Universal scaling of respiratory metabolism, size and nitrogen in plants

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, United States
Nature (Impact Factor: 42.35). 02/2006; 439(7075):457-61. DOI: 10.1038/nature04282
Source: PubMed

ABSTRACT The scaling of respiratory metabolism to body size in animals is considered to be a fundamental law of nature, and there is substantial evidence for an approximate (3/4)-power relation. Studies suggest that plant respiratory metabolism also scales as the (3/4)-power of mass, and that higher plant and animal scaling follow similar rules owing to the predominance of fractal-like transport networks and associated allometric scaling. Here, however, using data obtained from about 500 laboratory and field-grown plants from 43 species and four experiments, we show that whole-plant respiration rate scales approximately isometrically (scaling exponent approximately 1) with total plant mass in individual experiments and has no common relation across all data. Moreover, consistent with theories about biochemically based physiological scaling, isometric scaling of whole-plant respiration rate to total nitrogen content is observed within and across all data sets, with a single relation common to all data. This isometric scaling is unaffected by growth conditions including variation in light, nitrogen availability, temperature and atmospheric CO2 concentration, and is similar within or among species or functional groups. These findings suggest that plants and animals follow different metabolic scaling relations, driven by distinct mechanisms.


Available from: Mark Tjoelker, May 17, 2015
  • [Show abstract] [Hide abstract]
    ABSTRACT: A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential ‘metabolic theory of ecology’) may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) – direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.
    Biological Reviews 05/2015; 90(2):377-407. · 9.79 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Tissue expansion and patterning are integral to development; however, it is unknown quantitatively how a mother accumulates molecular resources to invest in the future of instructing robust embryonic patterning. Here we develop a model, Tissue Expansion-Modulated Maternal Morphogen Scaling (TEM(3)S), to study scaled anterior-posterior patterning in Drosophila embryos. Using both ovaries and embryos, we measure a core quantity of the model, the scaling power of the Bicoid (Bcd) morphogen gradient's amplitude nA. We also evaluate directly model-derived predictions about Bcd gradient and patterning properties. Our results show that scaling of the Bcd gradient in the embryo originates from, and is constrained fundamentally by, a dynamic relationship between maternal tissue expansion and bcd gene copy number expansion in the ovary. This delicate connection between the two transitioning stages of a life cycle, stemming from a finite value of nA~3, underscores a key feature of developmental systems depicted by TEM(3)S.
    Nature Communications 01/2015; 6:6679. DOI:10.1038/ncomms7679 · 10.74 Impact Factor
  • Source
    Ecology 10/2014; 95(10):2815-2825. DOI:10.1890/13-1955.1 · 5.00 Impact Factor