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Andrew A. Benson, 1917 – 2015 Andrew A. Benson, 1917–2015 Hartmut K. Lichtenthaler, Bob B. Buchanan, Roland Douce & Govindjee Photosynthesis Research Official Journal of the International Society of Photosynthesis Research ISSN 0166-8595 Volume 124 Number 2 Photosynth Res (2015) 124:131-135 DOI 10.1007/s11120-015-0119-8 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Photosynth Res (2015) 124:131–135 DOI 10.1007/s11120-015-0119-8 TRIBUTE Andrew A. Benson, 1917–2015 1 2 3 4 Hartmut K. Lichtenthaler • Bob B. Buchanan • Roland Douce • Govindjee Published online: 1 April 2015 Ó Springer Science+Business Media Dordrecht 2015 Abstract On January 16, 2015, Professor Andrew Alm Benson (called Andy by his friends) died on January 16, Benson, one of the leading plant biochemists of the 2015, in La Jolla, California; he was born in Modesto, twentieth century, died in La Jolla, California, at the age of California, on September 24, 1917; his father was a physi- 97; he was born on September 24, 1917. Benson was cian, and his mother was a schoolteacher. He graduated from known especially for his pioneering studies on photosyn- Modesto High School in 1935 as Valedictorian of his class thesis (CO2 assimilation, carbon reduction cycle) and plant and went on to the University of California, Berkeley, where lipids (phospholipid phosphatidyl glycerol; and the sul- he studied chemistry, obtaining a B.S. in 1939. It was at folipid, sulfoquinovosyl diglyceride). A photograph of Berkeley that he became infatuated with chemistry and de- Benson is shown in Fig. 1. cided to do graduate work at the California Institute of Technology (Cal Tech) under Carl Niemann, one of the Keywords The path of carbon in photosynthesis Á nation’s leading carbohydrate chemists. Calvin–Benson cycle Á RuBP Á Rubisco Á After receiving his doctorate in 1942, Benson returned Phosphoglycerate Á PGA Á Sulfolipid to Berkeley as an instructor in the Department of Chem- istry. There, he was exposed to photosynthesis and ra- Abbreviations dioisotope research by Samuel G. Ruben (1913–1943) and PGA Phosphoglyceric acid Martin Kamen (1913–2002)—two pioneers who two years RuBP Ribulose bis-phosphate earlier (1940) had discovered 14Carbon. Benson started his Rubisco Ribulose bis-phosphate carboxylase oxygenase photosynthesis work with the short-lived 11Carbon isotope 14 but, when it became available in 1943, turned to CO2 with a half-life of more than 5000 years (Benson 2011). His research came to a halt in 1942 with the onset of World War II. During that period Benson, a conscientious ob- jector, served with the US Forest Service, where he was & Hartmut K. Lichtenthaler [email protected] involved in fighting fires and aerial photogrammetry. He was later transferred to Stanford University and Cal Tech, 1 Botanical Institute 2 (Molecular Biology and Biochemistry of where he carried out antimalarial drug research. Plants), Karlsruhe Institute of Technology (KIT), University After resuming his career in 1946, Benson was appointed a Division, Kaiserstr. 12, 76131 Karlsruhe, Germany 2 Research Associate in the Radiation Laboratory at Berke- Department of Plant & Microbial Biology, University of ley in a photosynthesis group that Melvin Calvin (Nobel California, Berkeley, CA 94720, USA 3 Laureate in Chemistry, 1961) had just begun assembling. By Universite´ de Grenoble and CEA, Rue des Martyrs, feeding 14C-labeled CO to suspensions of the green alga 38026 Grenoble Cedex 9, France 2 Scenedesmus, Benson identified 3-phosphoglyceric acid 4 Department of Plant Biology, Department of Biochemistry, (PGA) as the first stable product of photosynthesis in joint and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, 265 Morrill Hall, 505 South work carried out with Calvin. For these studies, Benson de- Goodwin Avenue, Urbana, IL 61801, USA signed the ‘‘lollipop,’’ a flattened glass vessel that could be 123 Author's personal copy 132 Photosynth Res (2015) 124:131–135 Fig. 2 Andrew Benson in his office in La Jolla in 2001. He is holding one of the early radioautograms (from the 1950s) developed with a two-dimensional paper chromatogram. The film shows 14C-labeled 14 intermediates formed by Scenedesmus cells fed CO2.(Source Govindjee 2010) 3-phosphoglycerate had been unsuccessful, thus attesting to the significance of Benson’s discovery. Other intermediates of the carbon cycle, including sedoheptulose 7-phosphate (7-carbon sugar) and pentose monophosphates (5-carbon sugars), were identified by Benson in collaboration with other members of the Calvin group. James A. Bassham (1922–2012), a graduate student in chemistry, participated in much of this work. The compounds identified in lollipop Fig. 1 Photograph of Andrew A. Benson. Source: Annual Review of experiments served as the basis for formulating the carbon Plant Biology, Vol. 53, 2002, published with permission dioxide reduction cycle of photosynthesis. Although Calvin (1911–1997) had proposed the original concept of a cycle, 14 illuminated from both sides. After introducing CO2,sam- Benson was pivotal in bringing the idea to fruition. As a ples of the illuminated Scenedesmus suspension were re- result of expertise gained in carbohydrate chemistry during moved after short exposure times and collected in hot his doctoral research at Cal Tech, Benson was able to de- methanol, thereby stopping all enzymatic carbon reactions. velop techniques that the Calvin group adopted and applied The samples were then analyzed by two-dimensional paper for degrading 14C-labeled sugar phosphate intermediates to chromatography using solvents that had been developed for locate the 14C-label in individual C-atoms—innovations clear separation of the 14C-labeled metabolites formed in the central to deciphering the cycle. By late 1953, the photo- experiment. The labeled compounds were localized on the synthetic carbon reduction cycle had been more or less chromatograms and identified by autoradiography. These worked out and evidence for the complete cycle was pub- techniques, introduced by Benson to the Calvin group, sub- lished the following year (Bassham et al. 1954). sequently became the gold standard for 14C-labeling ex- Working with Jacques Mayaudon, a visiting professor periments by laboratories worldwide. Figure 2 shows Benson from Belgium, Benson showed that the highly abundant with a radiochromatogram. ‘‘fraction I protein’’ that Samuel Wildman (1912–2004) had In 1950, Benson, working on his own, detected and isolated catalyzed the incorporation of CO2 into ribulose 1,- chemically identified ribulose 1,5-bisphosphate (originally 5-bisphosphate to yield 3-phosphoglycerate (abbreviated named ribulose 1,5-diphosphate) as an essential component PGA). Mayaudon and Benson described their discovery of of the photosynthetic carbon reduction cycle. This 5-carbon this enzymatic activity in the draft of a manuscript they sugar phosphate proved to be the long-sought missing link presented to Calvin shortly after completing the work in of the cycle that enables photosynthetic organisms to fix 1954. However, Calvin shelved the manuscript and it was CO2 and form 3-phosphoglycerate—the compound Benson not published until three years later with Mayaudon as sole and Calvin had earlier identified as the first stable carbon author (Mayaudon 1957). Benson’s name was left off. product formed from CO2. All previous attempts to By then, Wildman had independently reported the CO2- identify the compound that accepts CO2 and yields fixing activity of the Fraction I protein that was called 123 Author's personal copy Photosynth Res (2015) 124:131–135 133 carboxydismutase (the enzyme is now known as ribulose Biology Research Division, Scripps Institution of 1,5-bisphosphate carboxylase or Rubisco). Benson had also Oceanography in La Jolla, where he spent the remainder of become fully occupied with other endeavors, and according his career, becoming emeritus in 1989. At Scripps he ini- to his letters and notes, he first became aware of the publi- tially continued his research on plant lipids, but with time, cation in 1997. At that time he also found out that Calvin turned his attention to marine biology. He and Ge´raud had reported his and Mayaudon’s results at the International Milhaud recognized the importance of calcitonin in calcium Congress of Biochemistry held in Brussels in 1955, men- regulation in salmon—a species they also studied as a model tioning Mayaudon, but not Benson. However, in a second for aging in humans. During this period, he identified wax as paper on the topic (Mayaudon et al. 1957) the names of both a major marine nutritional energy source important to the Benson and Calvin were included. survival of animals living in the sea. Benson went on to The picture is complicated by the fact that Calvin abruptly study the role of arsenic in oceans and identified previously dismissed Benson in 1954, the same year that evidence for the unknown intermediates of arsenic metabolism in aquatic complete cycle was published. When Benson left Berkeley, plants as well as the highest concentration of arsenic known he was appointed to the faculty at Pennsylvania State to accumulate in animals in kidneys of giant clams of the University (Penn State) where he drew on his earlier work Great Barrier Reef, Australia. Returning to plants, in 1992, with Calvin on thioctic (lipoic) acid and turned his attention to he and Arthur Nonomura discovered the ability of methanol plant lipids.
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