The paths of Andrew A. Benson: a radio-autobiography.

Andrew A. Benson, one of the greatest biochemists of our time, is celebrated on his centennial by the authors with whom he interacted performing experiments or contemplating metabolic pathways in a wide range of biological kingdoms. He charted the chemical flow of energy in cells, tissues, organs, plants, animals, and ecosystems. Benson collaborated with hundreds of colleagues to examine the natural history of autotrophy, mixotrophy, and heterotrophy while elucidating metabolic pathways. We present here a biological perspective of his body of studies. Benson lived from September 24, 1917, to January 16, 2015. Out of over 1000 autoradiograms he produced in his life, he left a legacy of 50 labeled autoradiograms to the authors who tell the story of his life's work that resulted in Benson's Protocol (Nonomura et al., Photosynth Res 127:369-378, 2016) that has been applied, over the years, for the elucidation of major metabolic pathways by many scientists.

Andrew A. Benson: personal recollections.

Andrew A. Benson, one of the greatest and much loved scientists of our century, passed away on January 16, 2015; he was born on September 24, 1917. A grand celebration of his life was held on February 6, 2015, in California. Here, we present one of his photographs and key excerpts from what was said then, and soon thereafter.

Untangling metabolic and spatial interactions of stress tolerance in plants. 1. Patterns of carbon metabolism within leaves.

The localization of the key photoreductive and oxidative processes and some stress-protective reactions within leaves of mesophytic C(3) plants were investigated. The role of light in determining the profile of Rubisco, glutamate oxaloacetate transaminase, catalase, fumarase, and cytochrome-c-oxidase across spinach leaves was examined by exposing leaves to illumination on either the adaxial or abaxial leaf surfaces. Oxygen evolution in fresh paradermal leaf sections and CO(2) gas exchange in whole leaves under adaxial or abaxial illumination was also examined. The results showed that the palisade mesophyll is responsible for the midday depression of photosynthesis in spinach leaves. The photosynthetic apparatus was more sensitive to the light environment than the respiratory apparatus. Additionally, examination of the paradermal leaf sections by optical microscopy allowed us to describe two new types of parenchyma in spinach-pirum mesophyll and pillow spongy mesophyll. A hypothesis that oxaloacetate may protect the upper leaf tissue from the destructive influence of active oxygen is presented. The application of mathematical modeling shows that the pattern of enzymatic distribution across leaves abides by the principle of maximal ecological utility. Light regulation of carbon metabolism across leaves is discussed.

Untangling metabolic and spatial interactions of stress tolerance in plants. 2. Accelerated method for measuring and predicting stress tolerance. Can we unravel the mysteries of the interactions between photosynthesis and respiration?

A simple method using the O(2) electrode that allows examination of the response of respiration and photosynthesis in leaf slices or algae to anoxia and high light under different temperatures useful for the examination of the interactions among photosynthesis, photorespiration, and respiration is described. The method provides a quantifiable assessment of stress tolerance that also permits us to examine fundamental biochemically and genetically related responses involved in stress tolerance and the cooperation among organelles. Additionally, we demonstrated a role for compounds, such as NO(-)(3) and oxaloacetate, as protective agents against photoinhibition, and we examined the role of dark adaptation in the activation of photosynthesis and NO(-)(3)-dependent O(2) oxygen evolution. A physiological and ecological role of a dark period (night) in stress tolerance is presented. Utilizing the method to follow changes in such metabolic activities as protein synthesis, protein conformation states, enzymes activity, carbon metabolism, and gene expression at different points during the treatments will be educational.

Structural features of the salt glands of the leaf of Distichlis spicata 'Yensen 4a' (Poaceae).

The epidermal salt glands of the leaf of Distichlis spicata 'Yensen 4a' (Poaceae) have a direct contact with one or two water-storing parenchyma cells, which act as collecting cells. A vacuole occupying almost the whole volume of the collecting cell has a direct exit into the extracellular space (apoplast) through the invaginations of the parietal layer of the cytoplasm, which is interrupted in some areas so that the vacuolar-apoplastic continuum is separated only by a single thin membrane, which looks as a valve. On the basis of ultrastructural morphological data (two shapes of the extracellular channels, narrow and extended, are found in basal cells), the hypothesis on the mechanical nature of the salt pump in the basal cell of Distichlis leaf salt gland is proposed. According to the hypothesis, a driving force giving ordered motion to salt solution from the vacuole of the collecting cell through the basal cell of the salt gland to cap cell arises from the impulses of a mechanical compression-expansion of plasma membrane, which penetrates the basal cell in the form of extracellular channels. The acts of compression-expansion of these extracellular channels can be realized by numerous microtubules present in the basal cell cytoplasm.

A photoacoustic method for rapid assessment of temperature effects on photosynthesis.

The photosynthetic and photoacoustic properties of leaf samples were studied using a photoacoustic system modified for precise temperature control. Data were collected over a temperature range of -10 degrees C to +60 degrees C. A distinct acoustic noise transient marked the freezing temperature of the samples. A positive absorption transient and a brief period of oxygen uptake marked the thermal denaturing temperature of the samples. Between these extremes, the effects of temperature on light absorption, oxygen evolution, and photochemical energy storage were quantified quickly and easily. Oxygen evolution could be measured as low as -5 degrees C and showed a broad temperature peak that was 10 degrees C lower under limiting light intensity than under saturating light intensity. Photochemical energy storage showed a narrower temperature peak that was only slightly lower for limiting light intensities than for saturating light intensities. In a survey of diverse plants, temperature response curves for oxygen evolution were determined readily for a variety of leaf types, including ferns and conifer needles. These results demonstrate that temperature-controlled photoacoustics can be useful for rapid assessment of temperature effects on photosynthesis and other leaf properties.