Distinctive mitochondrial and chloroplast components contributing to the maintenance of carbon balance during plant growth at elevated CO ₂

Plant carbon balance depends upon the difference between photosynthetic carbon gain and respiratory carbon loss. In C₃ plants, growth at an elevated atmospheric concentration of CO₂ (ECO₂) stimulates photosynthesis and raises the leaf carbohydrate status, but how respiration responds is less understood. In this study, growth of Nicotiana tabacum at ECO₂ increased the protein amount of the non-energy conserving mitochondrial alternative oxidase (AOX). Growth at ECO₂ increased AOX1a transcript amount, and the transcript amount of a putative sugar-responsive gene encoding a chloroplast glucose-6-phosphate/phosphate translocator (GPT3). We suggest that the elevated amounts of AOX and GPT3 represent distinctive mitochondrial and chloroplast mechanisms to manage an excessive cytosolic pool of sugar phosphates. AOX respiration could consume cytosolic sugar phosphates, without this activity being restricted by rates of ATP turnover. GPT3 could allow accumulating cytosolic glucose-6-phosphate to return to the chloroplast. This could feed starch synthesis or a glucose-6-phosphate shunt in the Calvin cycle. AOX and GPT3 activities could buffer against P_i depletions that might otherwise disrupt mitochondrial and chloroplast electron transport chain activities. AOX and GPT3 activities could also buffer against a down-regulation of photosynthetic capacity by preventing a persistent imbalance between photosynthetic carbon gain and the activity of carbon utilizing sinks.

Keywords: Photosynthesis; alternative oxidase; carbon balance; elevated carbon dioxide; glucose-6-phosphate/phosphate translocator; inorganic phosphate; respiration; source:sink balance.