Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection

Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection
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DOI:
10.1038/s41477-021-00947-5
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发表时间:
2021-06-17
期刊:
影响因子:
18
通讯作者:
Kirchhoff, Helmut
Kirchhoff, Helmut
中科院分区:
生物学1区
文献类型:
--
作者:
Li, Meng;Svoboda, Vaclav;Kirchhoff, Helmut

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类囊体膜必须维持由光驱动的光合作用产生的电位和pH电位的平衡。光保护机制和电子传递通过K+和Cl-通道介导的pH振荡进行微调。在光合类囊体膜中,质子动力(pmf)不仅驱动ATP的合成,而且是控制和调节能量转换的中心。因此,动态微调的两个pmf组件,电气(Δ psi)和化学(Δ pH值),是一个必要的元素,调整光合光反应,不断变化的环境条件。有充分的证据表明,Δ psi/Δ pH分配是由类囊体钾和氯离子转运蛋白和通道控制的。然而,这些类囊体离子转运蛋白/通道如何控制pmf分配的详细机制还缺乏了解。在这里,我们结合钾和氯离子转运蛋白和通道功能丧失突变体的功能测量与扩展的数学模拟类囊体膜中的光合光反应,以获得详细的动力学见解膜的光通量和离子通量之间的复杂的相互关系跨类囊体膜。这些数据表明,钾和氯离子通量在类囊体腔确定的K+/H+反向转运蛋白KEA 3和电压门控氯离子通道VCCN 1/Best 1有不同的动力学反应,导致特征和光强度依赖性Δ psi/Δ pH振荡。这些振荡微调光保护机制和电子传输,这是特别重要的第一分钟的照明和波动的光条件下。通过采用该模型的预测能力,我们揭示了KEA 3和VCCN 1丰度和调节/酶促参数对膜粘附和光保护的变化的功能后果。
Thylakoid membranes must maintain a balance of their electrical and pH potentials, created by light-driven photosynthesis. Photoprotective mechanisms and electron transport are fine-tuned through pH oscillations mediated by K+ and Cl- channels.In photosynthetic thylakoid membranes the proton motive force (pmf) not only drives ATP synthesis, in addition it is central to controlling and regulating energy conversion. As a consequence, dynamic fine-tuning of the two pmf components, electrical (Delta psi) and chemical (Delta pH), is an essential element for adjusting photosynthetic light reactions to changing environmental conditions. Good evidence exists that the Delta psi/Delta pH partitioning is controlled by thylakoid potassium and chloride ion transporters and channels. However, a detailed mechanistic understanding of how these thylakoid ion transporter/channels control pmf partitioning is lacking. Here, we combined functional measurements on potassium and chloride ion transporter and channel loss-of-function mutants with extended mathematical simulations of photosynthetic light reactions in thylakoid membranes to obtain detailed kinetic insights into the complex interrelationship between membrane energization and ion fluxes across thylakoid membranes. The data reveal that potassium and chloride fluxes in the thylakoid lumen determined by the K+/H+ antiporter KEA3 and the voltage-gated Cl- channel VCCN1/Best1 have distinct kinetic responses that lead to characteristic and light-intensity-dependent Delta psi/Delta pH oscillations. These oscillations fine-tune photoprotective mechanisms and electron transport which are particularly important during the first minutes of illumination and under fluctuating light conditions. By employing the predictive power of the model, we unravelled the functional consequences of changes in KEA3 and VCCN1 abundance and regulatory/enzymatic parameters on membrane energization and photoprotection.