XVII. B. Some Major Steps in the Understanding of the Biochemistry of porphyrin and Chl Formation

1. 1948: Granick demonstrated the accumulation of divinyl (DV) protoporphyrin IX (Proto) in Chlorella mutants inhibited in their capability to form chlorophyll (Chl) , and proposed that in plants, DV Proto is a precursor of MV Chl a.
2. 1948: Granick demonstrated the accumulation of divinyl (DV) Mg-protoporphyrin IX (Mg-Proto) in Chlorella mutants inhibited in their capability to form chlorophyll (Chl) , and proposed that in plants, DV Mg-Proto is a precursor of MV Chl a.
3. 1948: Koski and Smith, purified protochlorophyllide (Pchlide a) which they mistook for Pchlide a phytyl ester [i. e. protochlorophyll (Pchl) a ] and determined its spectral absorption properties.
4. 1948: On the basis of the correspondance of newly published absorbance spectra of MV Pchlide a (mistaken for MV Pchl a), and the action spectrum of MV Chl a formation, Smith proposed that MV Pchl a (in fact, MV Pchlide a) is the immediate precursor of MV Chl a .
5. 1949: Muir and Neuberger and Wittenberg and Shemin showed that one carbon atom and the nitrogen atom of each pyrrole ring of protoheme is derived from the alpha-atom and the associated nitrogen atom of glycine.
6. 1950: Granick demonstrated the accumulation of monovinyl (MV) Pchlide a in Chlorella mutants inhibited in their capability to form chlorophyll (Chl), and proposed that in plants, Pchlide a is the immediate precursor of Pchlide a phytyl ester (i. e. Pchl a). Granick then organized DV Proto, DV Mg-Proto, MV Pchlide a, MV Pchlide a phytyl ester, and MV Chl a by order of increasing chemical complexity into a paper chemistry, single branched, Chl a biosynthetic pathway that originated in DV Proto and ended in the formation of MV Chl a.
7. 1950: Muir and Neuberger and Wittenberg and Shemin showed that each of the four methine bridge carbon atoms of protoheme is derived from the alpha-carbon of glycine.
8. 1951: Shemin and Wittenberg concluded that all four pyrrole rings of protoheme arise from a common precursor pyrrole.
9. 1952: Smith, prepared the first Pchl a-apoprotein complex (actually containing a mixture of Pchlide a and Pchlide a phytyl ester) from etiolated barley, and determined its absorption maximum at 650 nm. Later the complex was named Pchl-holochrome by Smith and collaborators.
10. 1952: Shemin and Kumin demonstrated that the remaining carbon atoms as well as the side chains of protoheme are derived from succinate, which led shemin to suggest that the carbon atoms of succinate enter porphyrin metabolism as succinyl coenzyme A.
11. 1952: Westall, crystallized porphobilinogen (PBG) from the urine of a patient with acute porphyria.
12. 1953: Shemin and Russel proposed that glycine and succinate did not enter porphyrin metabolism as individual compounds but as a new compound: delta-aminolevulinic acid (ALA).
13. 1953: Della Rosa et al, demonstrated the incorporation of ¹⁴C-glycine and ¹⁴C-acetate into MV Chl.
14. 1953: Bogorad and Granick, described a Chlorella mutant capable of accumulating porphyrins with two, three, four, five, six, seven and 8 carboxyl groups, and proposed that these porphyrins may be intermediates in the formation of DV Proto.
15. 1953: Bogorad and Granick, demonstrated the conversion of exogenous PBG to DV Proto in frozen and thawed Chlorella cells, and proposed a single branched paper chemistry pathway that originated in glycine and succinate and ended with the formation of Proto via ALA, Uoroprphyrin III (Uro), Coproporphyrin III (Copro), hematoporphyrin IX, and DV Proto.
16. 1954: Granick, demonstrated the conversion of ALA to PBG and porphyrins by extracts of Chlorella cells, of spinach and chicken erythrocytes.
17. 1954: Smith and Benitez, described the kinetics of Pchl a (actually mainly Pchlide a) photoconversion to chlorophyll(ide) [Chl(ide)] a in etiolated barley leaves.
18. 1956: Neve and Labbe, recognized that the actual tetrapyrrole intermediates between PBG and DV proto are not porphyrins but porphyrinogens, i. e. hexahydroporphyrins.
19. 1956: Smith and Kupke extended their studies of Pchl-holochrome.
20. 1956: Goldberg et al, described the insertion of ferrous iron into Proto by ferrochelatase.
21. 1957:Shibata described his opal glass technique for the determination of the spectral properties of intact leaves, and described the Shibata shift during greening of etiolated tissues.
22. 1957: Wolff and Price demonstrated that the immediate product of Pchl(ide) a photoconversion is chlorophyllide (Chlide) a, which esterified to Chl a.
23. 1958: Bogorad, demonstrated the conversion of PBG to uroporphyrinogen III (Urogen III) in a wheat germ extract.
24. 1958: Mauzerall and Granick, demonstrated the conversion of Urogen III to coproporphyrinogen III (Coprogen III).
25. 1961: Sano and Granick described the conversion of Coprogen III to DV Proto by beef liver mitochondria.
26. 1961: Granick demonstrated the accumulation of DV Mg-Proto monomethyl ester (Mpe) in Chlorella mutants inhibited in their capability to form chlorophyll (Chl), and proposed that in plants, DV Mpe is a precursor of MV Pchlide a. In that same article Granick reported on the first usage of 2,2'-dipyridyl (Dpy) to induce the accumulation of Mpe in etiolated barley leaves.
27. 1961: Tait and Gibson, demonstration the conversion of Mg-Proto to Mpe by R. Spheroides chromatophotes.
28. 1963: Gibson et al, detected S-adenosylmethionine-Mg-Proto methyl transferase in R. Spheroides
29. 1963: Jones, detected divinyl Pchlide a in R. Spheroides inhibited in their growth by 8-hydroxyquinoline and suggested that DV Pchlide a is a transient precursor of MV Pchlide a. 1966: Jones, detected DV Pchlide a phytyl ester in the pumkin inner seed coat and proposed its involvement in Chl a Biosynthesis.
30. 1967:Sironval et al, proposed that the Pchl(ide) a holochrome acts as a shuttling photoenzyme that catalyzes the conversion of Pchlide a to Chlide a.
31. 1968: Shemin, proposed a detailed mechanism of the mode of action of ALA dehydratase, the enzyme that converts two moles of ALA to PBG.
32. 1969: Ellsworth and Aronoff, detected intermediates between Mpe and Pchlide a involving putative DV and MV metal-free acrylic, hydroxy and keto derivatives in ultraviolet Chlorella mutants, and proposed that in plants, that the formation of DV and MV Pchlide a involves a beta-oxidation sequence of the methyl propionate of DV and novel MV Mpe, at position 6 of the macrocycle.
33. 1970: Rebeiz et al, reported that kinetic analysis of the formation of the ¹⁴C-Pchl(ide) a pool, does not support the currently accepted notion that Pchlide a is the immediate precursor of Pchlide a phytyl ester. This observation constituted the first evidence of a potential Chl biosynthetic heterogeneity in plants.
34. 1971: Rebeiz and Castelfranco, reported the total biosynthesis of ¹⁴C-Pchlide a and its phytyl ester from ¹⁴C-ALA in a cell-free system from higher plants.
35. 1971: Rebeiz and Castelfranco, reported the total biosynthesis of ¹⁴C-Chl a and b from ¹⁴C-ALA in a cell-free system from higher plants.
36. 1972: Gorchein, demonstrated the conversion of exogenous Proto to Mpe in R. Spheroides, and the ATP requirement of the process.
37. 1974: Griffiths, demonstrated that NADPH is the hydrogen donor for the photoreduction of Pchlide a to Chlide a
38. 1974: Beale and Castelfranco, demonstrated that in green plants ALA is formed from glutamic acid.
39. 1975: Rebeiz et al, detected the formation of Mg-porphyrins during greening of etiolated tissues, and described their spectrofluorometric properties.
40. 1975: Poulson and Polglase demonstrated that protoporphyrinogen IX oxidase (Protox for short) catalyzes the conversion of Protogen IX to Proto.
41. 1977: Smith and Rebeiz, described the enzymic insertion of Mg into Proto, in-organello, to yield Mg-Proto.
42. 1977: Mattheis and Rebeiz, described the conversion of exogenous Proto to Pchlide a, in organello.
43. 1977: Mattheis and Rebeiz, Dewscribed the conversion of exogenous Mg-Proto monoester (Mpe)to Pchlide a, in organello.
44. 1978: Griffiths, Proposed that the Pchl holochrome i. e. Pchlide a oxidoreductase, NADPH and Pchlide a form a photoactive ternary Pchlide a NADPH-enzyme complex with a red absorption maximum at 652 nm.
45. 1979: Ellsworth and Murphy, reported the conversion of Mg-Proto to Pchlide a in crude cell-free homogenates.
46. 1979:Belanger and Rebeiz, reported that the Pchlide a pool of etiolated tissues consisted of two components (probably MV and DV components) which are photoconvertible into two distinct Chlide a species.
47. 1979: Recognition by Battersby et al, and Jordan and Seehra that 1-hydroxymethylbilane (HMBL) (also called preuroporphyrinogen) is the immediate precursor of Uroporphyrinogen III.
48. 1980: Apel et al, described the purification of Pchlide a oxidoreductase (POR-A) from etiolated barley.
49. 1980: Pardo et al, confirmed that ATP was a mandatory cofactor for Mg-insertion into Proto and that higher concentration of added ATP eliminated the formation of Zn-Proto.
50. 1980: Belanger and Rebeiz, described the detection of DV Pchlide a in higher plants.
51. 1980:Belanger and Rebeiz, described the formation of DV Chlide a and DV Chl a in higher plants.
52. 1980: Belanger and Rebeiz, described the detection of DV Pchlide a phytyl ester in etiolated higher plants.
53. 1980: Rebeiz et al, predicted the possible occurrence of DV Chl b in plants.
54. 1980: Schoch, wrapped up the demonstration that in etiolated tissues subjected to a light treatment followed by darkness, Chlide a is first esterified with geranylgeraniol (GG) to yield Chl a GG, which is reduced stepwise to Chl a dihydroGG (DHGG), tetrahyddroGG (THGG) and finally to hexahydroGG, i. e. phytylated Chl a.
55. 1981: McCarthy et al, described the detection of a fully esterified Mpe pool in etiolated higher plants treated with ALA and 2,2'-dipyridyl.
56. 1981: Rebeiz et al, proposed a 4-branched Chl a biosynthetic pathway.
57. 1981: Santel and Apel, demonstrated that during greening of etiolated tissues a rapid decline of POR-A is observed. After six hours of continuous illumination, when the rate of Chl a accumulation is at its peak, only traces of the POR-A protein are detected.
58. 1981: Bazzaz, described a lethal maize mutant Nec 2, (ex-ON 2) which accumulates only DV Chl a and b.
59. 1982:Belanger and Rebeiz, detected the formation of MV Mg-Proto, MV Mpe and MV Mpe diester in higher plants.
60. 1982:Belanger et al, ascertained the chemical structure of DV Chlide a.
61. 1982:Duggan and Rebeiz, Described the induction of the massive accumulation of DV Chlide a in greening tissues.
62. 1982: Duggan and Rebeiz, detected [4-vinyl] chlorophylllide a reductase (4VCR) activity in higher plants.
63. 1982: Duggan and Rebeiz, detected the occurrence of Chlide b in higher plants.
64. 1982: McCarty et al, demonstrated that Pchlide a and Pchlide a phytyl ester are formed via two distinct biosynthetic routes in higher plants.
65. 1983:Rebeiz et al, proposed a 6-branched Chl a biosynthetic pathway.
66. 1984: Wu and Rebeiz, ascertained the chemical structure of DV Pchlide a, and DV Chlide a, by nuclear magnetic resonance (NMR) spectroscopy.
67. 1984:Daniell and Rebeiz, demonstrted that direct esterification of endogenous Chlide a with exogenous phytol in the presence of added ATP , and Mg was also observed, in etiochloroplasts, which led to the proposal that depending on the stage of plastid development, the conversion of Chlide a to Chl a may follow different biosynthetic routes having different substrate and cofactor requirements.
68. 1985:Wu and Rebeiz, ascertained the chemical structure of DV Chl b, by NMR spectroscopy.
69. 1985: Carey and Rebeiz, discovered the DV and MV greening groups of plants.
70. 1986: Tripathy and Rebeiz, demonstrated precursor-product relationships among the various MV and DV monocarboxylic routes of the proposed multibranched Chl a biosynthetic pathway.
71. 1988: Wu and Rebeiz, ascertained the chemical structure of 10-OH-Chl a lactone by NMR spectroscopy.
72. 1988: Tripathy and Rebeiz, Demonstrated that only part of the MV Pchlide a in DMV-LDV-LDMV plant species such as barley, can arise by vinyl reduction of DV Pchlide a, the rest of the MV Pchlide a pool, is formed via an independent route.
73. 1988: Chisholm et al, reported the the major Chl in some prochlorophytes is DV Chl a and b.
74. 1988:Walker et al, described the conversion of beta-OH and beta-keto methyl propionate to Pchlide a
75. 1991: Shedbalkar et al, detected the occurrence of MV Pchl(ide) b in higher plants.
76. 1992: Parham and Rebeiz, determined that NADPH is a mandatory cofactor for [4-vinyl] Chlide a reductase.
77. 1993:Porra et al, reported that mass spectra of [7-hydroxymethyl]-chlorophyll b extracted from leaves greened in the presence of either ¹⁸O₂ or H₂¹⁸O₂ revealed that ¹⁸O was incorporated only from molecular oxygen into the 7-formyl group of Chl b .
78. 1995: Armstrong et al, demonstrated that in Arabidopsis thaliana and Barley, two different genes PorA and PorB ( with about 75 % homology) code for two different protochlorophyllide oxidoreductases, namely POR-A and POR-B
79. 1995: Jensen et al, expressed the three Mg-Proto chelatase genes (chlI, chlD, and chlH) in E. coli, and demonstrated that the three cognate proteins are required for activity.
80. 1996: Kim and Rebeiz, detected [4-vinyl] Mg-Proto reductase.
81. 1997:Abd El Mageed et al, discovered the LD-DV and -MV greening groups of plants.

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