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Plant Biol (Stuttg) 2006; 8(5): 579-586
DOI: 10.1055/s-2006-924240
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Effects of Cytokinin Production under Two SAG Promoters on Senescence and Development of Tomato Plants

D. Swartzberg1 , N. Dai1 , S. Gan2 , R. Amasino3 , D. Granot1
  • 1Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, P.O. Box 6, Bet Dagan, 50250, Israel
  • 2Department of Horticulture, Cornell University, Ithaca, NY 14853-5904, USA
  • 3University of Wisconsin, 433 Babcock Drive, Madison, WI 53706, USA
Further Information

Publication History

Received: February 7, 2006

Accepted: April 26, 2006

Publication Date:
01 August 2006 (online)

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Abstract

Two promoters of senescence-associated Arabidopsis genes, SAG12 and SAG13, were used in tomato plants to express IPT that catalyzes the rate-limiting step in cytokinin biosynthesis. Expression of these heterologous promoters in tomato plants was analyzed using the reporter gene β-glucuronidase. Both promoters are expressed in tomato leaves in a manner similar to their expression in Arabidopsis plants. The SAG12 promoter is very specific to senescing leaves, whereas the SAG13 promoter is expressed in mature leaves prior to the onset of visible senescence and its expression increases in senescing leaves. Expression of both promoters in tomato tissues other than leaves was very low. IPT expressed under the control of SAG12 and SAG13 promoters (PSAG12::IPT and PSAG13::IPT, respectively) resulted in suppression of leaf senescence and advanced flowering, as well as in a slight increase in fruit weight and fruit total soluble solids (TSS). However, expression of PSAG13::IPT also led to stem thickening, short internodal distances and loss of apical dominance. In contrast to the autoregulation of PSAG12::IPT, PSAG13::IPT is expressed at higher levels in mature leaves. This difference is likely due to PSAG13::IPT exhibiting two phases of expression - a senescence-independent expression prior to the onset of senescence that is not subjected to autoregulation by cytokinin, and enhanced expression throughout senescence which is autoregualted by cytokinin. This moderate different autoregulated behavior of PSAG12::IPT and PSAG13::IPT markedly influenced plant development, emphasizing the biological effects of cytokinin in addition to senescence inhibition.

Key words

Cytokinin - IPT - promoter - SAG - senescence - tomato

References

  • 1 Balibrea Lara M. E., Gonzalez Garcia M. C., Fatima T., Ehness R., Lee T. K., Proels R., Tanner W., Roitsch T.. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence.  Plant Cell. (2004);  16 1276-1287
    CrossrefPubMedSearch in Google Scholar
  • 2 Barg R., Pilowsky M., Shabtai S., Carmi N., Szechtman A. D., Dedicova B., Salts Y.. The TYLCV-tolerant tomato line MP‐1 is characterized by superior transformation competence.  Journal of Experimental Botany. (1997);  48 1919-1923
    CrossrefPubMedSearch in Google Scholar
  • 3 Bewli I. S., Whitam F. H.. Characterization of kinetin induced water uptake by detached radish cotyledons.  Botanical Gazzet. (1976);  137 58-64
    PubMedSearch in Google Scholar
  • 4 Buchanan-Wollaston V.. The molecular biology of leaf senescence.  Journal of Experimental Botany. (1997);  48 181-199
    PubMedSearch in Google Scholar
  • 5 Buchanan-Wollaston V., Page T., Harrison E., Breeze E., Lim P. O., Nam H. G., Lin J. F., Wu S. H., Swidzinski J., Ishizaki K., Leaver C. J.. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis.  The Plant Journal. (2005);  42 567-585
    CrossrefPubMedSearch in Google Scholar
  • 6 Chang H., Jones M. L., Banowetz G. M., Clark D. G.. Overproduction of cytokinins in petunia flowers transformed with PSAG12-IPT delays corolla senescence and decreases sensitivity to ethylene.  Plant Physiology. (2003);  132 2174-2183
    CrossrefPubMedSearch in Google Scholar
  • 7 Chen C.. Cytokinin biosynthesis and interconversion.  Physiologia Plantarum. (1997);  101 665-673
    CrossrefPubMedSearch in Google Scholar
  • 8 Chen L. F. O., Hwang J. Y., Charng Y. Y., Sun C. W., Yang S. F.. Transformation of broccoli (Brassica oleracea var. italica) with isopentenyltransferase gene via Agrobacterium tumefaciens for post-harvest yellowing retardation.  Molecular Breeding. (2001);  7 243-257
    CrossrefPubMedSearch in Google Scholar
  • 9 Cowan A. K., Freeman M., Bjorkman P. O., Nicander B., Sitbon F., Tillberg E.. Effects of senescence-induced alteration in cytokinin metabolism on source-sink relationships and ontogenic and stress-induced transitions in tobacco.  Planta. (2005);  221 801-814
    CrossrefPubMedSearch in Google Scholar
  • 10 Gan S.. Molecular characterization and genetic manipulation of plant senescence. PhD Thesis, Department of Biochemistry, Madison, WI, USA, University of Wisconsin-Madison. (1995): pp. 190
    Search in Google Scholar
  • 11 Gan S., Amasino R. M.. Inhibition of leaf senescence by autoregulated production of cytokinin.  Science. (1995);  270 1986-1988
    PubMedSearch in Google Scholar
  • 12 Gan S., Amasino R. M.. Cytokinins in plant senescence: from spray and pray to clone and play.  BioEssays. (1996);  18 557-565
    CrossrefPubMedSearch in Google Scholar
  • 13 Gan S., Amasino R.. Making sense of senescence.  Plant Physiology. (1997);  113 313-319
    PubMedSearch in Google Scholar
  • 14 Guivarc'h A., Rembur J., Goetz M., Roitsch T., Noin M., Schmulling T., Chriqui D.. Local expression of the ipt gene in transgenic tobacco (Nicotiana tabacum L. cv. SR1) axillary buds establishes a role for cytokinins in tuberization and sink formation.  Journal of Experimental Botany. (2002);  53 621-629
    CrossrefPubMedSearch in Google Scholar
  • 15 Hewelt A., Prinsen E., Schell J., Van Onckelen H., Schmulling T.. Promoter tagging with a promoterless ipt gene leads to cytokinin-induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effects.  The Plant Journal. (1994);  6 879-891
    CrossrefPubMedSearch in Google Scholar
  • 16 Jefferson R. A., Kavanagh T. A., Bevan M. W.. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.  EMBO Journal. (1987);  6 3901-3907
    PubMedSearch in Google Scholar
  • 17 Jordi W., Schapendonk A., Davelaar E., Stoopen G. M., Pot C. S., de Visser R., van Rhijn J. A., Gan S., Amasino R. M.. Increased cytokinin levels in transgenic PSAG12-IPT tobacco plants have large direct and indirect effects on leaf senescence, photosynthesis and N partitioning.  Plant, Cell and Environment. (2000);  23 279-289
    CrossrefPubMedSearch in Google Scholar
  • 18 Li Y., Hagen G., Guilfoyle T. J.. Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs.  Developmental Biology. (1992);  153 386-395
    CrossrefPubMedSearch in Google Scholar
  • 19 Lohman K. N., Gan S., John M. C., Amasino R. M.. Molecular analysis of natural leaf senescence in Arabidopsis thaliana.  Physiologia Plantarum. (1994);  92 322-328
    CrossrefPubMedSearch in Google Scholar
  • 20 Luo Y. Y., Gianfagna T. J., Janes H. W., Huang B., Wang Z., Xing J.. Expression of the ipt gene with the AGPase S1 promoter in tomato results in unbranched roots and delayed leaf senescence.  Plant Growth Regulation. (2005);  47 47-57
    CrossrefPubMedSearch in Google Scholar
  • 21 McCabe M. S., Garratt L. C., Schepers F., Jordi W. J., Stoopen G. M., Davelaar E., van Rhijn J. H., Power J. B., Davey M. R.. Effects of PSAG12-IPT gene expression on development and senescence in transgenic lettuce.  Plant Physiology. (2001);  127 505-516
    CrossrefPubMedSearch in Google Scholar
  • 22 McCormick S.. Transformation of tomato with Agrobacterium tumefaciens. Lindsey, K., ed. Plant Tissue Culture Mannual. Dordrecht; Kluwer Academic Publishers (1991): 1-9
    Search in Google Scholar
  • 23 McGaw B. A., Burch L. R.. Cytokinin biosynthesis and metabolism. Davies, P. J., ed. Plant Hormones: Physiology, Biochemistry and Molecular Biology Dordrecht,. The Netherlands; Kluwer Academic Publishers (1995): 98-117
    Search in Google Scholar
  • 24 McKenzie M. J., Mett V. V., Stewart Reynolds P. H., Jameson P. E.. Controlled cytokinin production in transgenic tobacco using a copper-inducible promoter.  Plant Physiology. (1998);  116 969-977
    CrossrefPubMedSearch in Google Scholar
  • 25 Medford J. I., Horgan R., El-Sawi Z., Klee H. J.. Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene.  Plant Cell. (1989);  1 403-413
    CrossrefPubMedSearch in Google Scholar
  • 26 Nam H. G.. The molecular genetic analysis of leaf senescence.  Current Opinion in Biotechnology. (1997);  8 200-207
    CrossrefPubMedSearch in Google Scholar
  • 27 Noh Y. S., Amasino R. M.. Identification of a promoter region responsible for the senescence-specific expression of SAG12.  Plant Molecular Biology. (1999);  41 181-194
    CrossrefPubMedSearch in Google Scholar
  • 28 Nooden L. D., Singh S., Letham D. S.. Correlation of xylem sap cytokinin levels with monocarpic senescence in soybean.  Plant Physiology. (1990);  93 33-39
    PubMedSearch in Google Scholar
  • 29 Roitsch T., Ehness R.. Regulation of source/sink relations by cytokinins.  Plant Growth Regulation. (2000);  32 359-367
    CrossrefPubMedSearch in Google Scholar
  • 30 Santokh S., Letham D. S., Palni L. M. S.. Cytokinin biochemistry in relation to leaf senescence. VII. Endogenous cytokinin levels and exogenous applications of cytokinins in relation to sequential leaf senescence of tobacco.  Physiologia Plantarum. (1992 a);  86 388-397
    CrossrefPubMedSearch in Google Scholar
  • 31 Santokh S., Letham D. S., Palni L. M. S.. Cytokinin biochemistry in relation to leaf senescence. VIII. Translocation, metabolism and biosynthesis of cytokinins in relation to sequential leaf senescence of tobacco.  Physiologia Plantarum. (1992 b);  86 398-406
    CrossrefPubMedSearch in Google Scholar
  • 32 Schroeder K. R., Stimart D. P., Nordheim E. V.. Response of Nicotiana alata to insertion of an autoregulated senescence-inhibition gene.  Journal of The American Society For Horticultural Science. (2001);  126 523-530
    PubMedSearch in Google Scholar
  • 33 Skene K. G. M.. Cytokinin production by roots as a factor in the control of plant growth. Torrey, J. G. and Clarkson, D. T., eds. The Development and Function of Roots Third Cabot Symposium. New York; Academic Press Inc. (1975): 365-396
    Search in Google Scholar
  • 34 Smart C. M.. Gene expression during leaf senescence.  New Phytologist. (1994);  126 419-448
    CrossrefPubMedSearch in Google Scholar
  • 35 Smart C. M., Scofield S. R., Bevan M. W., Dyer T. A.. Delayed leaf senescence in tobacco plants transformed with tmr, a gene for cytokinin production in Agrobacterium.  Plant Cell. (1991);  3 647-656
    CrossrefPubMedSearch in Google Scholar
  • 36 Smigocki A. C.. Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene.  Plant Molecular Biology. (1991);  16 105-115
    CrossrefPubMedSearch in Google Scholar
  • 37 Taiz L., Zeiger E.. Plant Physiology. 2nd ed. Sunderland; Sinauer Associates, Inc. (1998): 109
    Search in Google Scholar
  • 38 Van Loven K., Beinsberger S. E. I., Valcke R. L. M., Van Onckelen H. A., Clijsters H. M. M.. Morphometric analysis of the growth of Phsp70-ipt transgenic tobacco plants.  Journal of Experimental Botany. (1993);  44 1671-1678
    PubMedSearch in Google Scholar
  • 39 Van-Staden J., Cook E. L., Nooden L. D.. Cytokinins and senescence. Nooden, L. D. and Leopold, A. C., eds. Senescence and Aging in Plants. London; Academic Press Inc. (1988): 282-328
    Search in Google Scholar
  • 40 Wang J., Letham D. S., Cornish E., Stevenson K. R.. Studies of cytokinin action and metabolism using tobacco plants expressing either the ipt or the GUS gene controlled by a chalcone synthase promoter. I. Developmental features of the transgenic plants.  Australian Journal of Plant Physiology. (1997);  24 661-672
    PubMedSearch in Google Scholar
  • 41 Weaver L. M., Gan S., Quirino B., Amasino R. M.. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment.  Plant Molecular Biology. (1998);  37 455-469
    CrossrefPubMedSearch in Google Scholar
  • 42 Wingler A., Purdy S., Maclean J. A., Pourtau N.. The role of sugars in integrating environmental signals during the regulation of leaf senescence.  Journal of Experimental Botany. (2005);  57 391-399
    CrossrefPubMedSearch in Google Scholar
  • 43 Wingler A., von-Schaewen A., Leegood R. C., Lea P. J., Quick W. P.. Regulation of leaf senescence by cytokinin, sugars, and light. Effects on NADH-dependent hydroxypyruvate reductase.  Plant Physiology. (1998);  116 329-335
    CrossrefPubMedSearch in Google Scholar
  • 44 Young T. E., Giesler-Lee J., Gallie D. R.. Senescence-induced expression of cytokinin reverses pistil abortion during maize flower development.  The Plant Journal. (2004);  38 910-922
    CrossrefPubMedSearch in Google Scholar
  • 45 Zhang J., Kirkham M. B.. Antioxidant responses to drought in sunflower and sorghum seedlings.  New Phytologist. (1996);  132 361-373
    CrossrefPubMedSearch in Google Scholar

D. Granot

Institute of Plant Sciences
Agricultural Research Organization
The Volcani Center

P.O. Box 6

Bet Dagan 50250

Israel

Email: granot@agri.gov.il

Editor: J. T. M. Elzenga