The origin of cytosolic ATP in photosynthetic cells

Abstract

In photosynthetically active cells, both chloroplasts and mitochondria have the capacity to produce ATP via photophosphorylation and oxidative phosphorylation, respectively. Thus, theoretically, both organelles could provide ATP for the cytosol, but the extent, to which they actually do this, and how the process is regulated, both remain unclear. Most of the evidence discussed comes from experiments with rapid fractionation of isolated protoplasts subjected to different treatments in combination with application of specific inhibitors. The results obtained indicate that, under conditions where ATP demand for photosynthetic CO2 fixation is sufficiently high, the mitochondria supply the bulk of ATP for the cytosol. In contrast, under stress conditions where CO2 fixation is severely limited, ATP will build up in chloroplasts and it can then be exported to the cytosol, by metabolite shuttle mechanisms. Thus, depending on the conditions, either mitochondria or chloroplasts can supply the bulk of ATP for the cytosol. This supply of ATP is discussed in relation to the idea that mitochondrial functions may be tuned to provide an optimal environment for the chloroplast. By balancing cellular redox states, mitochondria can contribute to an optimal photosynthetic capacity.

ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology

“…Governance of cytosolic ATP levels by two bioenergetic organelles in green plant cells raises important questions about the regulatory basis of subcellular ATP control (Gardeström and Igamberdiev, 2016). The cytosolic sensor lines indicated no differences in ratio between cytosol and nucleoplasm, indicative of rapid diffusion between the two locations and in line with previous observations for free Ca 2+ concentrations and glutathione redox potential (Loro et al, 2012; Schwarzländer et al, 2016).…”

“…Thus, regulation of cytosolic and organelle ATP levels, and ATP/ADP transport across the mitochondrial and plastid envelope, give rise to particularly complex ATP dynamics in plant cells, that is critically dependent on the tissue type and external conditions (Neuhaus et al, 1997; Flügge, 1998; Reiser et al, 2004; Haferkamp et al, 2011). The exact nature of the interplay between mitochondria and chloroplasts in maintaining cytosolic and nuclear ATP homeostasis, especially under changeable conditions, such as light–dark cycles or varying O 2 /CO 2 status, has been investigated for decades, predominantly using biochemical techniques or in vivo NMR (Bailleul et al, 2015; Gardeström and Igamberdiev, 2016). For example, insight into subcellular adenine nucleotide pools have been possible through rapid membrane filter-based fractionation of leaf protoplasts, revealing a complex and dynamic interplay between the three cell compartments (Lilley et al, 1982; Stitt et al, 1982; Gardeström and Wigge, 1988; Krömer and Heldt, 1991; Krömer et al, 1993).…”

Coordinated regulation of photosynthetic and respiratory components is necessary to maintain chloroplast energy balance in varied growth conditions

“…Another possibility relates to a hypothesis put forward by Rasmusson and co-workers who suggested that the amount of AOX protein must be sufficient to support its ‘peak activity’, which might be significantly higher than its usual activity (Rasmusson et al , 2009). For example, it has been suggested that high AOX activity may be necessary during the photosynthetic induction period following darkness (Gardestrӧm and Igamberdiev, 2016). An energy imbalance could develop during this period since the energy-generating thylakoid reactions of photosynthesis become engaged more quickly that the energy-consuming Calvin cycle reactions.…”

“…Respiration in the mitochondrion and photosynthesis in the chloroplast share important carbon and energy intermediates, and hence it is thought that these pathways must act in a coordinated manner to optimize energy metabolism in the leaf cell (Hoefnagel et al , 1998; Gardestrӧm et al , 2002; Noctor et al , 2007; Noguchi and Yoshida, 2008; Nunes-Nesi et al , 2008; Tcherkez et al , 2012; Gardestrӧm and Igamberdiev, 2016). For example, an imbalance of energy intermediates in one organelle might be offset by compensatory metabolic changes in the other organelle.…”

Nitrogen Source Dependent Changes in Central Sugar Metabolism Maintain Cell Wall Assembly in Mitochondrial Complex I-Defective frostbite1 and Secondarily Affect Programmed Cell Death

“…Plant mitochondria carry out the final step of respiration to integrate sugar catabolism with ATP production. Therefore, mitochondria drive metabolism throughout the cell, since they can regulate energy and redox balance [3,4,5]. Furthermore, the central metabolic position of mitochondria, and their key roles in bioenergetics, mean that they are ideally placed to act as sensors and integrators of the biochemical status of the cell.…”