The McCree-de Wit-Penning de Vries-Thornley Respiration Paradigms: 30 Years Later

Abstract To grow, an organism must respire substrates to produce C-skeleton intermediates, usable energy (i.e. ATP), and reducing power [i.e. NAD(P)H] to support biosynthesis and related processes such as active transport of substrates. Respiration is also needed—mainly as a supplier of ATP—to maintain existing biomass in a functional state. As a result, quantifying links between respiration, growth, and maintenance are needed to assess potential plant productivity, to understand plant responses to environmental factors, and as the basis of cost-benefit analyses of alternative uses of photosynthate. Beginning 30 years ago, and continuing for about 5 years, rapid advances were made in understanding and quantifying relationships between respiration and the processes it supports. Progress has continued since then, though often as refinements rather than novel advances. The simplest framework (i.e. paradigm) for relating respiration to other processes divides respiration into growth and maintenance fractions. This often involves a combination of empiricism and mechanism. A three-component framework (growth, maintenance and wastage) has also been considered, although quantifying wastage (theoretically or empirically) remains problematic. The more general and flexible framework, called the general paradigm (GP, herein), relates respiration to any number of individual processes that it supports. The most important processes (from C and energy balance perspectives) identified to date that require respiration are: biosynthesis of new structural biomass, translocation of photosynthate from sources to sinks, uptake of ions from the soil solution, assimilation of N (including N 2 ) and S into organic compounds, protein turnover, and cellular ion-gradient maintenance. In addition, some part of respiration may be associated with wastage (e.g. futile cycles and mitochondrial electron transport uncoupled from oxidative phosphorylation). Most importantly, the GP can (semi-)mechanistically relate respiration to underlying physiology and biochemistry. The GP is more complicated than other approaches to describing or modelling respiration because it is more realistic, complete and mechanistic. This review describes a history of the GP and its present state. Future research questions are suggested.