Department of Biology, University of Padova, Via Ugo Bassi 58/B, Padova, 35131, Italy.
Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, Münster, D-48143, Germany.
New Phytol. 2024 Sep;243(6):2175-2186. doi: 10.1111/nph.19989. Epub 2024 Jul 28.
Plants rely on solar energy to synthesize ATP and NADPH for photosynthetic carbon fixation and all cellular need. Mitochondrial respiration is essential in plants, but this may be due to heterotrophic bottlenecks during plant development or because it is also necessary in photosynthetically active cells. In this study, we examined in vivo changes of cytosolic ATP concentration in response to light, employing a biosensing strategy in the moss Physcomitrium patens and revealing increased cytosolic ATP concentration caused by photosynthetic activity. Plants depleted of respiratory Complex I showed decreased cytosolic ATP accumulation, highlighting a critical role of mitochondrial respiration in light-dependent ATP supply of the cytosol. Consistently, targeting mitochondrial ATP production directly, through the construction of mutants deficient in mitochondrial ATPase (complex V), led to drastic growth reduction, despite only minor alterations in photosynthetic electron transport activity. Since P. patens is photoautotrophic throughout its development, we conclude that heterotrophic bottlenecks cannot account for the indispensable role of mitochondrial respiration in plants. Instead, our results support that mitochondrial respiration is essential for ATP provision to the cytosol in photosynthesizing cells. Mitochondrial respiration provides metabolic integration, ensuring supply of cytosolic ATP essential for supporting plant growth and development.
植物依赖太阳能来合成 ATP 和 NADPH，以进行光合作用碳固定和满足所有细胞的需求。线粒体呼吸对植物至关重要，但这可能是由于植物发育过程中的异养瓶颈，或者因为它在光合作用活跃的细胞中也是必需的。在这项研究中，我们通过在藓类植物Physcomitrium patens 中使用生物传感策略，研究了细胞溶胶中 ATP 浓度对光的响应的体内变化，揭示了光合作用活性引起的细胞溶胶中 ATP 浓度的增加。呼吸复合物 I 耗竭的植物表现出细胞溶胶中 ATP 积累减少，这突出了线粒体呼吸在光依赖的细胞溶胶 ATP 供应中的关键作用。一致地，通过构建缺乏线粒体 ATP 酶（复合物 V）的突变体直接靶向线粒体 ATP 产生，导致严重的生长减少，尽管光合作用电子传递活性只有微小的改变。由于 P. patens 在其整个发育过程中都是自养的，我们得出结论，异养瓶颈不能解释线粒体呼吸在植物中的不可或缺的作用。相反，我们的结果支持线粒体呼吸对于光合作用细胞中细胞溶胶中 ATP 的供应是必需的。线粒体呼吸提供代谢整合，确保供应对支持植物生长和发育至关重要的细胞溶胶 ATP。
