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Cellular energy levels and their effect on male cell abortion in cytoplasmically male sterile lines of Petunia hybrida

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Summary

Using an HPLC method it has proved possible to follow the levels of adenine and pyridine nucleotides in the anthers of normal and cytoplasmically male sterile (CMS) lines of Petunia hybrida. Well before the appearance of any structural differences, anthers of CMS plants begin to show lower ATP/ADP ratios. In anthers, as in other non-photosynthetic plant tissues, there is a strong correlation between the ATP/ADP ratio and levels of NADPH and, when NADPH was assayed in fertile and CMS anthers, very dramatic differences were discovered. In male fertile plants, the NADPH/NADP ratio differs strikingly between somatic and reproductive tissues and reaches a peak in anthers at the early prophase of meiosis. The ratio in male sterile anthers remains largely unchanged from that normally seen in somatic tissues over this period. A cytochemical localisation technique revealed that, at the stage of development in question, the major reserves of anther NADPH are held within the tapetal cells and that levels within CMS tapeta are strikingly lower than those of normal plants. These findings are discussed in the perspective of theories proposed to explain the operation of CMS, and also in terms of the now conclusive evidence that the genetical basis of CMS lies in changes in the organisation of the mitochondrial genome.

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References

  • Aldrich HC, Gracen VE, York D, Earle ED, Yoder DC (1977) Ultrastructural effects of Helminthosporium maydis Race T toxin on mitochondria of corn roots and photoplasts. Tissue Cell 9: 167–177

    Google Scholar 

  • Bino RJ (1985a) Histological aspects of microsporogenesis in fertile cytoplasmic male sterile and restored fertile Petunia hybrida. Theor Appl Genet 69: 423–428

    Google Scholar 

  • Bino RJ (1985b) Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma 127: 230–240

    Google Scholar 

  • Bino RJ, Hoop SJ de, Neut A van der (1985) Cytochemical localisation of cytochrome oxidase in anthers of cytoplasmic male sterile Petunia hybrida (Hook.) Vilm. In: Willemse MTM, Van Went JL (eds) Sexual reproduction in seed plants, ferns and mosses. Pudoc, Wageningen, pp 44–46

    Google Scholar 

  • Boeshore ML, Hanson MR, Izhar S (1985) A valant mitochondrial DNA arrangement specific to Petunia stable sterile somatic hybrids. Plant Mol Biol 4: 125–132

    Google Scholar 

  • Borck KS, Walbot V (1982) Comparison of the restriction endonuclease digestion patterns of mitochondrial DNA from normal and male sterile cytoplasms of Zea mays L. Genetics 102: 109–128

    Google Scholar 

  • Forde BG, Leaver CJ (1978) Variation in mitochondrial translation products associated with male-sterile cytoplasms in maize. Proc Natl Acad Sci USA 75: 3841–3845

    Google Scholar 

  • Forde BG, Leaver CJ (1980) Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc Natl Acad Sci USA 77: 418–422

    Google Scholar 

  • Gao MW (1981) A preliminary analysis of the genotypes of hybrid Xian rice with wild rice cytoplasm (in Chinese). Acta Genet Sin 8: 66–74

    Google Scholar 

  • Goebel K (1905) The organography of plants, vol 2. University Press, Oxford

    Google Scholar 

  • Goodwin TW, Mercer EI (1983a) Carbohydrate biosynthesis. In: Goodwin TW, Mercer EI (eds) Introduction to plant biochemistry, 2nd edn. Pergamon Press, Oxford New York Toronto, pp 227–272

    Google Scholar 

  • Goodwin TW, Mercer EI (1983b) Respiration. In: Goodwin TW, Mercer EI (eds) Introduction to plant biochemistry, 2nd edn. Pergamon Press, Oxford New York Toronto, pp 162–226

    Google Scholar 

  • Hawkesford MJ, Leaver CJ (1987) Structuré and biogenesis of the plant mitochondrial inner membrane. In: Moore AL, Beechey RB (eds) Plant mitochondria: structurel, functional and physiological aspects. Plenum Press, New York London, pp 251–262

    Google Scholar 

  • Heldt HW, Jacobs H, Klingenberg M (1965) Kinetic studies with 14C labelled ADP and ATP and with actractyloside. Biophys Res Commun 18: 174–179

    Google Scholar 

  • Heldt HW, Klingenberg M, Milovancev M (1972) Differences between the ATP/ADP ratio in the mitochondrial matrix and in the extra-mitochondrial space. Eur J Biochem 30: 434–440

    Google Scholar 

  • Kikuta Y, Akemine T, Tagawa T (1971) Role of the pentose phosphate pathway during callus development in expiants from potato tuber. Plant Cell Physiol 12: 73–79

    Google Scholar 

  • Klingenberg M (1985) The ADP/ATP carrier in mitochondrial membranes. In: Martonosi AN (ed) The enzymes of biological membranes, 2nd edn, vol 4. Plenum Press, New York London, pp 511–553

    Google Scholar 

  • Klingenberg M, Pfaff E (1966) Structural and fuctional compartmentation in mitochondria. In: Tager JM (ed) Regulation of metabolic processes in mitochondria. Elsevier, Amsterdam New York, pp 180–201

    Google Scholar 

  • Lee SLJ, Gracen VE, Earle ED (1979) The cytology of pollen abortion in C-cytoplasmic male sterile corn anthers. Am J Bot 66: 656–667

    Google Scholar 

  • Lee SLJ, Earle ED, Gracen VE (1980) The cytology of pollen abortion in S-cytoplasmic male sterile corn anthers. Am J Bot 67: 237–245

    Google Scholar 

  • Liu XC, Jones K, Dickinson HG (1987) DNA synthesis and cytoplasmic differentiation in tapetal cells of normal and cytoplasmically male sterile lines of Petunia hybrida. Theor Appl Genet 74: 846–851

    Google Scholar 

  • Liu XC, Jones K, Dickinson HG (1988) Cytoplasmic male sterility in Petunia hybrida. Factors affecting mitochondrial ATP export in normal and cytoplasmically male sterile plants. Theor Appl Genet 76: 305–310

    Google Scholar 

  • Lowry OH, Passonneav JV (1972) Typical fluorometric procedures for metabolite assays. In: Lowry OH, Passonneav JV (eds) A flexible system of enzymatic analysis. Academic Press, New York London, pp 4–18

    Google Scholar 

  • Moss GI, Heslop-Harrison J (1967) A cytochemical study of DNA, RNA and protein in developing maize anther. II. Observations. Ann Bot (London) 31: 555

    Google Scholar 

  • Pfanner N, Neupert W (1987) Distinct steps in the import of ADP/ATP carrier into mitochondria. J Biol Chem 262: 7528–7536

    Google Scholar 

  • Sheng T, Wang JE, Zhao BO (1982) Carbohydrate metabolism. In: Sheng T, et al. (eds) Biochemistry, vol 2 (in Chinese). Educational Press in China, Shanghai, pp 448–478

    Google Scholar 

  • Steer MW (1977) Differentiation of the tapetum in Avena. I. The cell surface. J Cell Sci 25: 125–138

    Google Scholar 

  • Tager JM, Wanders RJA, Groen AK, Kuntz W, Bohnensack R, Kuster U, Letko G, Bohme G, Duszynski J, Wojtozack L (1983) Control of mitochondrial respiration. FEBS Lett 151: 1–9

    Google Scholar 

  • Vallejos CB (1983) Enzyme activity staining. In: Tanksley SD, Orton TJ (eds) Isozymes in plant genetics and breeding, vol A. Elsevier, Amsterdam New York, pp 469–516

    Google Scholar 

  • Young E, Hanson M (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50: 41–49

    Article  CAS  PubMed  Google Scholar 

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Liu, X.C., Dickinson, H.G. Cellular energy levels and their effect on male cell abortion in cytoplasmically male sterile lines of Petunia hybrida . Sexual Plant Reprod 2, 167–172 (1989). https://doi.org/10.1007/BF00192763

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