The many meanings of gross photosynthesis and their implication for photosynthesis research from leaf to globe

Photosynthesis is a complicated process and its research has a long history (Govindjee & Gest 2002). During this history, components of the photosynthetic process and their interconnections were unravelled only gradually. As the understanding of photosynthesis deepened, terminologies and definitions of key concepts often had to be revised, in many cases, repeatedly, in order to correct earlier mistakes and/or accommodate new findings. For example, the definition of ‘photosynthesis’ itself has been changed many times. American Scientist Charles Barnes (1858–1910) coined the word ‘photosynthesis’, although he preferred to use the word ‘photosyntax’ to describe the light-driven reduction of CO2 to sugars in plants (Gest 2002). Earlier definitions of photosynthesis included simultaneous reduction of CO2 and evolution of O2, only to be corrected later after photosynthetic bacteria were discovered (Blankenship 2002). We are now facing a similar situation with the concept ‘gross photosynthesis’. ‘Gross photosynthesis’ is a term whose use has not been consistent in the long history of photosynthetic research. Historically, plant biochemists and physiologists, who studied photosynthesis at scales less than a leaf, did not consider photorespiration as part of photosynthesis even though photorespiration originates in chloroplasts (but photorespiratory CO2 is released via mitochondria into the cytosol), takes place simultaneously and competitively with CO2 reduction, and occurs only in light. This is because the discovery of photorespiration was relatively late (Decker 1955) and understanding its fundamental difference from the so-called dark respiration (also known as mitochondrial respiration) took even longer time (Bowes et al. 1971). Once photorespiration was discovered and its mechanism understood, researchers started to use the term ‘true photosynthesis’ to describe the total CO2 fixation (i.e. a measure of carboxylation or equivalently oxygen evolution in the Hill reaction or all electrons generated by photochemical reactions), not allowing for any loss of CO2 through darkand photorespiration. Meanwhile, the term ‘apparent photosynthesis’ was used to describe the difference between true photosynthesis and photorespiration, excluding dark respiration (Hew et al. 1969). Sometime during the following years, the term ‘gross photosynthesis’, which had been used earlier by experimental researchers of aquatic photosynthesis (e.g. Pratt & Berkson 1959), started to appear more frequently in the literature of general plant physiology. In the context of early aquatic studies, gross photosynthesis referred to the difference in oxygen concentrations between the light and dark bottles (Gaarder & Gran 1927; Pratt & Berkson 1959). In hindsight, gross photosynthesis in these early aquatic studies was actually equivalent to apparent photosynthesis because photorespiration occurs in the light bottle, but not in the dark bottle. Despite this early history, gross photosynthesis was used by plant biochemists and physiologists after the discovery of photorespiration to represent true photosynthesis. This use is continued in modern times as can be seen in influential textbooks of terrestrial and aquatic photosynthesis (e.g. Schopfer & Brennike 2010). Accompanying this changed meaning of gross photosynthesis, the term ‘net photosynthesis’ appeared and was used to describe the difference between true (gross) photosynthesis and the total (darkand photo-)respiratory losses of CO2, that is, the difference between apparent photosynthesis and dark respiration. Both gross photosynthesis and net photosynthesis are now key concepts at all scales of photosynthesis research from molecular to leaf to canopy to globe. Unfortunately, the history outlined previously has often been disregarded in the contemporary use of the term ‘gross photosynthesis’ and, to some extent, ‘net photosynthesis’ as well. Consequently, these two terms, particularly gross photosynthesis, have been used inconsistently across space and time scales. This situation is especially serious in ecologically oriented studies of photosynthesis, which have the ultimate goal of quantifying gross primary productivity (GPP). Sometimes, the same researcher may use these two terms for different meanings in the same paper (e.g. Porcar-Castell et al. 2014). The imprecise or incorrect use of different photosynthetic concepts has caused tremendous confusion. Because of the critical importance of photosynthesis to local, regional and global carbon cycles, it is essential to clear this confusion so that estimates of carbon budgets can be compared across space, time and methods. The present paper attempts to do so. We will appeal for respecting the historical developments of photosynthetic terminologies, which means the following: