Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

JOINTLESS is a MADS-box gene controlling tomato flower abscissionzone development

Abstract

Abscission is a universal and dynamic process in plants whereby organssuch as leaves, flowers and fruit are shed, both during normal development,and in response to tissue damage and stress1. Shedding occursby separation of cells in anatomically distinct regions of the plant, calledabscission zones (AZs). During abscission, the plant hormone ethylene stimulatescells to produce enzymes that degrade the middle lamella between cells inthe AZ. The physiology and regulation of abscission at fully developed AZsis well known2,3, but the molecular biology underlying theirdevelopment is not. Here we report the first isolation of a gene directlyinvolved in the development of a functional plant AZ. Tomato plants with the jointless mutation4 fail to develop AZs on their pedicelsand so abscission of flowers or fruit does not occur normally. We identify JOINTLESS as a new MADS-box gene in a distinct phylogenetic clade separatefrom those functioning in floral organs. We propose that a deletion in JOINTLESS accounts for the failure of activation of pedicel AZ developmentin jointless tomato plants.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: The tomato JOINTLESS gene.
Figure 2: Sense complementation and antisense suppression of AZs in jointless and wild-type tomatoes.
Figure 3: The segregation of transgenes in T1 progeny from an antisense primarytransgenic plant (a) and expression analysis of JOINTLESS gene(b).
Figure 4: The phylogenetic relationship of JOINTLESS with other MADS-boxgenes.

References

  1. 1

    Bleecker, A. B. & Patterson, S. E. Last exit:senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 8, 1169–1179 (1997).

    Article  Google Scholar 

  2. 2

    Addicott, F. T. Abscission (Univ. of California Press, Berkeley, Los Angeles, London, 1982).

    Google Scholar 

  3. 3

    Jinn, T. L., Stone, J. M. & Walker, J. C. HAESA, an Arabidopsis leucine-richrepeat receptor kinase, controls floral organ abscission. GenesDev. 14, 108–117 (2000).

    CAS  Google Scholar 

  4. 4

    Butler, L. Inherited characters in the tomato. II. Jointless pedicel. J. Hered. 37, 25–26 (1936).

    Google Scholar 

  5. 5

    Roberts, J. A., Schindler, C. B. & Tucker, G. A. Ethylene-promoted tomato flower abscission and thepossible involvement of an inhibitor. Planta 160, 159–163 (1984).

    CAS  Article  Google Scholar 

  6. 6

    Rick, C. M. & Sawant, A. C. Factor interactions affectingthe phenotypic expression of the jointless character in tomatoes. Am. Soc. Hort. Sci. 66, 354–360(1955).

    Google Scholar 

  7. 7

    Pnueli, L. etal. The SELF-PRUNING gene of tomato regulates vegetative toreproductive switching of sympodial meristems and is the ortholog of CEN andTFL1. Development 125, 1979–1989 (1998).

    CAS  PubMed  Google Scholar 

  8. 8

    Szymkowiak, E. J. & Irish, E. E. Interactionsbetween jointless and wild-type tomato tissues during development ofthe pedicel abscission zone and the inflorescence meristem. PlantCell 11, 159–175 (1999).

    CAS  Google Scholar 

  9. 9

    Rick, C. M. & Yoder, J. I. Classical and molecular geneticsof tomato: highlights and perspectives. Annu. Rev. Genet. 22, 281–300 (1988).

    CAS  Article  Google Scholar 

  10. 10

    Wing, R. A., Zhang, H. B. & Tanksley, S. D. Map-based cloning in crop plants. Tomato as a model:I. Genetic and physical mapping of jointless. Mol.Gen. Genet. 242, 681–688 (1994).

    CAS  Article  Google Scholar 

  11. 11

    Zhang, H. -B., Martin, G. B., Tanksley, S. D. & Wing, R. A. Map-based cloning in crop plants. Tomato as a model system II. Isolation andcharacterization of a set of overlapping yeast artificial chromosomes encompassing jointless locus. Mol. Gen. Genet. 244, 613–621 (1994).

    CAS  Article  Google Scholar 

  12. 12

    Budiman, M. A., Mao, L., Wood, T. & Wing, R. A. A deep-coveragetomato BAC library and prospects toward development of an STC framework forgenome sequencing. Genome Res. 10, 129–136 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Yanofsky, M. F. et al. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35–39 (1990).

    ADS  CAS  Article  Google Scholar 

  14. 14

    Sommer, H. et al. Deficiens, a homeotic gene involved in the controlof flower morphogenesis in Antirrhinum majus: the protein shows homologyto transcription factors. EMBO J. 9, 605–613 (1990).

    CAS  Article  Google Scholar 

  15. 15

    Riechmann, J. L. & Meyerowitz, E. M. MADS domainproteins in plant development. Biol. Chem. 378, 1079–1101 (1997).

    CAS  PubMed  Google Scholar 

  16. 16

    Carmona, M. J., Ortega, N. & Garcia-Maroto, F. Isolation and molecular characterization of a new vegetativeMADS-box gene from Solanum tuberosum L. Planta 207, 181–188 (1998).

    CAS  Article  Google Scholar 

  17. 17

    Anthony, R. G., James, P. E. & Jordan, B. R. The cDNA sequence of a cauliflower apetala-1/squamosa homolog. Plant Physiol. 108, 441–442 (1995).

    CAS  Article  Google Scholar 

  18. 18

    Kang, H. G., Jang, S., Chung, J. E., Cho, Y. G. & An, G. Characterization of two rice MADS box genes that control flowering time. Mol. Cell 7, 559–566 (1997).

    CAS  Google Scholar 

  19. 19

    Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M. F. & Lifschitz, E. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6, 163–173 (1994).

    CAS  Article  Google Scholar 

  20. 20

    Pnueli, L. et al. The MADS box gene family in tomato: temporal expression duringfloral development, conserved secondary structures and homology with homeoticgenes from Antirrhinum and Arabidopsis. Plant J. 1, 255–266 (1991).

    CAS  Article  Google Scholar 

  21. 21

    Gu, Q., Ferrandiz, C., Yanofsky, M. F. & Martienssen, R. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 509–1517 (1998).

    Google Scholar 

  22. 22

    Liljegren, S. J. et al. SHATTERPROOF MADS-box genes control seed dispersalin Arabidopsis. Nature 404, 766–770 (2000).

    ADS  CAS  Article  Google Scholar 

  23. 23

    Petersen, M. et al. Isolation and characterisation of a pod dehiscence zone-specificpolygalacturonase from Brassica napus. Plant Mol. Biol. 31, 517–527 (1996).

    CAS  Article  Google Scholar 

  24. 24

    Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein databasesearch programs. Nucleic Acids Res. 25, 3389–3402 (1997).

    CAS  Article  Google Scholar 

  25. 25

    Bernatzky, R. & Tanksley, S. D. Methods for detection of singleor low copy sequences in tomato on Southern blots. Plant Mol. Bio.Rep. 4, 37–41 (1986).

    CAS  Article  Google Scholar 

  26. 26

    McCormick, S. et al. Leaf disc transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens. Plant Cell Reporters 5, 81–84 (1986).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank H.-B. Zhang, S. D. Choi and C. Scheuring for their work duringthe early stage of this project; C. M. Rick for the NILs LA3023 and LA3021;S. S. Woo for sequence analysis of YAC end TY159L; and the staff of the CUGIDNA Sequencing, Bioinformatics (M. Sasinowsky) and BAC/EST Resource (D. Frisch)Centers. This work is supported by a National Science Foundation grant toR.A.W and E.J.S and the Coker Chair in Plant Molecular Genetics to R.A.W.Any opinions, findings, and conclusions or recommendations expressed in thismaterial are those of the author(s) and do not necessarily reflect the viewsof the National Science Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rod A. Wing.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mao, L., Begum, D., Chuang, Hw. et al. JOINTLESS is a MADS-box gene controlling tomato flower abscissionzone development. Nature 406, 910–913 (2000). https://doi.org/10.1038/35022611

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing