD, Theologis A (1991) 1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J Mol Biol 222:937–961

    Article  PubMed  CAS  Google Scholar 

  • Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis F (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, Willmitzer L, Zamir D, Fernie AR (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, Lopez J, Beck-Bunn T (1996) Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet 92:213–224

    Article  CAS  Google Scholar 

  • Taylor IB (1986) In: Atherton J, Rudich J (eds) The tomato crop. Chapman & Hall, London, pp 1–34

    Google Scholar 

  • Tieman DM, Zeigler M, Schmelz EA, Taylor MG, Bliss P, Kirst M, Klee HJ (2006) Identification of loci affecting flavour volatile emissions in tomato fruits. J Exp Bot 57:887–896

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Li H, Ecker J (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  Google Scholar 

  • Wilkinson JQ, Lanahan MB, Yen H-C, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by Never-ripe. Science 270:1807–1809

    Article  PubMed  CAS  Google Scholar 

  • Yang SF (1987) The role of ethylene and ethylene synthesis in fruit ripening. In: Thompson W, Nothnagel E, Huffaker R (eds) Plant senescence: its biochemistry and physiology. The American Society of Plant Physiologists, Rockville, pp 156–165

    Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by grant number 2005-35304-15988 from the United States Department of Agriculture—National Research Initiative to H.K. We would like to thanks Adriana Sacco and Chima Okonkwo (Charles) for their help with fruit harvests. We are very grateful to Timothy Wills of the TGRC for supplying the seeds of the S. habrochaites NILs.

Author information

Authors and Affiliations

  1. University of Florida, Horticultural Sciences, PO Box 110690, Gainesville, FL, 32611-0690, USA

    Valeriano Dal Cin, Brian Kevany & Harry J. Klee

  2. Boyce Thompson Institute, Cornell University, Ithaca, NY, 14853, USA

    Zhangjun Fei

  3. USDA Robert W. Holley Center for Agriculture and Health, Ithaca, NY, 14853, USA

    Zhangjun Fei

Authors
  1. Valeriano Dal Cin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian Kevany
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhangjun Fei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harry J. Klee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harry J. Klee.

Additional information

Communicated by M. Havey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 99 kb)

Supplementary material 2 (TIFF 6887 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dal Cin, V., Kevany, B., Fei, Z. et al. Identification of Solanum habrochaites loci that quantitatively influence tomato fruit ripening-associated ethylene emissions. Theor Appl Genet 119, 1183–1192 (2009). https://doi.org/10.1007/s00122-009-1119-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1119-x

Keywords

Search

Navigation