Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration

Abstract

We examined the effect of short-and long-term changes in temperature on gene expression, protein abundance, and the activity of the alternative oxidase and cytochrome oxidase pathways (AOP and COP, respectively) in Arabidopsis thaliana. The AOP was more sensitive to short-term changes in temperature than the COP, with partitioning to the AOP decreasing significantly below a threshold temperature of 20°C. AOP activity was increased in leaves, which had been shifted to the cold for several days, but this response was transient, with AOP activity subsiding (and COP activity increasing) following the development of leaves in the cold. The transient increase in AOP activity in 10-d cold-shifted leaves was not associated with an increase in alternative oxidase (AOX) protein or AOX1a transcript abundance. By contrast, the amount of uncoupling protein was significantly increased in cold-developed leaves. In conjunction with this, transcript levels of the uncoupling protein-encoding gene UCP1 and the external NAD(P)H dehydrogenase-encoding gene NDB2 exhibited sustained increases following growth in the cold. The data suggest a role for each of these alternative non-phosphorylating bypasses of mitochondrial electron transport at different points in time following exposure to cold, with increased AOP activity being important only in the early stages of cold treatment.

Thermal acclimation of leaf photosynthetic traits in an evergreen woodland, consistent with the coordination hypothesis

“…Acclimation results in R dark being of similar magnitude in plants grown at different temperatures when measured at their respective growth temperatures (Larigauderie and Körner, 1995;Atkin and Tjoelker, 2003) and also results in R dark at 25 • C, increasing upon cold acclimation and declining upon acclimation to warmer temperature . Growth temperature-dependent changes in R dark at a standard temperature can occur over periods of 1-3 days (Atkin et al, 2000;Bolstad et al, 2003;Lee et al, 2005;Zaragoza-Castells et al, 2007;Armstrong et al, 2008). A data synthesis of global patterns in R dark showed that geographic variation in R dark at growth temperature from the tropics to the tundra is much smaller than would be expected on the basis of enzyme kinetics.…”

Thermal acclimation of leaf photosynthetic traits in an evergreen woodland, consistent with the co-ordination hypothesis

“…acclimation and declining upon acclimation to warmer temperature (Reich et al, 2016). Growth temperature dependent changes in R dark at a standard temperature can occur over periods of 1-3 days (Atkin et al, 2000;Bolstad et al, 2003;Lee et al, 2005;Zaragoza-Castells et al, 2007;Armstrong et al, 2008). An example of acclimation is a recent data synthesis of global patterns in leaf R dark which showed that geographic variation in R dark at growth temperature from the tropics to the tundra is much smaller than would be expected on the basis of enzyme kinetics.…”

Post-transcriptional Regulation in Mitochondria of Rice and Wheat at Low Temperatures

“…For wheat at 2/0.5˚C, the accumulation of the intron-spliced transcript has a tendency to increase 39 , while in the case of rice at 12˚C, post-splicing transcripts remained almost unchanged 41 (Table 1). This does not contradict the increases in cytochrome pathway activity in cold acclimatable plants 3,79 . The RNA editing status of wheat mitochondria at low temperatures also resembles that in rice 40 .…”

“…It was reported that maintenance of growth rates at low temperatures in wheat cultivars with a high degree of respiratory homeostasis was associated with highly efficient respiratory ATP production 42 . It was also reported that Arabidopsis leaves developed at low temperatures showed increased COXII protein abundance and a drastically increased cytochrome pathway capacity, with a transient increase in alternative oxidase activity 3 that may only be significant in the early stages of cold treatment.…”

“…A temporal difference exists between developmental-and cold-induced increases, in that the accumulation of intron-containing transcripts is maximized half to one day after imbibition, whereas 3 to 7 days are required after cold treatment. However, mitochondrial responses are shared by germinating seeds and cold-treated plants, such as increased O 2 uptake capacity, differential fluxes between cyanide-sensitive (mainly, cytochrome) and -insensitive respiratory (AOX) pathways, and the activation of some mitochondrial genes encoded in the nuclear genome 3,42,52,62 . It is possible that one or more of these responses is directly associated with the accumulation of intron-containing transcripts and will shed light on the physiological significance of the phenomenon.…”