All life on earth ultimately relies on energy from the sun, and photosynthesis is the vital link. Photosynthesis generates adenosine triphosphate (ATP), which is the universal molecular fuel in living organisms. An international team of researchers developed an approach to visualize ATP in living plants and observed that mature plant chloroplasts manage their ATP largely in isolation from other cellular spaces. The results pinpoint a strategy of plants to use their energy efficiently that could inform future crop breeding.

Their observations indicated that only chloroplasts of very young developing leaves of Arabidopsis thaliana could import ATP from the cytosol to support chloroplast development, whereas the rate of ATP import into mature chloroplasts to support CO2fixation was negligible. This developmental transition could be important in order to restrict futile ATP consumption at night when photosynthesis is not operating.

“We saw a significantly lower concentration of ATP in the chloroplast than in the cytosol of mature photosynthetic cells,” said study lead author Dr Boon Leong Lim from School of Biological Sciences of The University of Hong Kong. “Although the chloroplast is the key energy harvester and producer in a plant cell, its demand for ATP is also extremely high. Illumination increases chloroplast ATP concentration instantly, but it drops to a basal level very quickly after illumination stops. Our results suggest that there was a need to restrict ATP consumption in mature chloroplasts in the dark. A primary job of mature mesophyll chloroplasts is to harvest energy and export sugar to support plant growth in the light. Nevertheless, wasteful energy consumption must be avoided in the dark.” Their findings were published recently in the journal Proceedings of the National Academy of Sciences.

Co-authors Dr Wayne K. Versaw and Abira Sahu of Texas A&M University said “Live imaging of intact plants provided the spatial and temporal resolution to reveal important changes in how different cell compartments collaborate to manage photosynthesis and overall cellular energy.”

These results also have important implications for the understanding of energy flow in plant cells. Using energy harvested from sunlight, water molecules are split into protons, oxygen and electrons. The electrons pass through photosystems to reduce NADP+ to NADPH. Together with water splitting, this so called linear electron flow (LEF) also creates a pH gradient across the thylakoid membrane, which is the driving force for ATP synthesis. To fix one CO2 molecule in a chloroplast, 3 ATP and 2 NADPH molecules are consumed. However, only 2.57 ATP molecules per 2 NADPH are generated by LEF. The shortfall of ATP must be met for photosynthesis to operate efficiently. A paper published in Nature in 2015 (524:366-369) showed that chloroplasts in unicellular diatoms can import cytosolic ATP to support carbon fixation.

Chiapao Voon, who joined the lab as a PhD student, said: “Unlike unicellular diatoms, mature plant chloroplasts are unable to import ATP from the cytosol to supplement the demand for CO2 fixation. Rather, the export of reducing equivalents is the key to maintaining the optimal ATP/NADPH ratio required for photosynthesis. Otherwise, the build-up of NADPH in chloroplasts will impede photosynthesis”.

“The ability to study metabolism in the living cell with a spatial resolution between the different cellular compartments is a big step forward and will significantly increase our understanding on how the cell is operating. I have in particular been interested in the implications for mitochondrial contributions to photosynthetic metabolism” said co-author Prof. Per Gardeström of Umeå University.

Co-author Prof. Markus Schwarzländer of Münster University added “The study brings us a step closer to understanding how carefully cells optimize the operating conditions in their different organelles. I find it particularly intriguing how efficiency of plant energy metabolism can be maintained, and how this appears to be dynamically adjusted.

IMAGE SOURCE: Creative Commons

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