Photosynthesis Research

, Volume 39, Issue 2, pp 93–113 | Cite as

Reminiscences, collaborations and reflections

  • Takashi Akazawa
Personal Perspective/Historical Corner

Abstract

This is a personal account by a semi old-timer who completed his official term as a professor of plant biochemistry at Nagoya University in Japan in 1992. My university student life began soon after the World War II (1948). I shared the hardships of many in my age group, in that life was difficult during my college years. I was fortunate to have the opportunity of studying in the USA on a Fulbright scholarship first at Purdue University (1955–1956), and then at the University of California, Berkeley (1956–1957). My graduate study and postdoctoral training in the new world were vitally refreshing and stimulating, which gave me the impetus for becoming a natural scientist associated with academic institutions. Consciously and subconsciously I was impressed by the friendly and liberal atmosphere surrounding young students as well as senior scholars in the United States. But more importantly, I was inspired by the critical and competitive minds prevailing among these people.

The appointment as a biochemist at the International Rice Research Institute (IRRI) in the Philippines (1962–1964) was the real start of my professional career. The work was continued upon my return to Nagoya to become a staff member of the Research Institute for Biochemical Regulation (1964–1992). Throughout the years, my major research interest has covered photosynthesis as a whole, involving photosynthetic CO2-fixation (RuBisCO), carbohydrate metabolism, e.g. starch biosynthesis and breakdown (α-amylase), and metabolic regulation, which are interrelated in the basic metabolism of plant cells.

I shall briefly describe in this article highlights from my studies and discoveries made and I shall also discuss their possible significance in plant metabolism, with the hope that it does not contradict my sense of humility: They are (a) discovery of ADPG in plants and its role in starch biosynthesis; (b) structure-function relationship of RuBisCO proteins, in particular on heterologous recombination of their subunits of plant-type enzyme molecules derived from the prokaryotic photosynthetic bacteria; (c) molecular evolution of RuBisCO genes; (d) mode of actions (formation, intracellular transport and secretion) of rice seed α-amylase and its structural characteristics (distinctive glycosylation), and (e) DNA methylation and regulatory mechanism of photosynthesis gene expression in plastids (amyloplasts). In each step of my research, I shared joy, excitement, disappointment, and agony with my colleagues, an experience that may be common to all researchers. Although it is now becoming well recognized among the scientific community in Japan, I want to point out that interaction of multinational scientific minds in the laboratory produces a vital and creative atmosphere for performance of successful research. I experienced and realized this important fact in my earlier days in the USA and the Philippines. Inasmuch as I believe that this is the most crucial element for any research laboratory to possess, I fondly remember the friendships gained with numerous overseas visitors and collaborators who have contributed immensely to our work.

Key words

fraction 1 protein RuBisCO starch biosynthesis α-amylase photosynthetic bacteria 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akazawa, T (1964) Biosynthesis of ipomeamarone II. Synthetic mechanism. Arch Biochem Biophys 105: 512–516PubMedGoogle Scholar
  2. Akazawa, T (1991) ADPG revisited-Nearly 30 years from Buenos Aires and Los Baños to Nagoya. Plant Mol Biol Report 9: 145–155Google Scholar
  3. Akazawa, T and Beevers, H (1957) Mitochondria in the endosperm of the germinating castor bean: A developmental study. Biochem J 67: 115–118PubMedGoogle Scholar
  4. Akazawa, T and Hara-Nishimura, I (1985) Topographic aspects of biosynthesis, extracellular secretion and intracellular storage of proteins in plant cells. Ann Rev Plant Physiol 36: 441–472Google Scholar
  5. Akazawa, T and Miyata, S (1982) Biosynthesis and secretion of α-amylase and other hybrolases in germinating cereal seeds. Essays Biochem 18: 40–78PubMedGoogle Scholar
  6. Akazawa, T and Osmond, CB (1977) Structural properties and ribulose bisphosphate carboxylase and oxygenase activity of fraction 1 protein from the marine green alga Halimeda cylindracea (Chlorophyta). Aust J Plant Physiol 3: 93–103Google Scholar
  7. Akazawa, T, Miljanich, P and Conn, EE (1960) Studies on cyanoglycoside of Sorghum vulgare. Plant Physiol 35: 535–538Google Scholar
  8. Akazawa, T, Newcomb, EH and Osmond, CB (1978) Pathway and products of CO2-fixation by green prokaryotic algae in the cloacal cavity of Diplosoma virens. Marine Biol 47: 325–330Google Scholar
  9. Akazawa, T, Takabe, T and Kobayashi, H (1984) Molecular evolution of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO). Trends Biochem Sci 9: 380–383CrossRefGoogle Scholar
  10. Andrews, TJ and Lorimer, GH (1987) Rubisco: Structure, mechanisms and prospects for improvement. The Biochemistry of Plants 10: 131–218Google Scholar
  11. Asami, S and Akazawa (1974) Oxidative formation of glycolic acid in photosynthesizing cells of Chromatium. Plant Cell Physiol 15: 571–576Google Scholar
  12. Asami, S, Takabe, T, Akazawa, T and Codd, GA (1983) Ribulose 1,5-bisphosphate carboxylase from the halophilic cyanobacterium Aphanothece halophytica. Arch Biochem Biophys 225: 713–721PubMedGoogle Scholar
  13. Aubert, JP, Milhaud, G and Millet, J (1957) C'assimilation de l'anhydride carbonique par des bacteries chimiautotrphes. Ann Inst Pasteur 92: 515–528Google Scholar
  14. Axelrod, B and Beevers, H (1956) Mechanism of carbohydrate breakdown in plants. Ann Rev Plant Physiol 7: 267–298CrossRefGoogle Scholar
  15. Baker, TS, Eisenberg, D, Eiserling, FA and Weisman, L (1975) The structure of form I crystals of d-ribulose-1,5-diphosphate carboxylase. J Mol Biol 91: 391–399PubMedGoogle Scholar
  16. Bassham, J, Shibata, K and Calvin, M (1955) Quantum requirement in photosynthesis related to respiration. Biochim Biophys Acta 17: 332–340CrossRefPubMedGoogle Scholar
  17. Beevers, H and Akazawa, T (1986) Metabolic Physiology of Plants (In Japanese). Iwanami Publ Co, TokyoGoogle Scholar
  18. Benson AA (1986) From Ruben to RuBisCO. Abstracts: The Oji International Seminar Kashikojima, MieGoogle Scholar
  19. Benson, AA and Calvin, M (1950) The path of carbon in photosynthesis. VII. Respiration and photosynthesis. J Expt Bot 1: 65–68Google Scholar
  20. Benson, AA and Maruo, B (1958) Identification of phosphatidyl glycerol. Biochim Biophys Acta 27: 189–195CrossRefPubMedGoogle Scholar
  21. Breidenbach, RW and Beevers, H (1967) Association of glyoxylate cycle enzymes in a novel subcellular particle from castor bean endosperm. Biochem Biophys Res Commun 27: 462–469PubMedGoogle Scholar
  22. Burris, RH (1953) Organic acids in plant metabolism. Ann Rev Plant Physiol 4: 91–114CrossRefGoogle Scholar
  23. Calvin, M (1958) The nurture of creative science and the men who make it. J Chem Educ 35: 428–432Google Scholar
  24. Calvin, M (1989) Forty years of photosynthesis and related activities. Photosynth Res 21: 3–16Google Scholar
  25. Gatenby, AA and Ellis, RJ (1990) Chaperonin function: The assembly of ribulose bisphosphate carboxylase-oxygenase. Ann Rev Cell Biol 6: 125–149PubMedGoogle Scholar
  26. Gerhart, JC (1964) Subunits for control and catalysis in aspartate transcarbamylase. Brookhaven Symposia Biol No. 17: 222–231Google Scholar
  27. Haselkorn, R, Fernandez-Moran, H, Kieras, FJ and van Bruggen, EFJ (1965) Electron microscopic and biochemical characterization of fraction 1 protein. Science 150: 1598–1591PubMedGoogle Scholar
  28. Hayashi, M, Tsuru, A, Mitsui, T, Takahashi, N, Hanzawa, H, Arata, Y and Akazawa, T (1990) Structure and biosynthesis of the xylose-containing carbohydrate moiety of rice α-amylase. Eur J Biochem 19: 287–295Google Scholar
  29. Incharoensakdi, A, Takabe, T, Takabe, T and Akazawa, T (1985) Heterologous hybridization of ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) restores the enzyme activities. Biochem Biophys Res Commun 126: 698–704PubMedGoogle Scholar
  30. Kalckar, HM (1941) The nature of energetic coupling in biological syntheses. Chem Rev 28: 71–178Google Scholar
  31. Kamen, M (1985) Radiant Science, Dark Polities. A memoir of nuclear age. Univ. California Press, BerkeleyGoogle Scholar
  32. Kamen, M (1989) Onward into a fabulous half-century. Photosynth Res 21: 139–144Google Scholar
  33. Karrer, EE, Litts, JC and Rodriguez, RL (1991) Differential expression of alpha-amylase genes in germinating rice and barley seeds. Plant Mol Biol 16: 797–805Google Scholar
  34. Kluyver, AJ and van Niel, CB (1956) The Microbes Contribution to Biology. Harvard Univ Press, CambridgeGoogle Scholar
  35. Knight, S, Andersson, I and Bränden, C-I (1990) Crystallo-graphic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2,4 Å resolution. J Mol Biol 215: 113–160PubMedGoogle Scholar
  36. Kobayshi, H, Ngernprasirtsiri, J and Akazawa, T (1990) Transcriptional regulation and DNA methylation in plastids during transitional conversion of chloroplasts to chromoplasts. EMBO J 9: 307–313PubMedGoogle Scholar
  37. Kobayshi, H, Viale, AM, Takabe, T, Akazawa, T, Wada, K, Shinozaki, K, Kobayashi, H and Sugiura, M (1991) Sequence and expression of genes encoding the large and small subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase from Chromatium vinosum. Gene 97: 55–62CrossRefPubMedGoogle Scholar
  38. Krebs, HA (1981) Reminiscences and Reflections. Oxford Univ Press/Clarendon Press, OxfordGoogle Scholar
  39. Leloir, LF (1983) Far away and long ago. Ann Rev Biochem 32: 1–15CrossRefGoogle Scholar
  40. Lorimer, GH and Andrews, TJ (1973) Plant respiration-an inevitable consequence of the existence of atmospheric oxygen. Nature (London) 243: 359–360Google Scholar
  41. Lorimer, GH, Osmond, CB, Akazawa, T and Asami, S (1978) On the mechanism of glycolate synthesis by Chromatium and Chlorella. Arch Biochem Biophys 185: 49–56PubMedGoogle Scholar
  42. Lundsgaard, E (1930) Uber die Einwirkung der Monojodessigsaure auf der Spaltungs and Oxydations Stoffwechsel. Biochem Z 220: 8–18Google Scholar
  43. Macherel, D, Kobayshi, H, Valle, E and Akazawa, T (1986) Expression of amylopiast DNA in suspension cultured cels of sycamore (Acer pseudomonas). FEBS Lett 201: 315–320CrossRefGoogle Scholar
  44. Mendiola, L and Akazawa, T (1964) Partial purification and the enzymatic nature of fraction 1 protein of rice leaves. Biochemistry 3: 174–179Google Scholar
  45. Millerd, A, Bonner, J, Axelrod, A and Bandurski, RS (1951) Oxidative and phosphorylative activity of plant mitochondria. Proc Natl Acad Sci USA 37: 855–862Google Scholar
  46. Mitsui, T, Akazawa, T, Christeller, JT and Tartakoff, AM (1985) Biosynthesis of rice seed α-amylase: Two pathways of amylase secretion by the scutellum. Arch Biochem Biophys 241: 315–328PubMedGoogle Scholar
  47. Miyano, M and Benson, AA (1962) The plant sulfolipid VII Synthesis of 6-sulfo-α-D-quinovosyl-(1–1′)-glycerol and radiochemical synthesis of sulfolipids. J Am Chem Soc 84: 59–62Google Scholar
  48. Miyata, S and Akazawa, T (1982) α-Amylase biosynthesis: Evidence for temporal sequence of NH2-terminal peptide cleavage and protein glycosylation. Proc Natl Acad Sci USA 79: 6566–6568PubMedGoogle Scholar
  49. Murata, T, Minamikawa, T and Akazawa, T (1963) Adenosine diphosphate glucose in rice and its role in starch synthesis. Biochem Biophys Res Commun 13: 439–444Google Scholar
  50. Murata, T, Minamikawa, T, Akazawa, T and Sugiyama, T (1964) Isolation of adenosine diphosphate glucose from ripening rice grains and its enzymic synthesis. Arch Biochem Biophys 166: 371–378Google Scholar
  51. Ngernprasirtsiri, J, Kobayashi, H and Akazawa, T (1988) DNA methylation as a mechanism of transcriptional regulation in nonphotosynthetic plastids in plant cells. Proc Natl Acad Sci USA 85: 4750–4754PubMedGoogle Scholar
  52. Ngernprasirtsiri, J, Chollet, R, Kobayashi, H, Sugiyama, T and Akazawa, T (1989) DNA methylation and the differentiation of C4 photosynthesis genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 264: 3241–3248Google Scholar
  53. Nishimura, M and Akazawa, T (1975) Reconstitution of spinach ribulose 1,5-diphosphate carboxylase from separated subunits. Biochem Biophys Res Commun 59: 584–590Google Scholar
  54. Nishimura, N, Hara-Nishimura, I and Akazawa, T (1987) Preparation of protoplasts from plant tissues for organelle isolation. Methods Enzymol 148: 27–34Google Scholar
  55. Nomura, M (1994) From mRNA to Ribosomes: Some reflections. In: Morimoto, R et al. (eds) Ribosomes, Protein synthesis and the Heat Shock Response. Cold Spring Harbor Press, Cold Spring Harbor, NY (in press)Google Scholar
  56. Perata, P, Pozueta-Romero, J, Yamaguchi, J and Akazawa, T (1992) Artifactual detection of ADP-dependent sucrose synthase in crude plant extracts. FEBS Lett 309: 283–287CrossRefPubMedGoogle Scholar
  57. Piras, R and Pontis, H (1972) Biochemistry of the Glycosidie Linkages-An Integrated View. Academic Press, New YorkGoogle Scholar
  58. Pozueta-Romero, J, Frehner, M and Akazawa, T (1991a) Filtering centrifugation through two layers of silicone oil: A method for the kinetic analysis of rapid metabolite transport in organelles. Cell Struct Funct 16: 357–363PubMedGoogle Scholar
  59. Pozueta-Romero, J, Frehner, M, Viale, AM and Akazawa, T (1991b) Direct transport of ADP-glucose by an adenylate translocator is linked to starch biosynthesis in amylaplasts. Proc Natl Acad Sci USA 88: 5769–5773PubMedGoogle Scholar
  60. Pozuela-Romero, J, Yamaguchi, J and Akazawa, T (1991c) ADPG formation by the ADP-specific cleavage of sucrose-Reassessment of sucrose synthase. FEBS Lett 291: 233–237CrossRefPubMedGoogle Scholar
  61. Preiss, J (1988) Biosynthesis of starch and its regulation. The Biochemistry of Plants 14: 181–254Google Scholar
  62. Quayle, JR, Fuller, RC, Benson, AA and Calvin, M (1954) Enzymic carboxylation of ribulose diphosphate. J Am Chem Soc 76: 3610Google Scholar
  63. Racker, E (1965) Mechanisms in Bioenergetics. Academic Press, New YorkGoogle Scholar
  64. Recondo, E, Dankert, M and Leloir, LF (1963) Isolation of adenosine diphosphate D-glucose from corn grains. Biochem Biophys Res Commun 12: 85–88Google Scholar
  65. Shibata, K, Benson, AA and Bassham, J (1954) The absorption spectra of suspension of living microorganisms Biochim Biophys Acta 15: 461–470CrossRefPubMedGoogle Scholar
  66. Snow, E (1958) Beginning to the Journey. Random House, New YorkGoogle Scholar
  67. Sugiura, M (1989) The chloroplast chromosomes in land plants. Ann Rev Cell Biol 5: 51–70PubMedGoogle Scholar
  68. Takabe, T and Akazawa, T (1973) Oxidative formation of phosphoglycolate from ribulose-1,5-bisphosphate catalyzed by Chromatium ribulose-1,5-bisphosphate carboxylase. Biochem Biophys Res Commun 53: 1173–1179PubMedGoogle Scholar
  69. Takabe, T and Akazawa, T (1975) Further studies on the subunit structure of Chromatium ribulose 1,5-bisphosphate carboxylase. Biochemistry 14: 46–50PubMedGoogle Scholar
  70. Takabe, T, Incharoensakdi, A and Akazawa, T (1984) Essentiality of the small subunit (B) in the catalysis of RuBP carboxylase/oxygenase is not related to subunit binding in the large subunit (A). Biochem Biophys Res Commun 122: 763–769PubMedGoogle Scholar
  71. Takahashi, N, Hotta, T, Ishihara, H, Mori, M, Tejima, S, Bligny, R, Akazawa, T, Endo, S and Arata, Y (1986) Xylose-containing common structural unit in N-linked oligosaccharides of laccase from sycamore cells. Biochemistry 25: 388–395Google Scholar
  72. Tamiya, H and Huzisige, H (1949) Effect of oxygen on the dark reaction of photosynthesis. Acta Phytochim 15: 83–104Google Scholar
  73. Umbreit, WW, Burris, RH and Stauffer, JF (1949) Manomeric Techniques and Tissue Metabolism. Burgess Publ Co, MinneapolisGoogle Scholar
  74. Uritani, I and Akazawa, T (1959) Alteration of the respiratory pattern in infected plants In: Horsfall, JG and Dimond, AE (eds) Plant Pathology, Vol I, pp 349–390. Academic Press, New YorkGoogle Scholar
  75. Varner, JE (1964) Gibberellic acid-controlled synthesis of α-amylase in barley endosperm. Plant Physiol 39: 413–415Google Scholar
  76. Viale, AM, Kobayashi, H, Takabe, T and Akazawa, T (1985) Expression of genes for subunits of plant-type RuBisCO from Chromatium and production of the enzymically active molecules in Escherichia coli. FEBS Lett 192: 283–288CrossRefPubMedGoogle Scholar
  77. Viale, AM, Kobayashi, H and Akazawa, T (1990) Distinct properties of Escherichia coli products of plant-type ribulose 1,5-bisphosphate carboxylase/oxygenase directed by two sets of genes from the photosynthetic bacterium Chromatium vinosum. J Biol Chem 265: 18386–18392PubMedGoogle Scholar
  78. Weissbach, A, Smyrniotis, PZ and Horecker, BL (1954) Pentose phosphate and CO2 fixation with spinach extracts. J Am Chem Soc 76: 361Google Scholar
  79. Wildman, SG (1992) Recollections: Early events along the trial leading to identification of RuBisCO. Prot Sci 1: 303–304Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Takashi Akazawa
    • 1
  1. 1.School of Agricultural SciencesNagoya UniversityNagoyaJapan

Personalised recommendations