Photosynthesis Research 34: 329-332, 1992. © 1992 Kluwer Academic Publishers. Printed in the Netherlands.

Robert Hill, FRS; his published work Roger C. Prince Exxon Research and Engineering Company, Annandale, NJ 08801, USA Received 7 May 1992; accepted 12 May 1992

Robert Hill, FRS (1899-1991) is well known as a central figure in unravelling the marvels of photosynthesis. He was the first to persuade chloroplasts to produce significant amounts of oxygen upon illumination (Hill 1937a) (in what became known as the Hill reaction), and with Dr Fay Bendall proposed the scheme for electron transport within chloroplasts that became known as the Z-scheme (Hill and Bendall 1960a). His own recollections of his contributions are reviewed, with characteristic modesty, in 'The Biochemist's Green Mansions' (Hill 1965). But, as has been emphasized elsewhere (Porter 1979, Anonymous 1991, Rich 1992), Robert Hill was a polymath with broad interests in natural chemistry, and he made many important contributions to our understanding of haemoglobin and myoglobin, natural pigments and dyes, in addition to those on electron transfer reactions in photosynthesis; this brief paper attempts to outline some of them. Robin's earliest published work included his first on his famous camera (Hill 1924, see also Hill 1926a, Anderson 1992), and work on cobaltous compounds (Hill and Howell 1924) indicating that 4-coordinate (tetrahedral) compounds are blue while 6-coordinate (octahedral) compounds are red (the origin of the colour-indicating properties of some proprietary drying agents). Much of his early work focussed on mammalian heme proteins, especially haemoglobin (Hill 1925, 1926b, 1929, 1933, 1937b, Hill and Holden 1926a,b, 1927, Hill and Wolvekamp 1936) and myoglobin, then known as muscle haemoglobin (Hill 1936). One important finding was that haemoglobin could be resolved into globin and heme, and reconstituted (Hill and Holden 1926a,b). He also showed that myoglo-

bin had a higher affinity than haemoglobin for oxygen, and thus had the appropriate properties to be the intermediary carrier of molecular oxygen from the blood to the cytochrome oxidase of the cells. Furthermore, the higher affinity was attributable to the protein rather than to the heme (Hill 1933, 1936). He worked on cytochrome c with Keilin (Hill and Keilin 1930, 1933) and introduced aa-dipyridyl for the determination of iron in biological systems (Hill 1930); this method is still in use today. Robin's famous work on oxygen evolution by isolated chloroplasts used his knowledge of the oxygen-binding properties of hemoglobin in an elegant assay for oxygen involving the determination of oxyhaemoglobin (Hill 1937a, 1939, Hill and Scarisbrick 1940a,b, Hill and Whittingham 1953). But his interests in electron transport in plants included far more than just the oxygenevolving apparatus. They included the respiratory system from succinate to cytochrome oxidase (Hill and Bhagvat 1939, Bhagvat and Hill 1951), the interrelationship of iron and chlorophyll during the growth and senescence of leaves (Hill and Lehmann 1941), the photo-reduction of oxygen (Good and Hill 1955), and indeed all the oxidation-reduction reactions involved in both the photosynthetic (Hill 1951a,b, 1955, 1965, 1982, Hill and Whittingham 1957, Hill and Bonner 1961, Hill and San Pietro 1963, Bonnet and Hill 1963, Hill and Bendall 1965, West and Hill 1967, Bendall and Hill 1968) and non-photosynthetic (Bendall and Hill 1956) parts of plants. Robin also worked on the phosphorylation reactions that accompanied light-induced electron transport (Walker and Hill 1958, Hill and Walker 1959, Hill et al. 1976), and the relation of oxygen evolution and carbon dioxide fixation (Hill 1955, Walker and Hill 1967). He was also

330 interested in the phenomenon of delayed light emission in chloroplasts (Bertsch et al. 1969, 1971), and indeed in the overall efficiency of power conversion during photosynthesis (Hill 1977, 1982, Hill and Rich 1983). Robin was particularly interested in isolating various electron transfer components from plants. Hill and Scarisbrick (1951) identified cytochrome f (frons = leaf) in chloroplasts of a variety of plants, and it was eventually purified from parsley (Davenport and Hill 1952, Bendall et al. 1971). Similarly, ferredoxin (Davenport et al. 1952, Davenport and Hill 1955, 1960, Hill and Bendall 1960b, Bendall et al. 1963) and cytochrome b 6 (Hill 1954) were identified in a variety of species, and, with the exception of cytochrome b6, eventually purified from parsley

( Petroseleneum sativum). But Robin was also a skilled organic biochemist with interests in natural pigments and products. He was particularly interested in Britain's natural dye plants, Woad (Isatis tinctoria), Weld (Ruseda luteola) and Madder (Rubia peregrina), and he grew all three in his garden. He isolated and characterized a range of anthraquinone pigments from Madder (Hill 1934, Hill and Richter 1936a,b, 1937), and indeed even attempted to improve dye-stuff production by developing polyploid strains of the plant. He was fascinated by irritant plants, and isolated and characterized the vessicant substance of buttercups (Hill and van Heyningen 1951), and used similar isolation procedures to isolate and characterize dyestuffs from a wide variety of plants (Trim and Hill 1952). Robin even collaborated on studies to understand the plant compounds that attracted wireworms, and elicited their biting response (Thorpe et al. 1941). He used his organic synthesis skills to develop a series of phenolindophenols (Hill 1973) which were a significant improvement as Hill acceptors over earlier compounds (Hill et al. 1976), and appropriately, wrote two fine reviews of Joseph Priestley's discovery of photosynthesis (Hill 1972, 1978). Robin's breadth of understanding and interest in the natural world is seen in the diversity of plant species he used in his work. His first oxygen evolution work used the white deadnettle (Lamium album) and the common chickweed (Stellaria media), although it eventually extended

throughout the plant kingdom and to Chlorella (Hill et al. 1953). His cytochrome studies included Asparagus (Asparagus officianalis), Good-King-Henry ( Chenopodium bonus-henricus), Cock's foot grass ( Dactylis glomerulata), the potato (Solanum tuberosum) and of course spinach (Spinacea oleracea) (Hill and Scarisbrick 1951); his fondness for parsley has been noted above. The early studies on iron:chlorophyll ratios in developing and senescing leaves (Hill and Lehmann 1941) used Spring Beauty (Claytonia perfoliata), Elder (Sambucus racemosa) and Horse chestnut (Aesculus hippocastanum) and the work on dyestuffs (Trim and Hill 1952) examined literally dozens of common and exotic species, many of which could be found in his garden. Of course this catalog of Robin's published work reflects only a small part of his impact on plant science. As has been discussed elsewhere (Porter 1979, Anonymous 1991, Rich 1992), Robin's personality, and particularly his patience with beginners, was what endeared him to so many of us.

Acknowledgements The author is indebted to Dr P.L. Dedert and R. Baurkot for the literature search that led to this paper.

References Anderson JM (1992) Cytochrome b6f complex: Dynamic molecular organization, function and acclimation. Photosynth Res 34:341-357 (this issue) Anonymous (1991) Dr Robert Hill, The Times (London) March 21 Bendall DS and and Hill R (1956) Cytochromecomponents in the spadix of Arum maculatum.New Phyto155:206-212 Bendall DS and Hill R (1968) Haem proteins in photosynthesis. Ann Rev Plant Physiol 19:167-186 Bendall DS, Gregory RPF and Hill R (1963) Chloroplast ferredoxin from parsley. Biochem J 88:29-30 Bendall DS, Davenport HE and Hill R (1971) Cytochrome components in chloroplasts of the higher plants. Methods Enzymol 23A: 327-344 Bertsch W, West J and Hill R (1969) Delayedlight studies on photosynthetic energy conversion. II. Effect of electron acceptors and phosphorylationcofactorson the millisecond

331 emission from chloroplasts. Biochim Biophys Acta 172: 525-538 Bertsch W, West J and Hill R (1971) Delayed light studies on photosynthetic energy conversion. Ill. Effect of 3-(3,4dichlorophenyl)-l,l-dimethylurea on the millisecond emission from chloroplasts performing photoreduction of ferricyanide. Photochem Photobiol 14:241-250 Bhagvat R and Hill R (1951) Cytochrome oxidase in higher plants. New Phytol 50:112-120 Bonner WD and Hill R (1963) Light-induced optical changes in green leaves. Natl Acad Sci, Natl Res Council Publ 1145:82-90 Davenport HE and Hill R (1952) The preparation and some properties of cytochrome f. Proc Roy Soc B139:327-345 Davenport HE and Hill R (1955) A protein fraction from leaves catalysing reduction of methaemoglobin by isolated chloroplasts. Abstracts 3rd. Intern, Congr. Biochem. pp 103. Brussels Davenport HE and Hill R (1960) A protein from leaves catalysing the reduction of haemprotein compounds by illuminated chloroplasts. Biochem J 74:493-501 Davenport HE, Hill R and Whatley FR (1952) Natural factor catalysing reduction of methaemoglobin by isolated chloroplasts. Proc. Roy Soc B139:346-358 Good N and Hill R (1955) Photochemical reduction of oxygen in chloroplast prepartions and in green plant cells. II. Mechanisms of the reaction with oxygen, Arch Biochem Biophys 57:355-366 Hill R (1924) A lens for whole sky photographs. Quart J Roy Met Soc 50:227-235 Hill R (1925) Haemoglobin in relation to other metallohaematoporphyrins. Biochem J 19:341-349 Hill R (1926a) A lens for whole sky photography. Proc. Optical Convention 1926, part II, 1-6 Hill R (1926b) Chemical nature of haemochromogen and its carbon monoxide compound. Proc Roy Soc 100B: 419-430 Hill R (1929) Reduced haematin and haemochromogen. Pr0c Roy Soc B105:112-130 Hill R (1930) Method for the estimation of iron in biological material. Proc Roy Soc B107:205-214 Hill R (1933) Oxygen affinity of muscle haemoglobin. Nature 132:897-898 Hill R (1934) A new glucoside from madder. Nature 134:628 Hill R (1936) Oxygen dissociation curves of muscle haemoglobin. Proc Roy Soc B120:472-483 Hill R (1937a) Oxygen evolved by isolated chloroplats. Nature I39:881-882 Hill R (1937b) Haemoglobin. In: Needham J and Green D E (eds) Perspectives in Biochemistry, pp 127-136. Cambridge University Press Hill R (1939) Oxygen produced by isolated chloroplasts. Proc Roy Soc B127:192-210 Hill R (1951a) Reduction by chloroplasts. In: Symposium Soc Exptl Biol Vol 5, pp 222 231. (Carbon Dioxide Fixation and Photosynthesis) Hill R (1951b) Oxidoreduction in chloroplasts. Advances in Enzymol 12:1 39 Hill R (1954) The cytochrome b component of chloroplasts. Nature 174:501-503

Hill R (1955) Cytochrome components and chlorophyll in relation to the carbon cycle of Calvin. In: Proc 3rd Intern Congr Biochem, pp 225-227. Brussels Hill R (1965) The biochemists' green mansions: the photosynthetic electron transport chain. Essays in Biochemistry 1:121-151 Hill R (1971) Joseph Priestley (1733-1804) and his discovery of photosynthesis in 1771. In: Photosynthesis Two Centuries after its discovery by Joseph Priestley. Proc. 2nd Int. Congr. Photosynth. Vol. 1, pp 1-18. Hill R (1973) Old and some possible new redox indicators. J Bioenerg 4:229-237 Hill R (1977) Some tentative questions about radiant energy and its conversion in chloroplasts. Plant Cell Physiol Special Issue 3 : 4 7 - 5 4 Hill R (1978) Oxygen evolution; some historical aspects. Biochem Soc Trans 6:901-904 Hill R (1982) Cytochromes and redox systems in photosynthesis. In: Kaplan NO and Robinson A (eds) From Cyclotrons to Cytochromes, A Symposium in Honor of Martin Kamen, pp 299-303. Academic Press, New York Hill R and Bendall F (1960a) Function of the two cytochrome components in chloroplasts, a working hypothesis. Nature 186:136-137 Hill R and Bendall F (1960b) Crystallization of a photosynthetic reductase from a green plant. Nature 187:417 Hill R and Bendall DS (1965) Oxidation~reduction potentials in relation to components of the chloroplast. Biochem Chloroplasts Proc. Aberystwyth, Wales, 2:559-564 Hill R and Bhagvat K (1939) Cytochrome oxidase in flowering plants. Nature 143:726 Hill R and Bonner WJ (1961) The nature and possible function of chloroplast cytochromes. John Hopkins University McCollum-Pratt Institute Contrib 302:424-435 Hill R and Holden HF (1926a) The reaction between globin and haematin. J Physiol 61: xxii Hill R and Holden HF (1926b) Preparation and some properties of the globin of oxyhaemoglobin. Biochem J 20: /326-1329 Hill R and Holden HF (1927) Reduction of haematin and methaemoglobin. Biochem J 21:625-631 Hill R and Howell OR (1924) Crystal structure and absorption spectra. Phil Mag 48:833-846 Hill R and Keilin D (1930) Porphyrin of component c of cytochrome and its relationship to other porphyrins. Proc Roy Soc BI07:286-292 Hill R and Keilin D (1933) Estimation of haematin iron and the oxidation-reduction equivalent of cytochrome c. Proc Roy Soc B114; 104-109 Hill R and Lehmann H (1941) Studies of iron in plants with special observations on the chlorophyll:iron ratio. Biochem J 23:1190 1199 Hill R and Rich PR (1983) A physical interpretation for the natural photosynthetic process. Proc Nat] Acad Sci USA 80:978-982 Hill R and Richter D (1936a) Glucosides of madder. Nature 138:38 Hill R and Richter D (1936b) Anthraquinone colouring matters: Gallosin: rubiadin primveroside. J Chem Soc 1936:1714-1719

332 Hill R and Richter D (1937) Anthraquinone pigments in Galium. Proc Roy Soc B121:547-560 Hill R and San Pietro A (1963) Hydrogen transport with chloroplasts. Z Naturforsch 18b: 677-682 Hill R and Scarisbrick R (1940a) Production of oxygen by illuminated chloroplasts. Nature 146:61-62 Hill R and Scarisbrick R. (1940b) Reduction of ferric oxalate by isolated chloroplasts. Proc Roy Soc B129:238-255 Hill R and Scarisbrick R (1951) The haematin compounds of leaves. New Phytol 50:98-111 Hill R and van Heyningen R (1951) Ranunculin: the precursor of the vessicant substance of buttercup. Biochem J 49:332-335 Hill R and Walker DA (1959) Pyocyanine and phosphorylation with chloroplasts. Plant Physiol 34:240-245 Hill R and Whittingham CP (1953) Induction phase of photosynthesis in Chlorella determined by spectroscopic method. New Phytol 52:133-148 Hill R and Whittingham CP (1957) Photosynthesis. Methuen and Co., London Hill R and Wolvekamp HP (1936) Oxygen dissociation curve of haemoglobin in dilute solution. Proc Roy Soc B120: 484-495 Hill R, Northcote DH and Davenport HE (1953) Production of oxygen from chloroplast preparations. Active chloro-

plast preparations from Chlorella pyrenoidosa. Nature 172: 948-949 Hill R, Crofts AR, Prince RC, Evans EH, Good NE and Walker DA (1976) Uncoupling of electron transport by anionic quinonoid redox indicator dyes. New Phytol 77: 1-9 Porter G (1979) In: Robert Hill, A Tribute from Friends and Colleagues on his Eightieth Birthday, pp 1-2. Rampant Lions Press, Cambridge Rich PR (1992) Robin Hill: A personal perspective. Photosynth Res 34:333-335 (this issue) Thorpe WH, Crombie AC, Hill R and Darrah JH (1947) The behaviour of wireworms in response to chemical stimulation. J Exptl Biol 23:234-266 Trim A R and Hill R (1952) Preparation of aucubin, asperuloside, and some related glycosides. Biochem J 50: 310-319 Walker DA and Hill R (1958) Phosphorylation by illuminated chloroplast preparations. Biochem J 69: 57-58. Walker DA and Hill R (1967) The relation of oxygen evolution to carbon assimilation with isolated chloroplasts. Biochim Biophys Acta 131:330-338 West J and Hill R (1967) Carbon dioxide and the reduction of indophenol and ferricyanide by chloroplasts. Plant Physiol 42:819-826

Robert Hill, FRS; his published work.

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