Sprent Noah, Cheung C Y Maurice, Shameer Sanu, Ratcliffe R George, Sweetlove Lee J, Töpfer Nadine
Department of Chemical Engineering, Imperial College London, South Kensington Campus, Exhibition Road, London SW7 2AZ, UK.
Institute for Plant Sciences, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany.
Plant Cell. 2024 Dec 23;37(1). doi: 10.1093/plcell/koae252.
Guard cell metabolism is crucial for stomatal dynamics, but a full understanding of its role is hampered by experimental limitations and the flexible nature of the metabolic network. To tackle this challenge, we constructed a time-resolved stoichiometric model of guard cell metabolism that accounts for energy and osmolyte requirements and which is integrated with the mesophyll. The model resolved distinct roles for starch, sugars, and malate in guard cell metabolism and revealed several unexpected flux patterns in central metabolism. During blue light-mediated stomatal opening, starch breakdown was the most efficient way to generate osmolytes with downregulation of glycolysis allowing starch-derived glucose to accumulate as a cytosolic osmolyte. Maltose could also accumulate as a cytosolic osmoticum, although this made the metabolic system marginally less efficient. The metabolic energy for stomatal opening was predicted to be derived independently of starch, using nocturnally accumulated citrate which was metabolized in the tricarboxylic acid cycle to malate to provide mitochondrial reducing power for ATP synthesis. In white light-mediated stomatal opening, malate transferred reducing equivalents from guard cell photosynthesis to mitochondria for ATP production. Depending on the capacity for guard cell photosynthesis, glycolysis showed little flux during the day but was crucial for energy metabolism at night. In summary, our analyses have corroborated recent findings in Arabidopsis guard cell research, resolved conflicting observations by highlighting the flexibility of guard cell metabolism, and proposed new metabolic flux modes for further experimental testing.
保卫细胞代谢对于气孔动态至关重要，但由于实验限制和代谢网络的灵活性，对其作用的全面理解受到阻碍。为应对这一挑战，我们构建了一个时间分辨的保卫细胞代谢化学计量模型，该模型考虑了能量和渗透溶质需求，并与叶肉整合。该模型解析了淀粉、糖和苹果酸在保卫细胞代谢中的不同作用，并揭示了中心代谢中几种意想不到的通量模式。在蓝光介导的气孔开放过程中，淀粉分解是产生渗透溶质的最有效方式，糖酵解下调使淀粉衍生的葡萄糖作为细胞质渗透溶质积累。麦芽糖也可以作为细胞质渗透剂积累，尽管这会使代谢系统的效率略有降低。气孔开放的代谢能量预计独立于淀粉产生，利用夜间积累的柠檬酸，柠檬酸在三羧酸循环中代谢为苹果酸，为ATP合成提供线粒体还原力。在白光介导的气孔开放过程中，苹果酸将保卫细胞光合作用的还原当量转移到线粒体中用于ATP生成。根据保卫细胞光合作用的能力，糖酵解在白天通量很小，但对夜间能量代谢至关重要。总之，我们的分析证实了拟南芥保卫细胞研究中的最新发现，通过强调保卫细胞代谢的灵活性解决了相互矛盾的观察结果，并提出了新的代谢通量模式以供进一步实验测试。
