n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c REVIEWS OPEN ACCESS Nobel Prizes for Research in Plant Science: Past, Present and Future Natsuki Hayami and Sachi Sri Kantha1

1 The Graduate School of Agricultural Sciences, Gifu University, Yanagido 1-1, Gifu City 501-1193, Japan.

ABSTRACT The Nobel Prizes awarded in two appropriate science categories (chemistry as well as physiology or medicine) and the peace category since 1901 were studied to evaluate the plant science related research that had received recognition. We also checked the Nobel prize nomination database for the two appropriate science categories to verify the number of scientists (with research reputation on plant-based studies) who were nominated, but were unlucky in the eventual selection process. The focus of this review is research on plant materials in a wider sense (including that of photosynthetic bacteria), that received Nobel prize recognition. Until 2017, Nobel Prizes for research in plant sciences have been awarded 17 times to 20 scientists. Pioneering work on five major research themes, namely, (1) chlorophyll and photosynthesis, (2) elucidation of the structure of vitamins (carotene, thiamin, ascorbic acid and vitamin K), (3) use of radioisotopes for metabolism studies, (4) plant natural product chemistry and (5) plant genetics had received Nobel award recognition so far. For future recognition, Nobel laureates such as Melvin Calvin and Barbara McClintock had opined the worth of interdisciplinary teams with expertise in botany for trend-setting new discoveries in plant science research. We predict that pioneering studies along the line of plants that can grow in a dessert or sea, plants which can be an enriched source of fuel and hydrocarbon-like materials may have potential to be considered for a Nobel Prize for plant science research. Keywords: cytogenetics, photosynthesis, plant breeding, plant natural products, vitamins

Introduction three were awarded for plant-related research).” We presume that Alfred Nobel (1833-1896) was a Swedish chemist, engineer, Gresshof’s (2002) count, derives from information scientist Garfield inventor, businessman, and philanthropist. His creative (1987) who had identified three Nobelists (Richard Willstatter, productivity includes over three hundred worldwide patents Robert Robinson and Melvin Calvin) as those who had been including that of dynamite. According to his famous will of 1895, recognized for research in plant-related sciences. Garfield (1987) Nobel’s fortune was to be used to establish the Nobel Prizes for did identify a major reason why research on plants receive less sciences (Chemistry, Physics and Medicine or Physiology), apart recognition and have less visibility; it may be because “they are not from that of Literature and Peace (Sohlman and Schuck, 1929； perceived as having a direct bearing on human health”. Is this so? Sri Kantha, 1999). These prizes were first bestowed in 1901 and How can humans, livestocks and other herbivorous animals survive announcement of these prizes in October still continue to be a and lead healthy lives without feeding on plant-based foods? news-worthy annual event for their merit and glamor (Sohlman, 1983; Garfield and Welljams-Dorof, 1992; Feldman, 2000; Stimulated by these thoughts, we studied the Nobel Prizes Levinovitz and Ringertz, 2001). awarded in two appropriate science categories (chemistry as well as physiology or medicine) and the peace category since 1901 for Between 1901 and 2017, the Nobel Prizes for chemistry as an alternate count. We also checked the Nobel prize nomination well as medicine or physiology categories have been awarded to database for the two appropriate science categories to verify the 178 and 214 individuals respectively. Previously, Gresshoff (2002) number of scientists (with research reputation on plant-based had expressed an editorial opinion related to research on plant studies) who were nominated, but were unlucky in the eventual biotechnology that, “There is no Nobel Prize for plant science, selection process. This derives from the concept of belonging to preventing the popular press from featuring achievements in this the ‘Nobel class’ introduced by Garfield (1980) that there are far area (NB, since the inception of Nobel Prizes one century ago, only more scientists whose work is worthy of the Nobel prize than the

Received October 10, 2017, Revised October 20, 2017, Accepted October 24, 2017. 83 Published on line: December 12, 2017. Correspondence to S.S.: [email protected] ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83 highest number (only 3) of prizes awarded each year for a specific Richard Willstatter (1872-1942) category. Thus, to be duly nominated for the Nobel prize deserves Hans Fischer (1881-1945) recognition because the findings of these scientists were ‘major Paul Karrer (1889-1971) breakthroughs’ in shaping the advances in science. Richard Kuhn (1900-1967) George de Hevesy (1885-1966) Past Record Arturi Virtanen (1895-1973) As presented in Table 1, since 1901, Nobel Prizes for research Robert Robinson (1886-1975) in plant sciences have been awarded 17 times to 20 scientists. The Melvin Calvin (1911-1997) focus of this review is research on plant materials in a wider sense Peter Mitchell (1920-1992) (including that of photosynthetic bacteria), that received Nobel prize Johann Deisenhofer (b.1943) recognition. We disregard specific disciplinary categories such as Robert Huber (b.1937) botany and microbiology. Why? A simple explanation is that scientists Hartmut Michel (b. 1948) frequently switch their research interests depending on factors such as availability of research funding, resources in proximity, collaborators Richard Willstatter was awarded the Nobel Chemistry Prize as well as personal preferences. The identifying criterion used for this for his research on plant pigments in 1915 (Trauner, 2015). It survey is whether research on plants and plant-derived materials had was the first time that Nobel Prize recognition was bestowed for been mentioned in the laureate’s Nobel award lectures. 18 among research in plant sciences. Willstatter was an organic chemist who the 20 scientists do satisfy this criterion. The sole exceptions were studied chemistry under Adolf von Baeyer. While in his twenties, Richard Kuhn and Edward A. Doisy, because they did not deliver Willstatter clarified the chemical structure of tropine, atropine their Nobel award lectures. and cocaine. (Adams, 1943). Subsequently, he began to focus on chlorophyll and anthocyanin pigments. Willstatter and his team Nobel Prizes for Chemistry discovered that the chlorophyll of different plant species is the Between 1915 and 1988, twelve scientists had received same, but it is a mixture of two different types; chlorophyll a and recognition for plant science research in the category of Nobel chlorophyll b. He showed that magnesium is an essential part of Chemistry award. (Fig. 1) They were, chlorophyll’s structure and pointed out chlorophyll’s relationship

Fig.1 Titles of Nobel Lectures delivered by 11 Chemistry Laureates, excluding Richard Kuhn

84 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

Table 1: Nobel Prizes for Research on Plant Sciences Year Scientist (country) Field Research Recognition CHEMISTRY 1915 Richard Willstatter (Germany) natural products chemistry ‘for his researches on plant pigments, especially chlorophyll’

1930 Hans Fischer (Germany) natural products chemistry ‘for his researches into the constitution of haemin and Chlorophyll and especially for his synthesis of haemin’

‘ ’ 1937 Paul Karrer (Switzerland) natural products chemistry for his investigations on carotenoids, flavins and vitamins A B2

1938 Richard Kuhn (Austria) natural products chemistry ‘for his work on carotenoids and vitamins’

1943 George de Hevesy (Sweden) nuclear chemistry ‘for his work on the use of isotopes as tracers in the study of chemical processes

1945 Artturi Virtanen (Finland) agricultural chemistry ‘for his research and inventions in agricultural and nutrition chemistry, especially for his fodder preservation method’

1947 Robert Robinson (UK) natural products chemistry ‘for his investigations on plant products of biological importance, especially the alkaloids’

1961 Melvin Calvin (USA) biochemistry ‘for his research on the carbon dioxide assimilation in plants’

1978 Peter Mitchell (UK) biochemistry ‘for his contribution to the understanding of biological energy transfer through the formulation of the chemiosmotic theory’

1988 Johann Deisenhofer (Germany) biochemistry ‘for the determination of the three-dimensional structure of a photosynthetic reaction centre’ Robert Huber (Germany) Hartmut Michel (Germany)

MEDICINE or PHYSIOLOGY

1929 Christiaan Eijkman nutrition, metabolism ‘for his discovery of the antineuritic vitamin’ (Netherlands)

1937 Albert Szent-Gyorgyi cell physiology, nutrition ‘for his discoveries in connection with the biological combustion (Hungary) process with special reference to vitamin C and the catalysis of fumaric acid’ 1943 Henrik Dam (USA) nutrition ‘for his discovery of vitamin K’ Edward A. Doisy nutrition ‘for his discovery of the chemical nature of vitamin K’

1950 Tadeus Reichstein (Switzerland) biochemistry ‘for discovery relating to the hormones of the adrenal cortex, their structure and biological effects”

1983 Barbara McClintock (USA) genetics ‘for her discovery of mobile genetic elements’

2015 Youyou Tu (China) pharmacology ‘for her discoveries concerning a novel therapy against malaria’ (artemisinin from Artemisia family of plants)

PEACE 1970 Norman Borlaug (USA) humanitarian work ‘developing high yield grains credited with helping to alleviate World hunger’ (contribution to ‘The Green Revolution’ – development of dwarf wheat and rice varieties)

©2017 Reviews in Agricultural Science 85 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83 with the hemoglobin in red blood cells (Willstätter, 1920). for his research and inventions in agricultural and nutrition - Willstatter also pioneered in investigating anthocyanin pigments especially for his fodder preservation method (Virtanen, 1945). (Robinson, 1932; Blank, 1947). Virtanen’s focus was on preserving food nutrients in plants of countries with cold winters. Towards this aim, his group In 1930, Hans Fischer received the Nobel Chemistry Prize for his studied the chemistry of nutrients in plants and nitrogen fixation researches into the constitution of hemin and chlorophyll. He studied by legumes (Virtanen, 1936; Virtanen and Laine, 1936, 1938a, pigmented substances of biological importance (Fischer, 1930). 1938b, 1946; Virtanen and Arhimo, 1939; Virtanen et al., 1938, 1939), including those which contributes to the formation of In 1937, organic chemist Paul Karrer received recognition with dairy products and developed a method for better preservation of the Nobel Chemistry prize for his investigations on carotenoids, nutrients in hay. Using hydrochloric and sulfuric acids, Virtanen

flavins and vitamins A and B2 (Karrer, 1937; Wettstein, 1972; Isler, impeded certain processes, preserving the proteins and vitamins 1978), and for demonstrating that in 1931 that vitamin A (retinol) in grass. This helped cows to produce more nutritious milk year is related to carotenoids in structure, in resembling half a molecule round without imported fodder (Miettinen, 1975). of a typical carotenoid (Karlson, 1978; Asimov, 1982). Apart from carotenoid research, Karrer also contributed his share to the (1) Robert Robinson, honored with the 1947 Nobel chemistry structural identification of other vitamins such as ascorbic acid prize, pioneered in ploughing the field of plant alkaloids such (Svirbely and Szent-Gyorgyi, 1933) and vitamin K (Dam, 1940), as quinine, strychnine, morphine and cocaine (Robinson, 1947; (2) characterization of anthocyanin pigments (Blank, 1947), and (3) Todd and Cornforth, 1976; Saltzman, 1986); thus, for his times, he characterization of lichenin from lichens (Perez-Llano, 1944). became one of the prolific organic chemists (Baglow and Bottle, 1979). Robinson elucidated the structure of morphine in 1925 The 1938 Nobel chemistry prize was awarded to Richard and strychnine in 1946 (Chakravarti et al., 1947; Openshaw and Kuhn in 1939, ‘for his work on carotenoids and vitamins’. Robinson, 1946; Pausaker and Robinson, 1947; Robinson, 1947; Kuhn received his Ph.D degree under the direction of Richard Asimov, 1982). For 20 years, Robinson had received 51 Nobel Willstatter; he subsequently worked on the synthesis of vitamin chemistry prize nominations cumulatively from 1928 to 1947

A, and was the first to isolate vitamin B6 (pyridoxine) in pure (Sir Robert Robinson nominations, 2017). Apart from alkaloids, form (Westphal, 1968; Asimov, 1982). Independently of Karrer, Robinson also enriched our knowledge on other plant derived Kuhn also distinguished three types of carotenes (β-carotene, α compounds like anthocyanins (Robinson, 1936, 1947). carotene and γ carotene) which were identified as the precursors of retinol (Bauernfeind, 1972; Shampoo and Kyle, 2000). Melvin Calvin was awarded the 1961 Nobel Chemistry Prize for his research on the carbon dioxide assimilation in plants (Moses, George Hevesy pioneered in introducing radioisotope tracers 1997; Schulz, 1997). Calvin and his colleagues Andrew Benson and for the first time to a biological problem (Anon, 1961). Hevesy James Bassham traced the path taken by carbon through different used thorium B (Pb212) to study the absorption and translocation stages of photosynthesis using radioactive isotopes in single- of lead nitrate in horse bean (Vicia faba) and P32 in maize to study cell green algae, Chlorella. They showed that sunlight acts on the plant metabolism (Hevesy, 1923; Hevesy et al., 1936; Burris, chlorophyll in a plant due to the manufacture of organic compounds, 1950). Though subsequently Hevesy moved on to study the use rather than on carbon dioxide as was previously believed (Calvin, of radioisotope tracers in animal and human tissues, in his Nobel 1961, 1989; Seaborg and Beson, 1998). lecture, he had observed the following: “Ions taken up by the plant can be removed by an exchange process under the action Peter Mitchell received the 1978 Nobel chemistry prize, for of other ions present in the soil or in the nutrient solution. It was his formulation of chemiosmotic theory to explain the biological already found in 1923 that minute amount of lead, labelled by the energy transfer in the cells of green plants, green algae and certain admixture of the lead isotope thorium B, when taken up by the bacteria during photosynthesis and how cholorophyll converts roots of Vicia faba, could to a large extent be removed by an excel carbon dioxide and water into organic compounds (Mitchell, 1961, of non-labelled lead added to the nutrient solution. Most other 1966, 1967, 1977, 1978; Hinkle and Garlid, 1992). It should be ions were found to be much less effective in removing the labelled noted that Mitchell had collaborative support from Jennifer Moyle lead ions from the plant.” (Hevesy, 1944). (1921 – 2016) and Peter Scholes. There was initial skepticism for the chemiosmotic hypothesis among peers (Lehninger, 1967; Artturi Virtanen was awarded the Nobel Chemistry Prize Huszagh and Infante, 1989; Slater, 1994) for the mechanism of

86 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c energy conservation during electron transport in the mitochondrion, Nobel Prize for Medicine of Physiology when the rival chemical coupling hypothesis was supported Between 1929 and 2015, seven scientists had received by other researchers (Slater, 1953; Racker, 1967). But, with the recognition for plant science research in the category of Nobel discovery of ATP synthase enzyme by Racker and his colleagues Medicine/Physiology award. They were, (Kresge et al., 2006) and the finding that a pH difference across Christiaan Eijkman (1858-1930) the thylakoid membrane in the spinach chloroplasts leads to ATP Albert Szent-Gyorgyi (1893-1986) synthesis (Jagendorf and Uribe, 1966; Jagendorf, 1967), Mitchell's Henrik Dam (1895-1976) chemiosmotic theory came to be accepted eventually. In this Edward A. Doisy (1893-1986) aspect, thoughts of Mitchell (1970) maybe of some relevance to Tadeus Reichstein (1897-1996) other researchers, because experimentalists in biosciences have Barbara McClintock (1902-1992) been blamed for their reluctance in advancing plausible hypotheses Youyou Tu (b.1930) (Huszagh and Infante, 1989). According to Mitchell (1970), “the practical utility of a concept or of a hypothesis depends, not on Christiaan Eijkman, a physician, was recognized in 1929 for his the proof of its validity, but on the extent to which it opens up discovery of the antineuritic vitamin. Eijkman found that hens fed avenues for research and comprehension by providing a basis polished rice were afflicted by neuritic symptoms, and identified for the precise formulation of experimentally testable questions.” that there was a substance in the rice husk that counteracted the Mitchell’s success in proving his chemiosmotic hypothesis illness (Merritt and Tan, 2011). The substance that counteracts may be attributed to the tenacity in using many experimental beriberi subsequently was designated vitamin B1 or thiamine models such as photosynthetic bacteria Rhodospirillum rubrum, (Eijkman, 1929; Rosenfeld, 1997, Verhoef et al., 1999). Rhodopseudomonas spheroides, Anabaena variabilis and spinach chloroplasts (Mitchell, 1967). In 1937, Albert Szent-Gyorgyi (1893-1986) received the Nobel Medicine or Physiology Prize for his discoveries in connection Johann Deisenhofer, Robert Huber and Hartmut Michel with the biological combustion processes, with special reference received the 1988 Nobel Chemistry prize for the determination to vitamin C and the catalysis of fumaric acid. Szent-Gyorgyi was of the three-dimensional structure of a photosynthetic reaction one of the great experimental biochemists of the 20th century, who center in photosynthetic bacterium (Rhodopseudomonas viridis). didn’t have qualms in choosing either plant or animal materials A photosynthetic reaction center is a protein-pigment complex for his experiments (Edsall, 1986). By his own admission, he was from photosynthetic membranes that perform the primary charge also a wild theorist, as well as a philosopher and a humorist. The of separation. This complex consists of 4 protein subunits, 4 way Szent-Gyorgyi (1963) progressed in isolating, identifying and molecules of chlorophyll, 2 molecules of pheophytin and 2 naming ascorbic acid (vitamin C) had been recorded for posterity. molecules of quinones. For the first time, Michel (1982) succeeded in crystallizing a membrane protein. Among these three laureates, We provide few excerpts to illustrate Szent-Gyorgyi’s rare Deisenhofer is a trained physicist, Michel - a molecular biologist story telling talent. and Huber – structural chemist and protein crystallographer. In “…I also became interested in vegetable respiration, being an unusual pattern rarely seen among Nobel science laureates, convinced that there is no basic difference between man and the Deisenhofer, Huber and Michel had published shared co-author grass he mows. Plants, at that time, were divided into two groups: papers (Deisenhofer et al., 1984, 1985a, 1985b), which attest to their the ‘catechol oxidase’ and ‘peroxidase’ plants. I started with collaborative effort in seeking a solution to the mystery behind the the catechol oxidase plants which contain catechol and a strong “most important chemical reaction on earth”, as touted in the press catechol oxidase. I simplified the accepted, rather complex ideas release of the Royal Swedish Academy of Sciences in announcing about this oxidation system. Then, I shifted to ‘peroxidase plants’ the word. The mystery here is, how electrons can be transferred which are called so because they contain peroxidase in high in biological system at a speed of billionth of a second (i.e., 10-12 concentration. If peroxide is added to a mixture of peroxidase and sec). For this Deisenhofer and his two colleagues choose to work benzidine, immediately an intense blue color appears due to the with a photosynthetic purple bacterium, a simpler model than that oxidation of benzidine. I found that if the reaction was performed of an algae or higher plant. Combining multiple methods such as with the plant juice, instead of purified peroxidase, there was a picosecond (10-15) absorption spectroscopy, X-ray crystallography very short delay, of a second or so, in the benzidine reaction. This and molecular biology from different disciplines proved to be fascinated me. There had to be present a reducing agent which valuable in solving the mystery (Lewin, 1988; Levi, 1989). reduced the oxidized benzidine, the delay corresponding to the

©2017 Reviews in Agricultural Science 87 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83 time necessary to oxidize away this unknown reducing agent, later In 1943, Henrik Dam and Edward Doisy jointly received Nobel to be known as ascorbic acid.” Medicine or Physiology prize to recognize their contributions for the discovery and isolation of anti-haemorrhagic vitamin K compounds In addition, Szent-Gyorgyi had described how his humorous pun from plants, mainly from alfalfa leaves (Olson, 1979). Dam (1934, on naming a newly identified sugar failed to pass the muster from the 1935) proposed the name ‘vitamin K’ for the antihaemorrhagic factor disciplinarian eyes of Arthur Harden (a biochemist cum editor, who which was not identical to ascorbic acid, because it is fat soluble was honored with the 1929 Nobel prize in chemistry) as follows: (Dam, 1935; Morton, 1976). In the late 1930s, Dam and his colleagues extended their studies on this vitamin to report that it is rich in “In Cambridge I isolated the reducing agent found at hemp seed and certain vegetables such as tomatoes and kale, and Groningen. I crystallized it from oranges, lemons, cabbages and to a less degree in many cereals (Dam, 1937, 1940, 1943; Dam and adrenal glands. I knew it was related to sugars, only did not Schonheyder, 1936; Dam and Lewis, 1937; Dam and Glavind, 1938, know which. ‘Ignosco’ meaning ‘don’t know’ and the ending Dam et al.,1947). Doisy’s group focused on isolation, distillation and ‘ ’ ‘ ’ ose meaning sugar, I called this carbohydrate Ignose . Harden, crystallization of two types of vitamin K – vitamin K1 (phylloquinone, the editor of the Biochemical Journal, did not like jokes and empirical formula C31H46O2) from alfalfa and vitamin K2 ‘ ’ reprimanded me. Godnose was not more successful and so, (menaquinone-n, empirical formula C40H54O2) from putrified fishmeal following Harden’s proposition, I called the new substance (Doisy, 1976; Bingley et al., 1939a, 1939b, 1940; MacCorquodale et ‘hexuronic acid’ since it had 6C’s and was acidic. I got my Ph.D al., 1939; Doisy et al., 1940). for it.” [Ignose = ‘I don’t know’; Godnose = ‘God knows’] Tadeus Reichstein received one third of the share of 1950 In his original paper (Szent Gyorgyi, 1928), the specific Nobel Medicine or Physiology prize for his studies on the sentence appears as, “Since the exact constitution of the reducing hormones of adrenal cortex, their structure and biological effects. substance is unknown, I propose to refer to it as a hexuronic In his Nobel lecture entitled, ‘Chemistry of the adrenal cortex acid.” The ‘peroxidase’ plants analyzed by Szent-Gyorgyi were, hormones’, Reichstein (1950) had described his African adventure turnip (Brassica rapa), Spanish black radish (Rafanus sat. niger), in finding Strophantus seeds to isolate cardiac glycoside leek (Allium porrum), Spanish onion (Allium cepa), pineapple sarmentogenin. Though Reichstein received his Nobel prize at the (Ananas sativus), tomato (Solanum lycopersicum), orange age of 53, his research in the subsequent four decades were plant (Citrus aurantium), lemon (Citrus lemonum), grape fruit (Citrus oriented. It appears that Reichstein was a phytophile of all grades decumana) and cabbage (Brassica oleracea). – tendering greenhouses, growing ferns, flowers and wild plants. He published well over 100 papers on ferns, during his post-Nobel How hexuronic acid became ascorbic acid due to the award career (Rothschild, 1999). collaboration with a young scientist was described by Szent- Gyorgyi (1963) as follows: Barbara McClintock was awarded the 1983 Nobel Medicine or Physiology Prize for her discovery of mobile genetic elements “One day a nice young American-born Hungarian J. Swirbely (Anon, 1983; Burr and Burr, 1983). She was a cytogeneticist and came to Szeged to work with me. When I asked him what he knew had earned a PhD in botany. McClintock studied corn’s (Zea he said he could find out whether a substance contained vitamin mays) hereditary characteristics, for example the different colors C. I still had a gram or so of my hexuronic acid. I gave it to him of its kernels. She proved that genetic elements can sometimes to test for vitaminic activity... Swirbely tested hexuronic acid. change position on a chromosome and that this causes nearby A full test took two months but after one month the result was genes to become active or inactive (McClintock, 1965; Comfort, evident: hexuronic acid was Vitamin C. We made no secret of this 2001). McClintock’s finding of transposon in corn was a trend and finished the test which left no doubt about the identity. So, we setting discovery (McClintock, 1965; Comfort, 2001). Later (Haworth and I) rebaptized hexuronic acid to ‘ascorbic acid’. ” studies had revealed that transposon exists not only in plants but also in other organisms including human (Mills et al., 2007). Based on the results of guinea pig feeding experiments using juices of lemon and paprika (Hungarian red pepper Capsicum In 2015, Youyou Tu was honored with the Nobel Medicine annuum), Szent-Gyorgyi proved that hexuronic acid (= ascorbic or Physiology Prize for her discoveries concerning a novel acid) possess antiscorbutic effect (Svirbely and Szent-Gyorgyi, therapy against malaria (Owens, 2015; Chen, 2016; Molyneux and 1932, 1933; Rosenfeld, 1997). Ward, 2015; Xie, 2016). In a correspondence, Zhai et al. (2016)

88 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c complimented the 84- year old woman scientist Tu ‘as a “three Sanger, 1942), the only one scientist to receive two Nobel prizes nos” professor (a professor with no doctorate, no background for chemistry in 1958 and 1980, was on the nitrogen and amino of studying abroad and no membership in any Chinese national acid contents of different domestic varieties of British potato! academies)’! Malaria is caused by 4 species of single-cell parasite Plasmodium (P. malariae, P. ovale, P. vivax, and P. falciparum) Theodor Svedberg (1884-1971) was a Swedish physical chemist, that causes malarial fever. Tu is a pharmaceutical chemist. who was awarded the 1926 Nobel prize in chemistry, for his “work According to her, in late 1960s (during the height of the Cultural on disperse systems” and devising the ultracentrifuge to separate Revolution) she was appointed as the head of the Malaria control biological molecules with large molecular weights. Before the (abbreviated as the National 523 Office) and was assigned the conclusion of his Nobel award lecture, delivered on May 19, 1927, task of searching antimalarial drugs used in traditional Chinese Svedberg (1927) had reported his preliminary data on the molecular medicine. Within three months, Tu was able to collect “2,000 weights of proteins phycocyanin (blue) and phycoerythrin (red) herbal, animal and mineral prescriptions” from malaria and reduced isolated from red alga Ceramium. Subsequently, quite a number of the number to “640 prescriptions”. Traditional Chinese medicine publications from Svedberg lab had described studies on proteins uses sweet wormwood (Artemisia annua L.) to treat malarial isolated from ‘nori’ Porphyra tenera (Svedberg and Katsurai, 1929), fever. Tu and her colleagues found out that though there are 6 Manitoba wheat flour (Krejci and Svedberg, 1935), carbohydrates in species of Artemisia genus, only A. annua contains meaningful plant juices (Svedberg and Gralen, 1938) and cellulose (Gralen and quantities of artemisinin. Tu and her team then isolated and Svedberg, 1943; Svedberg, 1947). Svedberg was also an influential purified, artemisinin (Qinghaosu in Chinese) in 1972, which can personality on the Nobel award selection process, during the first inhibit the malaria parasite (Tu, 2011, 2015). Early success using quarter of the 20th century. Artemisia extracts on malaria-infected monkeys was reported in March 1972. Background to artemisinin research by Tu and her As a mentee of Robert Robinson at the Oxford University, team has been reviewed by White et al. (2015) and Guo (2016). Alexander Todd (1907-1997) studied the constituents of flower pigments, and his D. Phil thesis submitted to the Oxford University in Nobel Prize for Peace 1933 was entitled, ‘Diglucosidic anthocyanins’ (Brown and Kornberg, American plant breeder Norman Borlaug (1914-2009) was 2000). Before he began his Nobel-prize recognized research on the honored with the Nobel Peace Prize in 1970 for his contribution structure and synthesis of nucleosides and nucleotides, Todd and his to “the Green Revolution”. He developed semi-dwarf, high-yield, colleagues published a series of papers on the active principles of disease-resistant wheat varieties in Mexico (Borlaug, 1944, 1965; Cannabis indica (hemp, cannabis resin, aka hashish) in ten parts! Brown, 1970). Borlaug also introduced dwarf wheat into India (Todd, 1939, 1940, 1946; Jacob and Todd, 1940). Brown and Kornberg and Pakistan, and production increased enormously. This form (2000) had recorded Todd’s remembrance of what happened after the of ‘Green Revolution’ have the potential to save over a billion first publication of his paper on the chemical constituents of Cannabis people globally from starvation (Borlaug, 1970, 1983, 2000, 2002, (Work et al., 1939). To quote, 2007). The yield of crop was increased two to three fold by “the “a call to appear at the [British] Home Office led to his [i.e., Green Revolution” (Borlaug, 2002). Since then, increase in yield Todd’s] registration as a holder of 2½ kg of the proscribed resin. is gradual due to improving technique of cultivation and breeding. This was accompanied by a request for twenty five reprints of any subsequent papers to be sent to the Bureau of Drugs and Indecent Few Omissions Publications!” Though excluded in this review (due to the criterion adapted that specific mention should be made by the scientist in his/her Derek Barton (1918-1998) had published co-authored papers, Nobel lecture), research conducted on plant materials by five in association with chemists who would subsequently receive other chemistry Nobel laureates (Theodor Svedberg, Alexander Nobel chemistry prize (such as Robert Woodward, Prelog and Todd, Derek Barton, John Cornforth and Vladimir Prelog) as well Elias Corey), on the constitution of some plant alkaloids (Barton as two other medicine/physiology Nobel laureates (Otto Warburg et al., 1950) and the bitter principle of citrus, limonin (Arigoni et and Severo Ochoa) who contributed to organic synthesis of plant- al., 1960). Early papers published by John Cornforth (1917-2013) derived substances and plant metabolism studies, at early, middle were on the constituents of Australian plants (Cornforth, 1938; or later stages of their careers should not be ignored. It may be Cornforth and Earl, 1938; Callow, 1975; Hanson, 2014). Similarly, of ephemeral interest to mention here that the very first paper of first independent research of Vladimir Prelog (1906-1998), starting Frederick Sanger as a 24 year old graduate student (Neuberger and around 1930, was on quinine, the main alkaloid from Cinchona

©2017 Reviews in Agricultural Science 89 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83 bark (Dunitz, 1998; Arigoni et al., 2000). Subsequently, Prelog also (Benson and Calvin, 1947, 1950; Calvin and Benson, 1948), had reported on his investigations on strychnine (Prelog and Szpilfogel, received two joint nominations with Calvin in 1952 and 1960. 1945) and strychnine related alkaloid sempervirins from Carolina But, only Calvin was singularly honored with the 1961 Nobel jasmin Gelsemium sempervirens (Goutarel et al., 1948). chemistry prize. Separately, Arnon had received 8 nominations cumulatively in the years 1961, 1962, 1965 and 1966. The 1931 Nobel prize for medicine or physiology was awarded to German biochemist of repute, Otto Warburg (1883-1970) “for Umetaro Suzuki (1874-1943) had received two nominations in his discovery of the nature and mode of action of the respiratory 1914 (medicine/physiology) and 1936 (chemistry) for his research enzyme.” Towards the conclusion of his Nobel lecture, Warburg on rice bran (anti-beri beri factor, or aberic acid, as designated by made a passing reference to the common origin of hemoglobin Suzuki), which later came to be identified as thiamine or vitamin and chlorophyll. In fact, Warburg and his junior colleagues had B1. As Suzuki published his original study in a Japanese journal researched on photosynthesis using green alga Chlorella and (Suzuki and Imamura, 1911), this attempt failed to gain due spinach Spinacea oleracea as models (Warburg and Luttgens, recognition among European vitamin researchers. Also, Yasuhiko 1944a, 1944b; Whittingham, 1952; Aronoff, 1957; Warburg, 1958). Asahina (1881-1975), a pioneer researcher on lichens (Perez-Llano, 1944; Kurokawa, 1976), had received two nominations in 1951 and The 1959 medicine/physiology Nobel prize was shared 1952 for the chemistry award. by Severo Ochoa (1905-1993) for discovery of mechanisms in biological synthesis of ribonucleic acid and deoxyribonucleic Mikhail Tsvet or variantly spelled as Michail Tswett (1872-1919) acid’. Photochemical reduction of pyridine nucleotides in spinach was a Russian botanist, who is credited for devising and introducing grana and isolated chloroplasts have been studied by Ochoa as the chromatography method for separation of plant pigments in the well (Vishniac and Ochoa, 1951, 1952). first decade of the 20th century (Tswett, 1911; Zechmeister, 1946; Asimov, 1982; Sakodynskii, 1972; Ettre and Sakodynskii, 1993a, Andrew Fire (b.1959) and Craig Mello (b.1960) received the 1993b). He received one nomination in 1918 for the chemistry prize 2006 Nobel Medicine or Physiology Prize for their discovery of (Ettre, 1996). Unfortunately, in the following year, he died at a RNA interference (RNAi) gene silencing by double stranded RNA relatively young age of 37. Nevertheless, Tswett’s contemporaries of nematode worm Caenorhabditis elegans (Fire et al., 1998). The Willstatter and Karrer exploited the chromatography method for their contribution of David Baulcombe, a British plant scientist and pigment analysis and received the Nobel chemistry awards in 1915 geneticist as a notable omission for this 2006 award, was reported and 1937 respectively. Ahead of Tswett, chemist Leon Marchlewski by Bots et al. (2006). His work (Hamilton and Baulcombe, 1999, (1969-1946) who studied organic pigments with emphasis on Baulcombe, 2004) was considered as a key to understanding the chlorophyll and published the first monograph on chrlorophylls in mechanism of RNAi that paved the way for Fire and Mello's findings. 1907 (Skarzynski, 1946), also did receive cumulatively 4 nominations Fire himself had acknowledged his debt to the work of plant scientists (2 nominations for 1913 chemistry prize and 2 nominations for 1913 on gene silencing (Weissmann, 2007). Thus, concerned views of plant and 1914 physiology and medicine prize) for his work on chlorophyll. science researchers (Kende, 1998; Gresshoff, 2002) that research on Ettre’s (1996) investigative study on the relative contributions plant science deserve better and more favorable evaluation in the of Tswett and that of his two antagonists for the Nobel prize, selection of science Nobel prizes can be appreciated. Machlewski and Willstatter is an interesting document that reveal the reasons why Willstatter received the 1915 Nobel prize for chemistry Nominated but Unlucky Scientists instead of either Machlewski or Tswett. We also scanned the Nobel Prize nomination database for the chemistry (1901-1966), and medicine or physiology (1901- Norman Wingate ‘Bill’ Pirie (1907-1997) was a prolific British 1953) prizes, and identified eight renowned scientists who did polymath scientist, who published in diverse fields, and became a exceptional research in plant sciences and were nominated for proponent of leaf proteins as food for starving population (Pirie, the Nobel Prizes in these two categories (Table 2); but were 1979, 1982, Pierpoint, 1999). In 1936, Pirie and Frederick Bawden unsuccessful in not receiving the prize. Andrew Benson (1917- (1908-1972), with two notable crystallographers, showed for the 2015) and Daniel Arnon (1910-1994) were well known for their first time that tobacco mosaic virus (TMV) could be crystallized, contribution to studies in photosynthesis (Arnon et al., 1954a, then considered as a remarkable work to study the structure of 1954b, Arnon, 1966; Benson, 2002; Govindjee, 2010). In fact, viral DNA and RNA (Bawden et al., 1936; Bawden and Pirie, Benson who had co-authored research papers with Melvin Calvin 1938a, 1938b). For this achievement, Bawden and Pirie received

90 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

Table 2: Nominees for the Nobel Prizes for Research on Plant Sciences Year* Scientist (country) Field Research Recognition 1913 Leon Marchlewski (Poland) Chemistry work on chlorophyll William Kuster (Germany)

1913 Leon Marchlewski (Poland) Chemistry work on chlorophyll William Kuster (Germany) Richard Willstatter (Germany)

1913 Leon Marchlewski (Poland) Medicine or Physiology work on chlorophyll and hemogobin William Kuster (Germany)

1914 Leon Marchlewski (Poland) Medicine or Physiology work on chlorophyll

1914 Umetaro Suzuki (Japan) Medicine or Physiology studies on anti-beriberi factor

1918 Mikhail Tswett (Russia) chemistry work on chlorophyll and other plant pigments

1936 Umetaro Suzuki (Japan) Chemistry studies on anti-beriberi factor

1939 Frederick Bawden (UK) Chemistry identification tobacco mosaic virus Norman W. Pirie (UK) Chemistry 1951 Yasuhiko Asahina (Japan) Chemistry pioneering studies in lichenology

1952 Yasuhiko Asahina (Japan) Chemistry pioneering studies in lichenology

1952 Melvin Calvin (USA) Medicine or Physiology studies in photosynthesis Andrew A. Benson (USA) Medicine or Physiology

1960 Melvin Calvin (USA) Chemistry studies in photosynthesis Andrew A. Benson (USA) Chemistry

1961 (2) Daniel I Arnon (USA) Chemistry studies in photosynthesis

1962 Daniel I Arnon (USA) Chemistry studies in photosynthesis

1965 Daniel I Arnon (USA) Chemistry studies in photosynthesis

1966(4) Daniel I Arnon (USA) Chemistry studies in photosynthesis Source: Nobel prize nomination database. (https://www.nobelprize.org/nomination/archive/list.php). Available information in this database is restricted from 1901 to 1966. *Number within parenthesis indicates the number of nominations received.

©2017 Reviews in Agricultural Science 91 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83 one nomination in 1939 for the chemistry prize. Similarly, the Nobel selection committee for medicine or Present Status physiology prize consists of 5 regular members and an executive If we analyze the trend of recognition for plant science research secretary. An additional 10 ad hoc committee members (who by the Nobel committee by collapsing the three major categories serve for a nine month period, but need not be members of the (chemistry, medicine/physiology and peace), with one decade as Nobel assembly) chosen for expertise and evaluation of nominees a unit, the emerging pattern is shown in Table 3. From 1901 to aid in the selection. Like that of the chemistry prize, invitations 2017, pioneering work on five major research themes, namely, (1) around 2,500 – 3,000 are sent to qualified nominators, according chlorophyll and photosynthesis, (2) elucidation of the structure to a rotating system (Lindsten and Ringertz, 2001). Thus, the of vitamins (carotene, thiamin, ascorbic acid and vitamin K), ‘fashion and whim’ of the majority of the selection committee (3) use of radioisotopes for metabolism studies, (4) plant natural members, reputation of the nominators of the scientists, merit and product chemistry and (5) plant genetics had received Nobel award reproducibility of the results symbolic of the scientist nominees, recognition 17 times. Given the reality of tough evaluation of the and last but not the least, ‘politics’ do play vital role in the screening process, the eventual selection of a Nobel award depends eventual selection for the Nobel award. on multiple factors. Table 4 indicates the prize awarding institutions Though advances in sciences had outgrown Nobel’s 1895 for selection of different Nobel prize categories. vision of his famous will (Larsson, 2008), when choosing one or two or three suitable laureates for each of the science prizes, The Nobel selection committee for chemistry prize consists still the Nobel award selection committees focus on two specific of five regular members. To widen the range of expertise, few conditions identified by Hevesy (1951): these are, “General merit decades ago, adjunct members (five in 1998) with equal voting alone in promoting science does not qualify for obtaining a Nobel rights as the regular members were added. Currently, a member prize. Several contributions by the same person but in different may serve a total of 9 years, in the committee. Invitations for fields, none of which is important enough by itself to qualify for nomination to the chemistry prize were sent to around 2,650 an award, are not considered.” qualified nominators in 1998. For each year, the number of valid nominations received by the committee range between 250 and Future Predictions 350 (Malmstrom and Anderson, 2001). For the chemistry prize, It may be pertinent to look at what past Nobel laureates in the selection committee’s decision is first passed to the respective plant science research had proposed as challenging issues awaiting section members of the Swedish Academy of Sciences, for a vote. resolution, in their Nobel award lectures. We provide a couple of The results of this voting is then forwarded to the full membership examples here. (~350) for final approval at the plenary session (Feldman, 2000). Calvin (1961) noted the following problem: “We are now in

Table 3: Nobel Prizes awarded for Research in Plant Sciences Decade Number of Nobel awards for plant science research (specific year with Nobel award recognition) 1901-10 0 1911-20 1 (1915) 1921-30 2 (1929, 1930) 1931-40 3 (1937*, 1937*, 1938) 1941-50 5 (1943○, 1945,1947, 1950) 1951-60 0 1961-70 2 (1961, 1970) 1971-80 1 (1978) 1981-90 2 (1983, 1988) 1991-2000 0 2001-10 0 2011-17△ 1 (2015) △Incomplete decade. *Unusually, chemistry and medicine/physiology awards recognized carotene and ascorbic acid research in plant material respectively.. ○Chemistry award recognized radioisotope research in plant material; medicine/physiology award recognized vitamin K research in plant materials..

92 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

Table 4: Prize Awarding Institutions for selection of different Nobel award categories

Prize Awarding Institution No. of Members Award category

Royal Swedish Academy of Sciences approximately 350 Chemistry and Physics

Nobel Assembly at Karolinska Institutet active full professors 50 Medicine or Physiology

Swedish Academy 18 Literature

Norwegian Nobel Committee 5* Peace *Appointed by the Norwegian Parliament (Storting) source: Lemmel (2001)

Fig.2 Barbara McClintock delivering her Nobel lecture on Dec 8, 1983 [photo courtesy, American Philosophical Society, Barbara McClintock Papers - Photographer unknown] the midst of trying to determine precisely what happens after the In her Nobel award lecture, McClintock (1983) had chlorophyll has absorbed the quantum and has become an excited emphasized the significance of genome research as follows: “In chlorophyll molecule, a problem that involves the physicist and the future attention undoubtedly will be centered on the genome... physical chemist, as well as the organic and biochemists. The We know about the components of genomes that could be made determination of the next stage in the energy-conversion process available for such restructuring. We know nothing, however, about is one of our immediate concerns. Either it is an electron transfer how the cell senses danger and instigates responses to it that often process, and thus comes close in its further stages to the electron are truly remarkable.”[Fig. 2] transfer processes which are being explored in mitochondria or it is some independent non-redox method of energy conversion. Studies to improve plant production in the field which is This remains for the future to decide.” unsuitable for agricultural production has been carried out in the last two decades (Kasuga et al., 1999; Nelson et al., 2007).

©2017 Reviews in Agricultural Science 93 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83

In-depth knowledge on the ecosystems within and surrounding Bawden, F.C., Pirie, N.W., Bernal, J. D. and Fankuchen, I. (1936). plants, called phytobiomes is needed for vital understanding of Liquid crystalline substances from virus-infected plants. varied factors. Thus, interdisciplinary teams including expertise Nature, 138, 1051-1052. in botany may be vital for trend-setting new discoveries (Leach Benson, A.A. (2002). Paving the path. Ann Rev Plant Biol., 53, 1-25. et al., 2017). Pioneering studies along the line of plants that can Benson, A.A. and Calvin, M. (1947). The dark reductions of grow in a dessert or sea, plants which can be an enriched source of photosynthesis. Science, 105, 648-649. fuel and hydrocarbon-like materials (Nielsen et al., 1977; Calvin, Benson, A.A. and Calvin, M. (1950). Carbon dioxide fixation by 1980, 1983) may have potential to be considered for a Nobel Prize green plants. Ann Rev Plant Physiol., 1, 25-42. for plant science research. Bingley, S.B., MacCorquodale, D.W., Thayer, S.A. and Doisy, E.A.

(1939a). The isolation of vitamin K1. J Biol Chem., 130, 219-234. Acknowledgement Binkley, S.B., Cheney, L.C., Holcomb, W.F., McKee, R.W., We dedicate this contribution to the memory of Dr. Eugene Thayer, S.A., MacCorquodale, D.W. and Doisy, E.A. (1939b)

Garfield (1925 – 2017), a pioneer in scientometrics and studies The constitution and synthesis of vitamin K1. J Am Chem Soc., on Nobel prizes, for inspiration offered. Dr. Garfield died on 61, 2558-2559. February 26, 2017. Bingley, S.B., McKee, R.W., Thayer, S.A. and Doisy, E.A. (1940).

The constitution of vitamin K2. J Biol Chem., 133, 721-729. References Blank, F. (1947). The anthocyanin pigments of plants. Bot Rev., Adams, R. (1943). Richard Willstatter. J Am Chem Soc., 65, 127-128. 13(5), 241-317. Anon (1961). Professor George C. de Hevesy. J Nucl Med., 2, 167. Borlaug, N. E. (1954). Mexican wheat production and its Anon (1983). Nobel prize to Barbara McClintock. Nature, 305, 575. role in the epidemiology of stem rust in North America. Arigoni, D., Barton, D.H.R., Corey, E.J., Jeger, O. et al. (1960). Phytopathology, 44, 398-404. The constitution of limonin. Experientia, 16(2), 41-49. Borlaug, N.E. (1965). Wheat, rust and people. Phytopathology, 55, Arigoni, D., Dunitz, J.D. and Eschenmoser, A. (2000). Vladimir 1088-1098. Prelog 23 July 1906 – 7 January 1998. Biogr Mem Fell R Soc., Borlaug, N. (1970). The Green revolution, peace and humanity. 46, 443-464. Nobel Lecture, Dec. 11. Arnon, D.I., Rosenberg, L.L. and Whatley, F.R. (1954a). A new (https://www.nobelprize.org/nobel_prizes/peace/laureates/1970/ glyceraldehyde phosphate dehydrogenase from photosynthetic borlaug-lecture.html) tissues. Nature, 173, 1132-1134. Borlaug, N.E. (1983). Contributions of conventional plant Arnon, D.I., Allen, M.B. and Whatley, F.R. (1954b). breeding to food production. Science, 219, 689-693. Photosynthesis by isolated chloroplasts. Nature, 174, 394-396. Borlaug, N.E. (2000). Ending world hunger. The promise of Arnon, D.I. (1966). The photosynthetic energy conversion process biotechnology and the threat of anti-science zealotry. Plant in isolated chloroplasts. Experientia, 22(5), 273-287. Physiol., 124(2), 487-490. Aronoff, S. (1957). Photosynthesis. Bot Rev., 23(2), 65-107. Borlaug, N. E. (2002). Feeding a world of 10 billion people: the Asimov, I. (1982). Asimov’s Biographical Encyclopedia of Science miracle ahead. In Vitro Cellular & Developmental Biology- and Technology, 2nd revised ed., Doubleday & Company, New Plant, 38(2), 221-228. York. Borlaug, N. Feeding a hungry world. Science, 318, 359. Baglow, G. and Bottle, R.T. (1979). Rate of publication of British Bots, M., Maughan, S. and Nieuwland, J. (2006). RNAi Nobel chemists. Chem Brit., 15(3), 138-141. ignores vital groundwork on plants. Nature, 443, 906. Barton, D.H.R., Jeger, O., Prelog, V. and Woodward, R.B. Brown, D.M. and Kornberg, H. (2000). Alexander Robertus Todd, (1954). The constitutions of cevine and some related alkaloids. 2 Oct 1907 – 10 Jan 1997. Biogr Mems Fell R Soc., 46, 515-532. Experientia, 10(3), 81-90. Brown, L.R. (1970). Nobel peace prize: developer of high-yield Baulcombe R. (2004). RNA silencing in plants. Nature, 431, 356-363. wheat received award. Science, 170, 518-519. Bauernfeind, J.C. (1972). Carotenoid Vitamin A precursors and Burr, B. and Burr, F.A. (1983). Barbara McClintock: Nobel prize analogs in foods and feeds. J Agric Food Chem., 20(3), 456-473. in physiology/medicine. Trends Biochem Sci., 8(12), 429-431. Bawden, F.C. and Pirie, N.W. (1938a). A plant virus preparation in Burris, R.H. (1950). Isotopes as traces in plants. Bot Rev., 16(3), a fully crystalline state. Nature, 141, 513-514. 150-180. Bawden, F.C. and Pirie, N.W. (1938b). Aggregation of purified Calvin, M. (1961). The path of carbon in photosynthesis. Nobel tobacco mosaic virus. Nature, 142, 842-843. Lecture, December 11.

94 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

(https://www.nobelprize.org/nobel_prizes/chemistry/ (https://www.nobelprize.org/nobel_prizes/chemistry/ laureates/1961/calvin-lecture.html) laureates/1988/deisenhofer-michel-lecture.pdf) Calvin, M. (1980). Hydrocarbons from plants: analytical methods Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, and observations. Naturwissenschaften, 67, 525-538. H. (1984). X-ray structure analysis of a membrane protein Calvin, M. (1983). New sources for fuel and materials. Science, complex. Electron density map at 3Ao resolution and a model 198, 24-26. of the chromophores of the photosynthetic reaction center from Calvin, M. (1989). Forty years of photosynthesis and related Rhodopsuedomonas viridis. J Mol Biol., 180, 385-398. activities. Photosyn Res., 21, 3-16. Deisenhofer, J., Epp, O., Miki, K., Huber, R. and Michel, H. Calvin, M. and Benson, A.A. (1948). The path of carbon in (1985a). Structure of the protein subunits in the photosynthetic photosynthesis. Science, 107, 476-480. reaction centre of Rhodopseudomonas viridis at 3Ao resolution. Callow, R.K. (1975). Cornforth’s prize. Nature, 258, 5. Nature, 318, 618-624. Chakravarti, R.N., Pausacker, K.H. and Robinson, R. (1947). Deisenhofer, J., Michel, H. and Huber, R. (1985b). The structural Strychnine and brucine: oxodihydroneostrychnine and basis of photosynthetic light reactions in bacteria. Trends oxodihydromethoxymethyldi-hydroneostrychnine. J Chem Soc., Biochem Sci., 10(6), 243-248. Pt. 2, 1554-1556. Doisy, E.A. (1976). An autobiography. Ann Rev Biochem., 45, 1-9. Chen, W.J. (2016). Honoring antiparastics: The 2015 Nobel prize Doisy, E.A., Binkley, S.B., Thayer, S.A. and McKee, R.W. (1940). in physiology or medicine. Biomed J., 39(2), 93-97. Vitamin K. Science, 91, 58-62. Comfort, N.C. (1995). Two genes, No enzyme: a second look Dunitz, J.D. (1998). Vladimir Prelog (1906-98) Pioneer of at Barbara McClintock and the 1951 Cold Spring Harbor stereochemistry. Nature, 391, 542. Symposium. Genetics, 140, 1161-1166. Edsall, J.T. (1986). Albert Szent-Gyorgyi (1893-1986). Nature, 324, Comfort, N. C. (2001). From controlling elements to transposons: 409. Barbara McClintock and the Nobel Prize. Trends Genetics, Eijkman, C. (1929). Antineuritic vitamin and beriberi. Nobel 17(8), 475-477. Lecture. Cornforth, J.W. (1938). The anthocyanin of Vitis hypoglauca. J (http://www.nobelprize.org/nobel_prizes/medicine/ Roy Soc New South Wales, 72, 325-328. laureates/1929/eijkman-lecture.html) Cornforth, J.W. and Earl, J.C. (1938). A chemical examination Ettre. L.S. (1996). M.S. Tswett and the 1918 Nobel prize in of the fruit of Pittosporum undulatum. J. Roy Soc New South chemistry. Chromatographia, 42(5-6, 343-351. Wales, 72, 249-254. Ettre, L.S. and Sakodynskii, K.I. (1993a). M.S. Tswett and the Dam, H. (1934). Haemorrhages in chicks reared on artificial diets: discovery of chromatography. I. Early work (1899-1903). a new deficiency disease. Nature, 133, 909-910. Chromatographia, 35(3/4), 223-231. Dam, H. (1935). The antihaemorrhagic vitamin of the chick. Ettre, L.S. and Sakodynskii, K.I. (1993b). M.S. Tswett and the Occurrence and chemical nature. Nature, 135, 652-653. discovery of chromatography. I. Early work (1899-1903). Dam, H. (1940). Fat-soluble vitamins. Ann Rev Biochem., 9, 353-382. Chromatographia, 35(5/6), 329-338. Dam, H. (1943). The discovery of vitamin K, its biological Fedoroff, N.V. (1994). Barbara McClintock (June 16, 1902 – function and therapeutical application. Nobel lecture, Dec. 12. September 2, 1992). Genetics, 136, 1-10. (http://www.nobelprize.org/nobel_prizes/medicine/ Feldman, B. (2000). The Nobel Prize, Arcade Publishing, New laureates/1943/dam-lecture.pdf) York. Dam, H. and Schonheyder, F. (1936). The occurrence and chemical Fire A., Xu S.Q., Montgomery M.K., Kostas S.A., Driver S.E. and nature of vitamin K. Biochem. J., 30(5), 897-901. Mello C.C (1998) Potent and specific genetic interference by Dam, H. and Lewis, L. (1937). The chemical concentration of double-stranded RNA in Caenorhabditis elegans. Nature, 391, vitamin K. Biochem. J., 31(1), 17-21. 806-811. Dam, H. and Glavind, J. (1938). Vitamin K in the plant. Biochem. Fischer, H. (1930). On Haemin and the Relationships between J., 32(3), 485-487. Haemin and Chlorophyll. Nobel Lecture Dec. 11 Dam, H., Glavind, J. and Gabrielsen, E.K. (1947). On the occurrence (https://www.nobelprize.org/nobel_prizes/chemistry/ of vitamin K in plants. Acta Physiol Scand., 13(1-2), 9-19. laureates/1930/fischer-lecture.pdf) Deisenhofer, J and Michel, H. (1988). The photosynthetic reaction Garfield, E. (1980). Are the 1979 prize winners of Nobel Class? centre from the purple bacterium Rhodopseudomonas viridis. Current Contents (38). September 22. (Reprinted in: Essays of Nobel lecture, Dec. 8. an Information Scientist, 1979-1980, ISI Press, Philadelphia,

©2017 Reviews in Agricultural Science 95 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83

1981, vol.4, pp. 609-617. acid-base transition of spinach chloroplasts. Proc Natl Acad Sci Garfield, E. (1987). Citation Classics in Plant Sciences and their USA, 55, 170-177. impact on current research. Current Contents (40). October 5. Karlson, P. (1978). Carotene as provitamin A. Trends Biochem (Reprinted in: Essays of an Information Scientist: Peer Review, Sci., 3(4), 235-236.

Refereeing, Fraud and Other Essays, ISI Press, Philadelphia, Karrer, P. (1937). Carotenoids, Flavins and Vitamin A and B2. 1989, vol. 10, pp. 282-292. Nobel Lecture, December 11. Garfield, E. and Welljams-Dorof, A. (1992). Of Nobel class: a (https://www.nobelprize.org/nobel_prizes/chemistry/ citation perspective on high impact research authors. Theoret laureates/1937/karrer-lecture.pdf) Med., 13(2), 117-135. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. and Gould, S.J. (1985). Jumping genes. ChemTech, 15, 712-715. Shinozaki, K. (1999). Improving plant drought, salt, and Govindjee. (2010). Celebrating Andrew Alm Benson’s 93rd freezing tolerance by gene transfer of a single stress-inducible birthday. Photosynthesis Res., 105(3), 201-208. transcription factor. Nature Biotechnology, 17(3), 287-291. Gralen, N. and Svedberg, T. (1943). Molecular weight of native Kende, H. (1998). Plant biology and the Nobel Prize. Science, 282, cellulose. Nature, 152, 625. 627. Gresshoff, P. M. (2002). All We Are Saying Is Give Plants a Kresge, N., Simoni, R.D. and Hill, R.L. (2006). Unraveling the Chance!. J Biomed Biotechnol., 2(3), 115-116. enzymology of oxidative phosphorylation: the work of Efraim Guo, Z. (2016). Artemisnin anti-malarial drugs in China. Acta Racker. J Biol Chem., 281(4), e4-e6. Pharmaceutica Sinica B, 6(2), 115-124. Krejci, L. and Svedberg, T. (1935). The salt extactable proteins of Hamilton, A. J. and Baulcombe, D. C. (1999). A species of small wheat flour, Ultracentrifugal study. J Amer Chem Soc., 57(7), antisense RNA in posttranscriptional gene silencing in plants. 1365-1369. Science, 286, 950-952. Kurokawa, S. (1976). Obituary – Yasuhiko Asahina 1881 – 1975. Hanson, J. (2014). John Cornforth (1917-2013). Nature, 506, 35. Lichenologist, 8, 93-94. Hevesy, G. (1923). The absorption and translocation of lead by Larsson, U. (2008). Alfred Nobel Networks of Innovation, Nobel plants. Biochem J., 17, 439-445. Museum and Science History Publications/USA, Sagamore Hevesy, G. de (1944) Some applications of isotopic indicators, Beach, MA, pp. 204-209. Nobel lecture, Dec. 12. Leach, J.E., Triplett, L.R., Argueso, C.T. and Trivedi, P. (2017). (https://www.nobelprize.org/nobel_prizes/chemistry/ Communication in the phytobiome. Cell, 169, 587-596. laureates/1943/hevesy-lecture.pdf) Lehninger, A.L. (1967). Energy coupling in electron transport. Hevesy, G. (1951). Fiftieth anniversary of the Nobel Foundation. Introduction. Fed Proc., 26(5), 1333-1334. Nature, 167, 57-59. Lemmel, B. (2001. The Nobel Foundation: A century of growth Hevesy, G., Linderstrom-Lang, K. and Olsen, C. (1936). Atomic and change. In: The Nobel Prize – the first 100 years, dynamics of plant growth. Nature, 137, 66-67. Levinovitz, A.W and Ringertz, N. (eds.), Imperial College Hinkle, P.C. and Garlid, K.D. (1992). Peter Mitchell 1920-1992. Press, London, pp. 13-24. Trends Biochem Sci., 17(8), 304-305. Levi, B.G. (1989). Nobel chemists shed light on key structure in Horton, R.A. (1976). Carl Peter Henrik Dam. Nature, 261, 621. photosynthesis. Phys Today, 42(2), 17-18. Huber, R (1988). A structural basis of light energy and electron Levinovitz, A.W. and Ringertz, N. ed. (2001). The Nobel Prize – transfer in biology. Nobel lecture Dec. 8. The First 100 Years, Imperial College Press, London. (https://www.nobelprize.org/nobel_prizes/chemistry/ Lewin, R. (1988). Membrane protein holds photosynthetic secrets. laureates/1988/huber-lecture.pdf) Science, 242, 672-673. Huszagh, V.A. and Infante, J.P. (1989). The hypothetical way of Lindsten, J. and Ringertz, N. (2001). The Nobel Prize in progress. Nature, 338, 109. physiology or medicine. In: Nobel Prize – the First 100 Years, Isler, O. (1978). Paul Karrer, 21 April 1889 – 18 June 1971. Biogr Levinovitz, A.W. and Ringertz, N. (eds.), Imperial College Mems Fell R Soc., 24, 245-321. Press, London, pp. 111-127. Jacob, A. and Todd, A.R. (1940). Cannabidiol and Cannabol, MacCorquodale, D.W., McKee, R.W., Binkley, S.B., Chaney, L.C., Constituents of Cannabis indica resin. Nature, 145, 350-351. Holcomb, W.F., Thayer, S.A. and Doisy, E. (1939) Identification

Jagendorf, A.T. (1967). Acid-based transitions and phosphorylation of vitamin K1 (alfalfa). J Biol Chem., 130, 433. by chloroplasts. Fed. Proc., 26(5), 1361-1369. Malmstrom, B.G and Anderson, B. (2001). The Nobel Prize in Jagendorf, A.T. and Uribe, E. (1966). ATP formation caused by chemistry. In: Nobel Prize – the First 100 Years, ed. Levinovitz,

96 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

A.W. and Ringertz, N., Imperial College Press, London, pp. 73- 4(5), 118-120. 101.. Openshaw, H.T. and Robinson, R. (1946). Constitution of McClintock, B. (1983/1984). The significance of responses of the strychnine and the biogenetic relationship of strychnine and genome to challenge. Nobel lecture, Dec. 8. Science, 226, 792-801. quinine. Nature, 157, 438. (http://www.nobelprize.org/nobel_prizes/medicine/ Owens, B. 2015 Nobel prize goes to antiparasitic drug discoverers. laureates/1983/mcclintock-lecture.pdf) Lancet, 386, 1433. Meritt, C. and Tan, S.Y. (2011). Christiaan Eijkman (1858-1930): Pausacker, K.H. and Robinson, R. (1947). Strychnine and The vicar of vitamins. Singapore Med J., 52(9), 652-653. brucine: degradation of the strychnineacetic acid prepared from Michel, H. (1982). Three-dimensional crystals of a membrane pseudostrychnine. J Chem Soc., Pt 2, 1557-1560. protein complex: the photosynthetic reaction centre from Perez-Llano, G.A. (1944). Lichens – Their biological and Rhodopseudomonas viridis. J Mol Biol., 158(3), 567-572. economic significance. Bot. Rev., 10(1), 1-65. Miettinen, J. K. (1975). Artturi Ilmari Virtanen. Plant Soil, 43(1), Pierpoint, W.S. (1999). Norman Wingate Pirie 1 July 1907 – 29 229-234. Mar 1997. Biogr Mems Fell R Soc., 45, 397-415. Mills, R. E., Bennett, E. A., Iskow, R. C. and Devine, S. E. (2007). Pirie, N.W. (1979). Potential for leaf protein as human food. J Am Which transposable elements are active in the human genome? Oil Chem Soc., 56, 472. Trends Genetics, 23(4), 183-191. Pirie, N.W. (1982). Leaf protein as a food source. Experientia, 38, Mitchell, P. (1961). Coupling of phosphorylation to electron and 28-31. hydrogen transfer by a chemi-osmotic type of mechanism. Racker, E. (1967). Resolution and reconstitution of the inner Nature, 191, 144-148. mitochondrial membrane. Fed Proc., 26(5), 1335-1340. Mitchell, P. (1966). Chemi-osmotic coupling in oxidative and Reichstein, T. (1950). Chemistry of the adrenal cortex hormones. photosynthetic phosphorylation. Biol Rev., 41(3), 445-501. Nobel lecture, Dec. 11. Mitchell, P. (1967). Proton-translocation phosphorylation in (http://www.nobelprize.org/nobel_prizes/medicine/ mitochondria, chloroplasts and bacteria: natural fuel cells and laureates/1950/reichstein-lecture.pdf) solar cells. Fed Proc., 26(5), 1370-1379. Robinson, R. (1932). Richard Willstatter’s investigations on the Mitchell, P. (1970). Aspects of the chemiosmotic hypothesis. anthocyanins. Naturwissenschaften, 20, 612-618. Biochem J., 116(4), 5P-6P. Robinson, R. (1936). Formation of anthocyanins in plants. Nature, Mitchell, P. (1977). Vectorial chemiosmotic processes. Ann Rev 137, 172-173. Biochem., 46, 996-1005. Robinson, R. (1947). Constitution of strychnine and its relation to Mitchell, P. (1978). David Keilin’s respiratory chain concept and cinchonine. Nature, 159, 263. its chemiosmotic consequences. Nobel Lecture, Dec. 8. Robinson, R. (1947). An essay in correlation arising from alkaloid (https://www.nobelprize.org/nobel_prizes/chemistry/ chemistry. Nature, 160, 815-817. laureates/1978/mitchell-lecture.html) “Sir Robert Robinson – Nominations”. Nobelprize.org. Nobel Molyneux, D.H. and Ward, S.A. (2015). Reflections on the Nobel Media AB-2015. Web. 15 Sep. 2017. http://www.nobelprize.org/ prize for Medicine 2015 – The public health legacy and impact of nobel_prizes/chemistry/laureates/1947/robinson-nomination. Avermectin and Artemisinin. Trends Parasitol., 31(12), 605-607. html (accessed Sept 15, 2017). Morton, R.A. (1976). Carl Peter Henrik Dam. Nature, 261, 621. Robinson, R. (1947). Some polycyclic natural products. Nobel Moses, V. Melvin Calvin (1911-1997). Nature, 385, 586. Lecture, Dec. 12. Nelson, D. E., Repetti, P. P., Adams, T. R., Creelman, R. A., Wu, (https://www.nobelprize.org/nobel_prizes/chemistry/ J., Warner, D. C. and Hinchey, B. S. (2007). Plant nuclear laureates/1947/robinson-lecture.html) factor Y (NF-Y) B subunits confer drought tolerance and lead Rosenfeld, L. (1997). Vitamine̶vitamin. The early years of to improved corn yields on water-limited acres. Proc Natl Acad discovery. Clin. Chem., 43(4), 680-685. Sci USA, 104(42), 16450-16455. Rothschild, M (1999) Tadeus Reichstein. 20 July 1897 – 1 August Neuberger, A. and Sanger, F. (1942). The nitrogen of the potato. 1996. Biogr Mems Fell R Soc., 45, 449-467. Biochem. J., 36(7-9), 662-671. Sakodynskii, K. (1972). The life and scientific works of Michael Nielsen, P.E., Nishimura, H., Otvos, J.W. and Calvin, M. Plant Tswett. J Chromatogr., 73(2), 303-360. crops as a source of fuel and hydrocarbon-like materials. Saltzman, M.D. (1986). Sir Robert Robinson – a centennial tribute. Science, 198, 942-944. Chem Brit, 22(6), 543-548. Olson, R.E. (1979). Discovery of vitamin K. Trends Biochem Sci., Schultz, W. (1997). Melvin Calvin, pioneer biochemist, dead at 85.

©2017 Reviews in Agricultural Science 97 n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

B Please cite this article as ★

★ L

i

e

f Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 c

e n S e i

c http://dx.doi.org/10.7831/ras.5.83

Chem Eng News, 75(3), 11. Todd, A. and Cornforth, J.W. (1976). Robert Robinson, 13 Seaborg, G.T. and Benson, A.A. (1998). Melvin Calvin 1911-1996. September 1886 – 8 February 1975. Biogr Mems Fell R Soc., Biogr Mem Nat Acad Sci., 75, 96-115. 22, 414-527. Shampoo, M.A. and Kyle, R.A. (2000). Richard Kuhn – Nobel prize Trauner, D. (2015). Richard Willstatter and the 1915 Nobel Prize for work on carotenoids and vitamins. Mayo Clin Proc., 75, 990. in chemistry. Angew Chem Int Ed., 54, 11910-11916. Shapiro, J. (1992). Barbara McClintock, 1902-1992. BioEssays, Tswett, M. (1911). Uber den makro- und mikrochemischen 14(11), 791-792. Nachweis des Carotins. Ber Deut Bot Ges., 29, 630-636. Skarzynski, B. (1946). Prof. Leon Marchlewski. Nature, 157, 650-651. Tu, Y. (2011). The discovery of artemisinin (qinghaosu) and gifts Slater, E.C. (1953). Mechanism of phosphorylation in the from Chinese medicine. Nature Med., 17(10), 1217-1220. respiratory chain. Nature, 172, 975-978. Tu, Y. (2015). Artemisinin – a gift from traditional Chinese Slater, E.C. (1994). Peter Dennis Mitchell. 29 September 1920 – medicine to the world. Nobel lecture, Dec. 7. 10 April 1992. Biogr Mem Fell R Soc., 40, 282-305. (http://www.nobelprize.org/nobel_prizes/medicine/ Sohlman, R. (1983). The Legacy of Alfred Nobel – The Story laureates/2015/tu-lecture.pdf) behind the Nobel Prizes, The Bodley Head, London. Verhoef, J., Snippe, H. and Nottet, H.S.L.M., (1999). Christian Sohlman, R. and Schuck, H. (1929). Nobel – Dynamite and Peace, Eijkman. Antonie van Leewenhock, 75(3), 165-169. Cosmopolitan Book, Corporation, New York pp. 239-308. Virtanen, A. (1936). Nature of the excretion of nitrogen Sri Kantha. S (1998). Alfred Nobel’s unusual creativity: an compounds from legume nodules. Nature, 138, 880-881. analysis. Med Hypotheses, 53, 338-344. Virtanen, A. (1945). The Biological Fixation of Nitrogen and the Suzuki, U. and Shimamura, T. (1911), On the effective substance Preservation of Fodder in Agriculture and Their Importance to present in rice bran. Tokyo Kagaku Kaishi, 32, 4-17. (in Japanese) Human Nutrition. Nobel Lecture, Dec. 12. Svedberg, T. (1927). The Ultracentrifuge. Nobel lecture, May 19. (https://www.nobelprize.org/nobel_prizes/chemistry/ https://www.nobelprize.org/nobel_prizes/chemistry/ laureates/1945/virtanen-lecture.html) laureates/1926/svedberg-lecture.pdf Virtanen, A.I. and Laine, T. (1936). Aminoacid content of plants at Svedberg, T. (1947). The cellulose molecule: Physical-chemical different stages of growth. Nature, 137, 237. studies. J Physical Colloid Chem., 51(1), 1-18. Virtanen, A.I. and Laine, T. (1938a). Biological synthesis of amino Svedberg, T. and Gralen, N. (1938). Carbohydrates of well-defined acids from atmospheric nitrogen. Nature, 141, 748-749. molecular weight in plant juices. Nature, 142, 261-262. Virtanen, A.I. and Laine, T. (1938b). Biological fixation of Svedberg, T. and Katsurai, T. (1929). The molecular weights of nitrogen. Nature, 142, 165. phycocyan and of phycoeruthrin from Porphyra tenera and of Virtanen, A.I. and Laine, T. (1946). Red, Brown and Green phycocyan from Aphanizomenon flos aquae. J Amer Chem Soc., pigments in leguminous root nodules. Nature, 157, 25-26. 51(12), 3573-3583. Virtanen, A.I. and Arhimo, A.A. (1939). Oxaloacetic acid in the Svirbely, J. L. and Szent-Györgyi, A. (1932). The chemical nature leguminous plants. Nature, 144, 36. of vitamin C. Biochem. J., 26(3), 865-870. Virtanen, A.I., Arhimo, A.A. and Suomalainen, H. (1939). Svirbely, J. L. and Szent-Györgyi, A. (1933). The chemical nature Estimation and occurrence of keto-acids in green plants. of vitamin C. Biochem. J., 27(1), 279-285. Nature, 144, 597. Szent-Gyorgyi, A. (1928). CLXXIII. Observations on the function Virtanen, A.I., Rintala and Laine, T. (1938). Decarboxylation of of peroxidase systems and the chemistry of the adrenal cortex. aspartic and glutamic acids. Nature, 142, 674. Description of a new carbohydrate derivative. Biochem J., Vishniac, W. and Ochoa, S. (1951). Photochemical reduction of 26(7), 1387-1409. pyridine nucleotides by spinach grana and coupled carbon Szent-Gyorgyi, A. (1937). Oxidation, energy transfer and vitamins. dioxide fixation. Nature, 167, 768-769. Nobel Lecture, Dec.11. Vishniac, W. ad Ochoa, S. (1952). Phosphorylation coupled to a (http://www.nobelprize.org/nobel_prizes/medicine/ photochemical reduction by pyridine nucleotides by isolated laureates/1937/szent-gyorgyi-lecture.pdf) chloroplasts. J Biol Chem., 198, 501-506. Szent-Gyorgyi, A. (1963). Lost in the Twentieth Century. Ann Rev Warburg, O. (1931). The oxygen-transferring ferment of Biochem., 32, 1-14. respiration. Nobel lecture, Dec.10. Todd, A. R. (1939). The marijuana problem. Nature, 144, 611. https://www.nobelprize.org/nobel_prizes/medicine/ Todd, A.R. (1940). Chemistry of hemp drugs. Nature, 146, 829. laureates/1931/warburg-lecture.pdf Todd, A.R. (1946). Hashish. Experientia, 2, 55-60. Warburg, O. (1958). Photosynthesis. Science, 128, 68-73.

98 ©2017 Reviews in Agricultural Science n ★ En tio v c ir u o d n

o m

r e

p

n

o

i t

Please cite this article as B ★

★ L

i

e

Hayami and Sri Kantha, Reviews in Agricultural Science, 5:83-99, 2017 f c

e n S e i

http://dx.doi.org/10.7831/ras.5.83 c

Warburg, O. and Luttgens, W. (1944a). Experiment zur assimilation der Kohlensaure. Naturwissenschaften, 32, 161. (in German) Warburg, O. and Luttgens, W. (1944b). Weitere Experimente zur Kohlensaureassimilation. Naturwissenschaften, 32, 301. (in German) Weissmann, G. (2007). Americans sweep Nobel Prizes: Thinking Inside and Outside the box. FASEB J., 21(1), 1-4. Westphal, O. (1968). Richard Kuhn zum gedachtnis. Angew Chem., 80, 501-519. (in German). Wettstein, A. (1972). Paul Karrer 1889-1971. Helv Chim Acta, 55, 313-328. White, N.J., Hien, T.T. and Nosten, F.H. (2015). A brief history of Qinghaosu. Trends Parasitol., 31(12), 607-610. Whittingham, C.P. (1952). The chemical mechanism of photosynthesis. Bot Rev., 18(4), 245-290. Willstätter, R. (1920). On Plant Pigments. Nobel Lecture, June, 3. (https://www.nobelprize.org/nobel_prizes/chemistry/ laureates/1915/willstatter-lecture.pdf) Work, T.S., Bergel, F and Todd, A.R. (1939). The active principles of Cannabis indica resin. Part 1. Biochem. J., 33, 123-127. Xie, D.Y. (2016). Artemisia annua, artemisinin and the Nobel Prize: beauty of natural products and educational significance. Science Bull., 61(1), 42-44. Zechmeister, L. (1946). Mikhail Tswett – the inventor of chromatography. Isis, 36(2), 108-109. Zhai, X., Wang, Q and Li, M. (2016). Tu Youyou’s Nobel prize and the academic evaluation system in China. Lancet, 387, 1722.

©2017 Reviews in Agricultural Science 99