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• W1554439392 abstract "Over the past decade there have been several claims of sensor-operated respiratory down-regulation in plants at O2 pressures greatly in excess of the critical O2 pressure (COP) for mitochondrial respiration (Geigenberger et al., 2000; Gupta et al., 2009; Zabalza et al., 2009). These claims, which have largely gone unchallenged until recently (Colmer & Voesenek, 2009; Colmer & Greenway, 2011), seem to have been based principally on the results of respirometry data interpreted with reference to evidence that eukaryotes, such as yeast and animal cells, operate O2-consumption control mechanisms. However, there is other evidence that the O2 concentration ([O2]) dependency of O2 consumption by yeast and certain animal cells can also be described by Michaelis–Menten plots that have very low Km values and low COPs for respiration (Longmuir, 1954). Similarly, there is long-standing evidence that the respiration of plant cells is relatively indifferent to the [O2] until levels are ≤ 1–2 kPa in the tissues (Thimann et al., 1954; Yocum & Hackett, 1957; Armstrong & Gaynard, 1976) and more recent evidence also supports this point (Lammertyn et al., 2001; Laisk et al., 2007). However, measurements based on tissues/whole organs can introduce very substantial diffusion limitations on O2 supply. Our paper (Armstrong & Beckett, 2010) is concerned specifically with assessing the robustness of the interpretations of the respirometry data for roots that is presented by Zabalza et al. (2009) and Gupta et al. (2009) in support of their controlled down-regulation hypothesis. We found that their results could be explained without the necessity to invoke an O2-sensed down-regulation of respiration. Rather, the data could be readily accounted for in terms of severe hypoxia at the centre of roots (brought about by respiration and diffusion limitations) spreading radially outwards under the influence of a diminishing O2 supply in the respirometer fluid. In their Letter, Nikoloski & van Dongen (2011) argue that our results do not allow us to refute their hypothesis of controlled down-regulation. We hoped that we had made it clear in our Perspectives and Conclusions that we were not seeking to dismiss all suggestions of sensor-based respiratory down-regulation in plants. However, the control mechanism envisaged by Nikoloski & van Dongen appears to be one that starts to operate at a high [O2]. What we were refuting was the interpretation that Zabalza et al. (2009) and Gupta et al. (2009) placed upon their respirometry evidence in support of this. The complete scavenging of respirometer O2 to zero in a relatively short time frame (< 2 h; Zabalza et al., 2009; Gupta et al., 2009) also argues against a ‘metabolic regulation’ or homeostatic [O2] control in their roots and against a gradual [O2]-dependent expression of COX genes (Burke & Poyton, 1998). If instead of using a Michaelis–Menten response, we programme our model to effect an [O2]-dependent decline in the cell respiration from the start of the scavenging period (the type of control apparently envisaged by Nikoloski & van Dongen (2011), scavenging to near zero takes > 5 h rather than the c. 90 min observed by Zabalza et al. (2009) and Gupta et al. (2009). Furthermore, well-documented examples of hypoxia and fermentation in the stele of roots surrounded by an aerobic nonfermenting cortex (Thomson & Greenway, 1991) are not consistent with a down-regulation hypothesis of the type envisaged by Nikoloski & van Dongen (2011). Additionally, by modelling we were able to show that a rise in respiration is to be expected, even if roots that are already O2 deficient are fed with additional respiratory substrate (e.g. pyruvate). This contradicted the intuitive assumptions of Zabalza et al. (2009) and Gupta et al. (2009), viz. that increased respiration on pyruvate feeding indicates prior O2 sufficiency; this interpretation was a major plank in their arguments in favour of down-regulation. Another consideration is that if down-regulation operates only when the [O2] in the cell/organelles is approaching very low values (e.g. 0.1 μM for seeds; Borisjuk & Rolletschek, 2009) or requires long exposure at specific O2 levels to be realized, this would not be revealed by experiments such as those of Zabalza et al. (2009), or Gupta et al. (2009). Ho et al. (2010a,b; cited by Nikoloski & van Dongen, 2011) and colleagues (Lammertyn et al., 2001) have consistently demonstrated, by modelling and experiments, the importance of the combined effects of diffusive resistance and demand in determining the O2 profiles through pear and other fruits. Their results are consistent with those that we obtain for roots with respiratory demand following Michaelis–Menten-type plots similar to ours and respiration unaffected by [O2] until this is very low. Excellent comparisons between whole organs and protoplasts of pear are again supportive of the approach that we have taken: respiratory activity in pear protoplasts began to diminish along a Michaelis–Menten type curve at a COP of c. ≤ 2 kPa (Km = 3 μM) depending upon the temperature. However, whole pears with their diffusive limitations displayed an apparent Km of 82 μM, and large pears can develop severely hypoxic/anaerobic cores, even when in air. Again this does not seem to indicate O2-conserving down-regulation processes at work. Finally, whole leaves of plants with their labyrinth of gas space and small diffusion limitations have been shown to exhibit very low COPs and apparent Km values of viz. 0.33–1.1 μM (Laisk et al., 2007). In our study we adapted methods of mathematical modelling that have a proven record of predicting observed data for O2 transport and distribution in plants. Some of the input data in our current paper involved a limited amount of educated guesswork necessary because, for example, specific anatomical information was not available in the papers of Zabalza et al. (2009), or Gupta et al. (2009). However, we believe that the estimates used were within acceptable limits and we reject the view expressed by Nikoloski & van Dongen (2011) that our modelling approach does not allow us to discriminate between different hypotheses. For the specific examples chosen, we believe that we have shown clearly that it can. We were confused by Nikoloski & van Dongen’s (2011)‘four alternatives for modelling oxygen uptake’ and uncertain as to the meaning or relevance of their additional paragraphs on future modelling. Their references to ways that differential equations arise in the study of O2 uptake are inconsistent with the classifications used in our mathematical model: this may go some way to explaining their confusion. Ultimately, the question of what, if any, [O2]-controlled metabolic down-regulation of respiration occurs in plants can only be fully resolved by appropriate experimental methods, not by mathematical modelling. Modelling can only be a helpful interpretative and predictive tool. In the case of roots, attention must be paid to both short-term and long-term exposure to O2 decline and to the previous physiological state. For example, the result might be quite different in an actively growing root compared with one that has stopped growing because it has reached the limits of its internal O2 supply from the shoot. One possibility for resolving whether controlled down-regulation of respiration occurs in roots might be to extend the types of study employed by Armstrong et al. (1994, 2009), Gibbs et al. (1998) and Darwent et al. (2003), which involve the measurement of radial O2 concentration gradients across the root and into the stele while manipulating the [O2] at source: either around the shoot or in the medium around the root. For the situation in which there is controlled down-regulation starting at high O2 pressures, as envisaged by Nikoloski & van Dongen (2011), the O2 profiles across the stele, for example, should show a gradual decline in steepness (and deficit) with decreasing source concentration (Fig. 1a). If, on the other hand, respiration follows the Michaelis–Menten-type curve shown in our paper, then the profiles (and O2 deficits) across the stele will tend to match each other with declining source concentration until the [O2] within the stele falls below c. 1–2 kPa (Fig. 1b). This is more or less what has been found in existing data (Armstrong et al., 1994; Gibbs et al., 1998; Darwent et al., 2003), again indicating that any down-regulation, if it exists, occurs at a very low internal [O2]. Studies of this type require microprobes with a very small tip diameter (of at least ≤ 12 μm) to minimize damage. It is also necessary to ensure that sensor performance is not compromised by abrasion or the physico-chemical characteristics of the tissues and that probes follow a strictly radial, not tangential, path. Measurements of radial O2 loss from apical regions of roots while manipulating shoot [O2] can also potentially detect [O2]-concentration-induced changes in respiratory activity. Again, existing data indicate that respiration does not decline until a very low [O2] is reached (Armstrong & Gaynard, 1976; Garthwaite et al., 2008; Armstrong et al., 2009). Similarly, extension growth in rice roots did not decline until the cortical [O2] fell below 2 kPa (Armstrong & Webb, 1985), while measurements of the gas-phase [O2] in the leaves of whole plants of the wetland sedge, Eriophorum angustifolium, revealed no decline in respiratory activity until the internal [O2] had fallen below 3 kPa (Armstrong & Gaynard, 1976). Predicted radial oxygen concentration ([O2]) profiles across the stele of roots with a diminishing source [O2] under the influence of (a) concentration-dependent sensor down-regulation of respiration, and (b) respiration vs concentration following a Michaelis–Menten relationship. In (a) the profile gradients are all different, whereas in (b) the top six profiles (where the [O2] is above the critical oxygen pressure at all points) are identical. To conclude, nothing in the letter by Nikoloski & van Dongen (2011) has persuaded us to deviate from our original conclusions. The readership must be left to judge the veracity of the various approaches." @default.
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• W1554439392 title "The respiratory down-regulation debate" @default.
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