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Ethylene regulates the timing of anther dehiscence in tobacco

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Abstract

We investigated the involvement of ethylene signaling in the development of the reproductive structures in tobacco (Nicotiana tabacum L.) by studying flowers that were insensitive to ethylene. Ethylene-insensitivity was generated either by expression of the mutant etr1-1 ethylene-receptor allele from Arabidopsis thaliana or by treatment with the ethylene-perception inhibitor 1-methylcyclopropene (MCP). Development of ovaries and ovules was unaffected by ethylene-insensitivity. Anther development was also unaffected, but the final event of dehiscence was delayed and was no longer synchronous with flower opening. We showed that in these anthers degeneration of the stomium cells and dehydration were delayed. In addition, we found that MCP-treatment of detached flowers and isolated, almost mature anthers delayed dehiscence whereas ethylene-treatment accelerated dehiscence. This indicated that ethylene has a direct effect on a process that takes place in the anthers just before dehiscence. Because a similar function has been described for jasmonic acid in Arabidopsis, we suggest that ethylene acts similarly to or perhaps even in concurrence with jasmonic acid as a signaling molecule controlling the processes that lead to anther dehiscence in tobacco.

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Abbreviations

ACC:

1-aminocyclopropane-1-carboxylate

ACO:

1-aminocyclopropane-1-carboxylate oxidase

MCP:

1-methylcyclopropene

PCD:

programmed cell death

References

  • Abeles FB, Morgan PW, Salveit MEJ (1992) Ethylene in plant biology. Academic Press, San Diego

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    CAS  PubMed  Google Scholar 

  • Beals TP, Goldberg RB (1997) A novel cell ablation strategy blocks tobacco anther dehiscence. Plant Cell 9:1527–1545

    Article  CAS  PubMed  Google Scholar 

  • Bonner LJ, Dickinson HG (1989) Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects. New Phytol 113:97–115

    Google Scholar 

  • Bowman JL, Baum SF, Eshed Y, Putterill J, Alvarez J (1999) Molecular genetics of gynoecium development in Arabidopsis. Curr Top Dev Biol 45:155–205

    CAS  PubMed  Google Scholar 

  • Bui AQ, O'Neill SD (1998) Three 1-aminocyclopropane-1-carboxylate synthase genes regulated by primary and secondary pollination signals in orchid flowers. Plant Physiol 116:419–428

    Article  CAS  PubMed  Google Scholar 

  • Chibi F, Matilla AJ (1994) The involvement of ethylene in in vitro maturation of mid-binucleate pollen of Nicotiana tabacum. J Exp Bot 45:529–532

    CAS  Google Scholar 

  • Child RD, Chauvaux N, John K, Ulvskov P, Van Onckelen HA (1998) Ethylene biosynthesis in oilseed rape pods in relation to pod shatter. J Exp Bot 49:829–838

    Article  CAS  Google Scholar 

  • Cox KH, Goldberg RB (1988) Analysis of plant gene expression. In: Shaw CH (ed) Plant molecular biology: a practical approach. IRL Press, Oxford, pp 1–34

    Google Scholar 

  • De Jong AJ, Yakimova ET, Kapchina VM, Woltering EJ (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta 214:537–545

    PubMed  Google Scholar 

  • De Martinis D, Mariani C (1999) Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants. Plant Cell 11:1061–1071

    Article  PubMed  Google Scholar 

  • Gunawardena A, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214

    Article  CAS  PubMed  Google Scholar 

  • Hase Y, Tanaka A, Baba T, Watanabe H (2000) FRL1 is required for petal and sepal development in Arabidopsis. Plant J 24:21–32

    Article  CAS  PubMed  Google Scholar 

  • Ishiguro S, Kawai Oda A, Ueda K, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209

    CAS  PubMed  Google Scholar 

  • Jenkins ES, Paul W, Craze M, Whitelaw CA, Weigand A, Roberts JA (1999) Dehiscence-related expression of an Arabidopsis thaliana gene encoding a polygalacturonase in transgenic plants of Brassica napus. Plant Cell Environ 22:159–167

    Article  CAS  Google Scholar 

  • Jones ML, Woodson WR (1999) Interorgan signaling following pollination in carnations. J Am Soc Hort Sci 124:598–604

    Google Scholar 

  • Keijzer CJ, Hoek IHS, Willemse MTM (1987a) The processes of anther dehiscence and pollen dispersal. Ⅲ. The dehydration of the filament tip and the anther in three monocotyledonous species. New Phytol 106:281–287

    Google Scholar 

  • Keijzer CJ, Hoek IHS, Willemse MTM (1987b) The development of the staminal filament of Gasteria verrucosa. Acta Bot Neerl 36:271–282

    Google Scholar 

  • Knoester M, Van Loon LC, Van Den Heuvel J, Hennig J, Bol JF, Linthorst HJM (1998) Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc Natl Acad Sci USA 95:1933–1937

    Article  CAS  PubMed  Google Scholar 

  • Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224

    CAS  Google Scholar 

  • O'Neill SD (1997) Pollination regulation of flower development. Annu Rev Plant Physiol Plant Mol Biol 48:547–574

    Google Scholar 

  • Orzáez D, Granell A (1997) DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J 11:137–144

    Article  Google Scholar 

  • Penninckx I, Thomma B, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113

    CAS  PubMed  Google Scholar 

  • Petersen M, Sander L, Child R, Van Onckelen H, Ulvskov P, Borkhardt B (1996) Isolation and characterisation of a pod dehiscence zone-specific polygalacturonase from Brassica napus. Plant Mol Biol 31:517–527

    CAS  PubMed  Google Scholar 

  • Roberts JA, Whitelaw CA, Gonzalez Carranza ZH, McManus MT (2000) Cell separation processes in plants—models, mechanisms and manipulation. Ann Bot 86:223–235

    Article  Google Scholar 

  • Roberts JA, Elliott KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence, and other cell separation processes. Annu Rev Plant Biol 53:131–158

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    CAS  Google Scholar 

  • Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1061

    CAS  PubMed  Google Scholar 

  • Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya X, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: Self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161

    CAS  PubMed  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    CAS  PubMed  Google Scholar 

  • Sisler EC, Serek M (1997) Inhibitors of ethylene responses in plants at the receptor level: recent developments. Physiol Plant 100:577–582

    Article  CAS  Google Scholar 

  • Smyth DR (2001) Flower development. Curr Biol 10:R82-R84

    Google Scholar 

  • Weiss D (2000) Regulation of flower pigmentation and growth: multiple signaling pathways control anthocyanin synthesis in expanding petals. Physiol Plant 110:152–157

    Article  CAS  Google Scholar 

  • Woltering EJ, Somhorst D, Van Der Veer P (1995) The role of ethylene in interorgan signaling during flower senescence. Plant Physiol 109:1219–1225

    CAS  PubMed  Google Scholar 

  • Wolters-Arts M, Derksen J, Kooijman JW, Mariani C (1996) Stigma development in Nicotiana tabacum. Cell death in transgenic plants as a marker to follow cell fate at high resolution. Sex Plant Reprod 9:243–254

    Article  Google Scholar 

  • Zhang JS, Xie C, Shen YG, Chen SY (2001a) A two-component gene (NTHK1) encoding a putative ethylene-receptor homolog is both developmentally and stress regulated in tobacco. Theor Appl Genet 102:815–824

    CAS  Google Scholar 

  • Zhang JS, Xie C, Wu XL, Du BX, Chen SY (2001b) Tobacco two-component gene NTHK2. Chin Sci Bull 46:574–577

    CAS  Google Scholar 

  • Zhang XS, O'Neill SD (1993) Ovary and gametophyte development are coordinately regulated by auxin and ethylene following pollination. Plant Cell 5:403–418

    Google Scholar 

Download references

Acknowledgements

The authors thank Mark Aarts for critical reading of the manuscript and for sharing data prior to publication. We are grateful to Huub Linthorst for Tetr transformant seeds and to Gerard Bögemann and Liesbeth Pierson for technical assistance. All plants used in this study were in perfect condition due to excellent greenhouse personnel. This research was funded by grant 805-22-681 of the Netherlands Organization for Scientific Research.

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Authors and Affiliations

  1. Department of Experimental Botany, Graduate School of Experimental Plant Sciences, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

    I. Rieu, M. Wolters-Arts, J. Derksen, C. Mariani & K. Weterings

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  1. I. Rieu
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  2. M. Wolters-Arts
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  3. J. Derksen
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  4. C. Mariani
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  5. K. Weterings
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Correspondence to K. Weterings.

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Rieu, I., Wolters-Arts, M., Derksen, J. et al. Ethylene regulates the timing of anther dehiscence in tobacco. Planta 217, 131–137 (2003). https://doi.org/10.1007/s00425-003-0976-9

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  • DOI: https://doi.org/10.1007/s00425-003-0976-9

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