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. 1996 Oct;112(2):537–547. doi: 10.1104/pp.112.2.537

The Tomato E8 Gene Influences Ethylene Biosynthesis in Fruit but Not in Flowers.

M L Kneissl 1, J Deikman 1
PMCID: PMC157976  PMID: 12226407

Abstract

We investigated the function of the tomato (Lycopersicon esculentum) E8 gene. Previous experiments in which antisense suppression of E8 was used suggested that the E8 protein has a negative effect on ethylene evolution in fruit. E8 is expressed in flowers as well as in fruit, and its expression is high in anthers. We introduced a cauliflower mosaic virus 35S-E8 gene into tomato plants and obtained plants with overexpression of E8 and plants in which E8 expression was suppressed due to co-suppression. Overexpression of E8 in unripe fruit did not affect the level of ethylene evolution during fruit ripening; however, reduction of E8 protein by cosuppression did lead to elevated levels during ripening. Levels for ethylene, 1-aminocyclopropane-1-carboxylic acid (ACC), and ACC oxidase mRNA were increased approximately 7-fold in fruit of plants with reduced E8 protein. Levels of ACC synthase 2 mRNA were increased 2.5-fold, and ACC synthase 4 mRNA was not affected. Reduction of E8 protein in anthers did not affect the accumulation of ACC or of mRNAs encoding enzymes involved in ethylene biosynthesis. Our results suggest that the product of the E8 reaction participates in feedback regulation of ethylene biosynthesis during fruit ripening.

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Selected References

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  1. Chi G. L., Pua E. C., Goh C. J. Role of Ethylene on de Novo Shoot Regeneration from Cotyledonary Explants of Brassica campestris ssp. pekinensis (Lour) Olsson in Vitro. Plant Physiol. 1991 May;96(1):178–183. doi: 10.1104/pp.96.1.178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Deikman J., Fischer R. L. Interaction of a DNA binding factor with the 5'-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J. 1988 Nov;7(11):3315–3320. doi: 10.1002/j.1460-2075.1988.tb03202.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Deikman J., Hammer P. E. Induction of Anthocyanin Accumulation by Cytokinins in Arabidopsis thaliana. Plant Physiol. 1995 May;108(1):47–57. doi: 10.1104/pp.108.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Deikman J., Kline R., Fischer R. L. Organization of Ripening and Ethylene Regulatory Regions in a Fruit-Specific Promoter from Tomato (Lycopersicon esculentum). Plant Physiol. 1992 Dec;100(4):2013–2017. doi: 10.1104/pp.100.4.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dellapenna D., Alexander D. C., Bennett A. B. Molecular cloning of tomato fruit polygalacturonase: Analysis of polygalacturonase mRNA levels during ripening. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6420–6424. doi: 10.1073/pnas.83.17.6420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dellapenna D., Lincoln J. E., Fischer R. L., Bennett A. B. Transcriptional Analysis of Polygalacturonase and Other Ripening Associated Genes in Rutgers, rin, nor, and Nr Tomato Fruit. Plant Physiol. 1989 Aug;90(4):1372–1377. doi: 10.1104/pp.90.4.1372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Giovannoni J. J., DellaPenna D., Bennett A. B., Fischer R. L. Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell. 1989 Jan;1(1):53–63. doi: 10.1105/tpc.1.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Good X., Kellogg J. A., Wagoner W., Langhoff D., Matsumura W., Bestwick R. K. Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase. Plant Mol Biol. 1994 Nov;26(3):781–790. doi: 10.1007/BF00028848. [DOI] [PubMed] [Google Scholar]
  9. Gray J., Picton S., Shabbeer J., Schuch W., Grierson D. Molecular biology of fruit ripening and its manipulation with antisense genes. Plant Mol Biol. 1992 May;19(1):69–87. doi: 10.1007/BF00015607. [DOI] [PubMed] [Google Scholar]
  10. Hua J., Chang C., Sun Q., Meyerowitz E. M. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science. 1995 Sep 22;269(5231):1712–1714. doi: 10.1126/science.7569898. [DOI] [PubMed] [Google Scholar]
  11. 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 J. 1987 Dec 20;6(13):3901–3907. doi: 10.1002/j.1460-2075.1987.tb02730.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kim W. T., Yang S. F. Turnover of 1-aminocyclopropane-1-carboxylic Acid synthase protein in wounded tomato fruit tissue. Plant Physiol. 1992 Nov;100(3):1126–1131. doi: 10.1104/pp.100.3.1126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Klee H. J. Ripening Physiology of Fruit from Transgenic Tomato (Lycopersicon esculentum) Plants with Reduced Ethylene Synthesis. Plant Physiol. 1993 Jul;102(3):911–916. doi: 10.1104/pp.102.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  17. Li N., Mattoo A. K. Deletion of the carboxyl-terminal region of 1-aminocyclopropane-1-carboxylic acid synthase, a key protein in the biosynthesis of ethylene, results in catalytically hyperactive, monomeric enzyme. J Biol Chem. 1994 Mar 4;269(9):6908–6917. [PubMed] [Google Scholar]
  18. Lincoln J. E., Cordes S., Read E., Fischer R. L. Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proc Natl Acad Sci U S A. 1987 May;84(9):2793–2797. doi: 10.1073/pnas.84.9.2793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Martin M. N., Saftner R. A. Purification and Characterization of 1-Aminocyclopropane-1-Carboxylic Acid N-Malonyltransferase from Tomato Fruit. Plant Physiol. 1995 Jul;108(3):1241–1249. doi: 10.1104/pp.108.3.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Montgomery J., Pollard V., Deikman J., Fischer R. L. Positive and negative regulatory regions control the spatial distribution of polygalacturonase transcription in tomato fruit pericarp. Plant Cell. 1993 Sep;5(9):1049–1062. doi: 10.1105/tpc.5.9.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Napoli C., Lemieux C., Jorgensen R. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. Plant Cell. 1990 Apr;2(4):279–289. doi: 10.1105/tpc.2.4.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Odell J. T., Nagy F., Chua N. H. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. 1985 Feb 28-Mar 6Nature. 313(6005):810–812. doi: 10.1038/313810a0. [DOI] [PubMed] [Google Scholar]
  23. Oeller P. W., Lu M. W., Taylor L. P., Pike D. A., Theologis A. Reversible inhibition of tomato fruit senescence by antisense RNA. Science. 1991 Oct 18;254(5030):437–439. doi: 10.1126/science.1925603. [DOI] [PubMed] [Google Scholar]
  24. Penarrubia L., Aguilar M., Margossian L., Fischer R. L. An Antisense Gene Stimulates Ethylene Hormone Production during Tomato Fruit Ripening. Plant Cell. 1992 Jun;4(6):681–687. doi: 10.1105/tpc.4.6.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Riov J., Yang S. F. Autoinhibition of Ethylene Production in Citrus Peel Discs : SUPPRESSION OF 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID SYNTHESIS. Plant Physiol. 1982 Mar;69(3):687–690. doi: 10.1104/pp.69.3.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roach P. L., Clifton I. J., Fülöp V., Harlos K., Barton G. J., Hajdu J., Andersson I., Schofield C. J., Baldwin J. E. Crystal structure of isopenicillin N synthase is the first from a new structural family of enzymes. Nature. 1995 Jun 22;375(6533):700–704. doi: 10.1038/375700a0. [DOI] [PubMed] [Google Scholar]
  27. Rottmann W. H., Peter G. F., Oeller P. W., Keller J. A., Shen N. F., Nagy B. P., Taylor L. P., Campbell A. D., Theologis A. 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. 1991 Dec 20;222(4):937–961. doi: 10.1016/0022-2836(91)90587-v. [DOI] [PubMed] [Google Scholar]
  28. Tang X., Gomes AMTR., Bhatia A., Woodson W. R. Pistil-Specific and Ethylene-Regulated Expression of 1-Aminocyclopropane-1-Carboxylate Oxidase Genes in Petunia Flowers. Plant Cell. 1994 Sep;6(9):1227–1239. doi: 10.1105/tpc.6.9.1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Theologis A., Oeller P. W., Wong L. M., Rottmann W. H., Gantz D. M. Use of a tomato mutant constructed with reverse genetics to study fruit ripening, a complex developmental process. Dev Genet. 1993;14(4):282–295. doi: 10.1002/dvg.1020140406. [DOI] [PubMed] [Google Scholar]
  30. Theologis A. One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell. 1992 Jul 24;70(2):181–184. doi: 10.1016/0092-8674(92)90093-r. [DOI] [PubMed] [Google Scholar]
  31. Theologis A. Plant hormones: more than one way to detect ethylene. Curr Biol. 1996 Feb 1;6(2):144–145. doi: 10.1016/s0960-9822(02)00446-3. [DOI] [PubMed] [Google Scholar]
  32. Uknes S., Dincher S., Friedrich L., Negrotto D., Williams S., Thompson-Taylor H., Potter S., Ward E., Ryals J. Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell. 1993 Feb;5(2):159–169. doi: 10.1105/tpc.5.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ursin V. M., Yamaguchi J., McCormick S. Gametophytic and sporophytic expression of anther-specific genes in developing tomato anthers. Plant Cell. 1989 Jul;1(7):727–736. doi: 10.1105/tpc.1.7.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wilkinson J. Q., Lanahan M. B., Yen H. C., Giovannoni J. J., Klee H. J. An ethylene-inducible component of signal transduction encoded by never-ripe. Science. 1995 Dec 15;270(5243):1807–1809. doi: 10.1126/science.270.5243.1807. [DOI] [PubMed] [Google Scholar]
  35. Zarembinski T. I., Theologis A. Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol. 1994 Dec;26(5):1579–1597. doi: 10.1007/BF00016491. [DOI] [PubMed] [Google Scholar]
  36. Zeroni M., Galil J. Autoinhibition of Ethylene Formation in Nonripening Stages of the Fruit of Sycomore Fig (Ficus sycomorus L.). Plant Physiol. 1976 Apr;57(4):647–650. doi: 10.1104/pp.57.4.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van der Krol A. R., Mur L. A., Beld M., Mol J. N., Stuitje A. R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 1990 Apr;2(4):291–299. doi: 10.1105/tpc.2.4.291. [DOI] [PMC free article] [PubMed] [Google Scholar]

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