Organ-specific rates of cellular respiration in developing sunflower seedlings and their bearing on metabolic scaling theory

Abstract

Fifty years ago Max Kleiber described what has become known as the "mouse-to-elephant" curve, i.e., a log-log plot of basal metabolic rate versus body mass. From these data, "Kleiber's 3/4 law" was deduced, which states that metabolic activity scales as the three fourths-power of body mass. However, for reasons unknown so far, no such "universal scaling law" has been discovered for land plants (embryophytes). Here, we report that the metabolic rates of four different organs (cotyledons, cotyledonary hook, hypocotyl, and roots) of developing sunflower (Helianthus annuus L.) seedlings grown in darkness (skotomorphogenesis) and in white light (photomorphogenesis) differ by a factor of 2 to 5 and are largely independent of light treatment. The organ-specific respiration rate (oxygen uptake per minute per gram of fresh mass) of the apical hook, which is composed of cells with densely packaged cytoplasm, is much higher than that of the hypocotyl, an organ that contains vacuolated cells. Data for cell length, cell density, and DNA content reveal that (1) hook opening in white light is caused by a stimulation of cell elongation on the inside of the curved organ, (2) respiration, cell density and DNA content are much higher in the hook than in the stem, and (3) organ-specific respiration rates and the DNA contents of tissues are statistically correlated. We conclude that, due to the heterogeneity of the plant body caused by the vacuolization of the cells, Kleiber's law, which was deduced using mammals as a model system, cannot be applied to embryophytes. In plants, this rule may reflect scaling phenomena at the level of the metabolically active protoplasmic contents of the cells.

Kleiber's Law: How theFire of Lifeignited debate, fueled theory, and neglected plants as model organisms

“…42 This interpretation is also consistent with the fact that tissue-level DNA content correlates almost one-to-one with respiration rate 43 (Fig. 7B).…”

“…As an example of how different tissues affect respiration rates, we turn to studies of sunflower (Helianthus annuus L.) seedlings [42][43][44] (Fig. 7A).…”

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…At the intraspecific level, the hypometry of metabolic rate of various fish species relates, at least in part, to increases in the relative masses of tissues with low metabolic activity (e.g., fat and skeletal tissues), and decreases in the relative masses of tissues with high metabolic activity (e.g., brain, heart, kidney, hepatopancreas, and digestive tract) during growth (e.g., [152,186,187]. Supportive results also exist for plants [190,193], humans [194] and cladocerans [195], but not for amphipods [105,196] and insects [49]. In the freshwater amphipod Gammarus minus, the inter-population variation in the scaling of resting metabolic rate is unrelated to the scaling of relatively metabolically inert fat and skeletal materials [105].…”

“…During the last four decades, several investigators have rediscovered or revived system-composition (SC) models of metabolic scaling (e.g., [25,28,29,85,89,99,106,156,167,[186][187][188][189][190]; and other references cited in [19,20]). These models focus on how body-size-related changes in the relative proportions of system components (e.g., tissues and organs) with different metabolic activities affect the scaling of metabolic rate.…”

“…Kleiber [91,92,169] and Glazier [20] reviewed the early history of this viewpoint. Recent investigators have implicated membrane composition and function [89,167,179,234], mitochondrial activity and number [97,179,[235][236][237], intracellular transport costs [130], DNA content [182,190], and other biochemical factors [238], as importantly involved in the intrinsic cellular control of metabolic scaling. Evidence for and against various specific aspects of this approach can be found in [19,20,89,[91][92][93][94]130,167,169,[235][236][237][238][239][240][241][242][243].…”