Environmental Sciences Division and Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.
Department of Plant Agriculture, University of Guelph, Guelph, ON, N1G 2W1, Canada.
New Phytol. 2022 Oct;236(2):319-329. doi: 10.1111/nph.18371. Epub 2022 Aug 3.
In higher plants, photosystems II and I are found in grana stacks and unstacked stroma lamellae, respectively. To connect them, electron carriers negotiate tortuous multi-media paths and are subject to macromolecular blocking. Why does evolution select an apparently unnecessary, inefficient bipartition? Here we systematically explain this perplexing phenomenon. We propose that grana stacks, acting like bellows in accordions, increase the degree of ultrastructural control on photosynthesis through thylakoid swelling/shrinking induced by osmotic water fluxes. This control coordinates with variations in stomatal conductance and the turgor of guard cells, which act like an accordion's air button. Thylakoid ultrastructural dynamics regulate macromolecular blocking/collision probability, direct diffusional pathlengths, division of function of Cytochrome b f complex between linear and cyclic electron transport, luminal pH via osmotic water fluxes, and the separation of pH dynamics between granal and lamellar lumens in response to environmental variations. With the two functionally asymmetrical photosystems located distantly from each other, the ultrastructural control, nonphotochemical quenching, and carbon-reaction feedbacks maximally cooperate to balance electron transport with gas exchange, provide homeostasis in fluctuating light environments, and protect photosystems in drought. Grana stacks represent a dry/high irradiance adaptation of photosynthetic machinery to improve fitness in challenging land environments. Our theory unifies many well-known but seemingly unconnected phenomena of thylakoid structure and function in higher plants.
在高等植物中，光系统 II 和光系统 I 分别位于类囊体垛叠和非垛叠的基质片层中。为了连接它们，电子载体需要通过曲折的多介质路径，并受到大分子的阻碍。为什么进化会选择一种明显不必要、低效的二分法呢？在这里，我们系统地解释了这一令人费解的现象。我们提出，类囊体垛叠就像手风琴的风箱一样，通过渗透水通量引起的类囊体肿胀/收缩，增加光合作用的超微结构控制程度。这种控制与气孔导度和保卫细胞膨压的变化相协调，保卫细胞就像手风琴的风箱按钮一样。类囊体超微结构动力学调节大分子的阻碍/碰撞概率、扩散路径长度、细胞色素 b f 复合物在线性和环式电子传递之间的功能划分、通过渗透水通量调节腔室 pH 值以及响应环境变化时在粒状和层状腔室之间分离 pH 值动力学。由于两个功能上不对称的光系统彼此远离，超微结构控制、非光化学猝灭和碳反应反馈最大程度地合作，以平衡电子传递与气体交换，在波动的光照环境中提供内稳态，并在干旱条件下保护光系统。类囊体垛叠代表了光合机构对干燥/高光强的适应，以提高在挑战性陆地环境中的适应性。我们的理论统一了高等植物中许多众所周知但看似不相关的类囊体结构和功能现象。
