PhotosynthesisResearch 46: 37-39, 1995. (~) 1995KluwerAcademicPublishers. Printedin theNetherlands. Historical corner

Photosynthesis, inorganic plant nutrition, solutions, and problems Emanuel Epstein Department of Land, Air and Water Resources, Soils and Biogeochemistry Program, University of California, Davis, Davis, CA, 95616-8627, USA Received8 March 1995;acceptedin revisedform 15 April 1995 Key words: D.I. Arnon, plant nutrition, solution culture, essentiality, silicon

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A brief account is given of the research that D.I. Arnon did before he ventured into the field of photosynthesis, viz. his work on inorganic plant nutrition in the laboratory of D.R. Hoagland. The connection between the two areas is indicated. In his work on plant nutrition Dr Arnon emphasized the role of specific nutrients and, with P.R. Stout, formulated a definition of essentiality that is used to this day. It is now necessary, however, to take into account elements not meeting their criteria of essentiality, as shown by a consideration of the element silicon. Photosynthetic phosphorylation was the groundbreaking discovery made by D.I. Amon and his coworkers; it is amply discussed in the first part of this special issue devoted to his outstanding career. It is most fitting, and no mere serendipity, that this discovery should have come from him. Certainly, he had the qualities of mind that make for success in science; they have been beautifully discussed by Beveridge (1950) in his The Art of Scientific Investigation. What is not adequately discussed there is the importance of the setting in which the young scientist starts out. For Amon, that setting was the renowned laboratory of plant nutrition founded by D.R. Hoagland at the University of California at Berkeley. It provided inspiration and guidance through the people with whom he had the opportunity to associate, and the example they set in two ways: their approach to science and the specific areas of expertise they excelled in. The incisive thinking so evident in Hoagland's Lectures on the Inorganic Nutrition of Plants (1944) left none untouched who had the privilege of being part of that environment. Hoagland was unfailingly gracious and kind, but when dubious thinking surfaced in a discussion or a seminar he did not hesitate to raise the issue, expose the fallacy - and then steer the talk into a new channel to move the discussion forward. He set a standard for other members of his group to emulate.

A second factor was the specific topic that Hoagland, his associates and students worked on: the inorganic nutrition of plants. Emphasis was on two subjects: the mechanism of ion transport and the significance of specific elements. Arnon collaborated with Hoagland and others in many investigations on these subjects and thus, well before he ventured into photosynthesis right after World War II, his name had become a household word among plant physiologists interested in inorganic plant nutrition. Micronutrients were one of the subjects he tackled in collaboration, principally, with Perry R. Stout (Arnon and Stout 1939a). This research of necessity was done with plants grown in solution culture, and to this day, the booklet by Hoagland and Arnon describing this technique, as revised by Arnon in 1950, is still quoted with great frequency. Nowhere at that time, in the years preceding and following World War II, was there a laboratory devoted to inorganic plant nutrition that could rival Hoagland's Division of Plant Nutrition. Amon's association with it had this important consequence when, after the war, he turned his attention to photosynthesis: his mind was not fixated on the element carbon. The very first paper to emerge from his work on this new topic, published in 1949, bore the title, Copper enzymes in isolated chloroplasts. Polyphenoloxidase inBeta vulgaris

38 (Arnon 1949). And who can doubt that this entire prior career in inorganic plant nutrition made him receptive to the idea that an element other than carbon, an inorganic, soil-derived nutrient, might play a central role in photosynthesis? Let us remember that Fritz Lipmann and Herman Kalckar had by 1941 recognized the central role which phosphate plays in biological energy transformations; by 1944 Robert Emerson had applied that insight to photosynthesis. That thinking was not lost on the avid student of contemporary biology that Arnon was. As for yet other inorganic nutrients and their significance to photosynthesis, Arnon himself has given an excellent account of the meshing together of his interests in inorganic plant nutrition and photosynthesis (Arnon 1951). Let us return, however, to his prior work in which the focus was on inorganic nutrition per se. Hoagland was under the impression that elements other than those then recognized as needed for the growth of plants might be necessary. (In addition to the macronutrient elements, iron, boron, manganese, zinc, and copper had by then been identified as micronutrients.) Hoagland prepared several ' A - Z ' solutions containing elements he considered candidates for micronutrient status. That and the microchemical skills of P.R. Stout (Stout and Arnon 1939) led to the discovery of the essentiality of molybdenum for the growth of higher plants (Arnon and Stout 1939b). Arnon and Stout were aware that there was no formal, generally accepted definition of the concept of essentiality and proceeded to formulate such a definition (Arnon and Stout 1939a): 'an element is not considered essential unless (a) a deficiency of it makes it impossible for the plant to complete the vegetative or reproductive stage of its life cycle; (b) such deficiency is specific to the element in question, and can be prevented or corrected only by supplying this element; and (c) the element is directly involved in the nutrition of the plant quite apart from its possible effects in correcting some unfavorable microbiological or chemical condition of the soil or other culture medium'. This is an excellent operational definition and entirely satisfactory for establishing an element as essential. It has, however, two drawbacks, one recognized from the beginning and dependent on advances in microchemistry, the other conceptual in nature and only now becoming recognized. The former difficulty is straightforward. Techniques for removing small amounts of contaminant elements from the major nutrient salts needed for making up nutrient solutions are not perfect. By means

of modern analytical chemistry small amounts of such elements as selenium, strontium, silicon, and many others can be demonstrated in any nutrient solution, no matter what precautions were taken to remove them. Water, containers, and the atmosphere are also sources of such elements. It would thus be foolhardy to assert that these elements are not essential; 'not known to be essential' is more valid terminology (Epstein 1972). Thus until recently, nickel was not known to be essential for higher plants. The requirement for it being minute, even carefully prepared culture solutions contained enough of the element to supply experimental plants adequately with the element. But when Brown et al. (1987) used a new method of preparing highly purified nutrient solutions they showed that barley plants could not complete their life cycle unless nickel was deliberately added to the solutions. Nickel is now recognized as an essential element for higher plants generally. Other such discoveries of new micronutrients may well be in the offing. The other problem with the definition of essentiality formulated by Arnon and Stout (1939a) is more pernicious. The definition, rigid and explicit in its operational criteria of essentiality, has willy-nilly led to the view that elements not meeting these criteria are ipso facto of no account to plant biology, need not be included in the formulation of nutrient solutions, and can be disregarded with impunity. Since 1988 that view has been questioned. It was a consideration of the element silicon that occasioned this challenge to received doctrine (Epstein et al. 1988; Huang et al. 1992; Epstein 1994). Silicon is the second most prevalent element in soils, the mineral medium of most of terrestrial plant life. Its concentration in the soil water (strictly, the soil solution) is appreciable, on the order of 0.1-0.6 mM. As H4SiO4, its dominant form in soils with a pH of about 7.5 and below, it is readily absorbed by plant roots and transported to the shoot. Hence plant material generally contains silicon in amounts of the same order of magnitude as that of calcium, sulfur, and other macronutrient elements, the particulars depending on the soil, the genotype, and other factors. In some plants, such as wetland grasses (paddy-grown rice), the silicon content may be on the order of 5% of the dry matter, equaling or exceeding that of nitrogen. Much of the silicon is normally located in the cell wall, in the form of amorphous silica or 'opal', Sit2 • nH20. It has large effects on the physical properties of the cell wall. There are some soils that are rather poor sources of silicon, and such crops as rice and sugarcane on

39 these soils may benefit from applications of silica slag, because without it they tend to lodge as a result of having inadequately rigid cell walls. Epstein (1994) has documented many other such effects, chemical as well as physical, and including a number which bear on photosynthesis. The conclusion emerged from this survey that the plant physiologist's solution cultured plants, deprived of silicon except for what little of it is supplied as an inadvertent contaminant, are to an extent experimental artifacts. They differ so markedly from normal, soil grown plants, with their substantial silicon content, that the addition of silicon to solution cultures should not be considered an experimental treatment but as the normal, control condition. It is the usual omission of the element that ought to be looked upon as a treatment - a treatment with many untoward consequences for the biological competence of the plant (Epstein 1994). So far, however, this laboratory is the only one on record in which silicon is routinely included in the formulation of solution cultures (Epstein 1994, and references there). What, then, should we do about the definition of essentiality as it now stands? It has served well in the past and should not be abandoned. But we should recognize that elements failing the criteria for essentiality cannot be disregarded and omitted. We need to reexamine our thinking about the elements that go into the make-up of plants. Specifically, we should include silicon in the formulation of solution cultures. In doing so we shall depart from long established thinking and practice. What better compliment could we pay to our predecessors such as Daniel Arnon, who set an example by doing precisely that?

Acknowledgments Research in the author's laboratory on silicon in plant biology is supported by the US Department of EnergY.

References ArnonDI (1949) Copperenzymesin isolatedchloroplasts.Polyphenoloxidasein Beta vulgaris. Plant Physiol24: 1-15 Amon DI (1951) Growth and functionas criteriain determiningthe essentialnature of inorganicnutrients.In: TruogE (ed) Mineral Nutrition of Plants, pp 313-341. The University of Wisconsin Press, Madison Amon DI and Stout PR (1939a) The essentialityof certainelements in minute quantity for plants with special reference to copper. Plant Physiol 14:371-375 AmonDI and StoutPR (1939b)Molybdenumas an essentialelement for higherplants. Plant Physio114: 599-602 Beveridge WIB (1950) The Art of Scientific Investigation.WW Norton Company,New York Brown PH, Welch RM and Cary EE (1987) Nickel: a micronutrient essentialfor higherplants. Plant Physiol 85:801-803 Epstein E (1972) Mineral Nutrition of Plants: Principlesand Perspectives. John Wileyand Sons, New York Epstein E (1994) The anomalyof silicon in plant biology.Proc Natl Acad Sci USA 91:11-17 Epstein E, NorlynJD and Cabot C (1988) Siliconand plant growth. Plant PhysiolSuppl 86(4): 134 (Abstract804) Hoagland DR (1944) Lectures on the InorganicNutritionof Plants. ChronicaBotanicaCompany,Waltham Hoagland DR and Arnon DI (1950) The Water-CultureMethod for GrowingPlantswithoutSoil. Circular347. The College of Agriculture, Universityof California,Berkeley Huang Z-Z, Yan X, Jalil A Norlyn JD and Epstein E (1992) Shortterm experimentson ion transportby seedlingsand excised roots: Techniqueand validity.Plant Physiol 100:1914-1920 Stout PR and Arnon DI (1939) Experimentalmethods for the study of the role of copper, manganese, and zinc in the nutrition of higher plants. Am J Bot 26:144-149

Photosynthesis, inorganic plant nutrition, solutions, and problems.

A brief account is given of the research that D.I. Arnon did before he ventured into the field of photosynthesis, viz. his work on inorganic plant nut...
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