Optimizing the photoprotection of different leaves as a whole is important for plants to adapt to fluctuations in ambient light conditions. However, the molecular basis of this leaf-to-leaf communication is poorly understood. Here, we used a range of techniques, including grafting, chlorophyll fluorescence, revers transcription quantitative PCR, immunoblotting, chromatin immunoprecipitation, and electrophoretic mobility shift assays, to explore the complexities of leaf-to-leaf light signal transmission and activation of the photoprotective response to light fluctuation in tomato (Solanum lycopersicum). We established that light perception in the top leaves attenuated the photoinhibition of both PSII and PSI by triggering photoprotection pathways in the bottom leaves. Local light promoted the accumulation and movement of LONG HYPOCOTYL5 from the sunlit local leaves to the systemic leaves, priming the photoprotective response of the latter to light fluctuation. By directly activating the transcription of PROTON GRADIENT REGULATION5 and VIOLAXANTHIN DE-EPOXIDASE, LONG HYPOCOTYL5 induced cyclic electron flow, the xanthophyll cycle, and energy-dependent quenching. Our findings reveal a systemic signaling pathway and provide insight into an elaborate regulatory network, demonstrating a pre-emptive advantage in terms of the activation of photoprotection and, hence, the ability to survive in a fluctuating light environment.

优化不同叶子的整体光保护对于植物适应环境光照条件的波动非常重要。然而，人们对这种叶与叶通讯的分子基础知之甚少。在这里，我们使用了一系列技术，包括嫁接、叶绿素荧光、反转录定量PCR、免疫印迹、染色质免疫沉淀和电泳迁移率变化测定，来探索叶间光信号传递和光保护反应激活的复杂性对番茄（Solanum lycopersicum）的轻微波动。我们确定顶部叶子的光感知通过触发底部叶子的光保护途径来减弱 PSII 和 PSI 的光抑制。局部光促进LONG HYPOCOTYL5从阳光照射的局部叶向全身叶的积累和移动，引发后者对光波动的光保护反应。通过直接激活质子梯度调节 5和紫黄素脱环氧化酶的转录，长下胚轴 5 诱导循环电子流、叶黄素循环和能量依赖性猝灭。我们的研究结果揭示了系统性信号通路，并提供了对复杂调控网络的深入了解，证明了在光保护激活方面的先发优势，以及因此在波动的光环境中生存的能力。