Maeng Chang-Hyun, Fujita Takuya, Kishimoto Junko, Tanaka Ryouichi, Takabayashi Atsushi, Fujita Tomomichi
Graduate School of Life Science, Hokkaido University, Sapporo, Japan.
Institute of Low Temperature Science, Hokkaido University, Sapporo, Japan.
J Plant Res. 2025 Apr 7. doi: 10.1007/s10265-025-01627-7.
The transition of plants in the green lineage from aquatic to terrestrial environments during the bryophyte stage marked a pivotal point in evolution. Successful terrestrialization required evolutionary adaptations to harsh and fluctuating light conditions, where direct irradiation is stronger than in aquatic environments. To cope with these challenges, plants evolved regulatory mechanisms to control cellular activities. One such acclimation is rapidly reversible, energy-dependent non-photochemical quenching (NPQ), which dissipates excess light energy as heat to protect the photosynthetic apparatus. Another critical innovation is abscisic acid (ABA) signaling, believed to have first emerged in bryophytes. Here, we reveal a potential link between these two key acclimations in bryophytes. We demonstrate that exogenous ABA induces NPQ in the moss Physcomitrium patens, increasing the levels of LHCSR, a key NPQ regulator, while concurrently decreasing PsbS. Exogenous ABA also enhances the xanthophyll cycle pigments, contributing to NPQ. In mutants deficient in ABA signaling components, including SNF1-related kinase 2 (SnRK2) and the transcription factor, Abscisic Acid-Insensitive 3 (ABI3), ABA-induced NPQ, LHCSR and PsbS expression, and xanthophyll cycle pigment accumulation were significantly reduced. These findings suggest that exogenous ABA enhances NPQ through the SnRK2 and ABI3-mediated signaling pathway by promoting LHCSR expression and xanthophyll cycle pigment production. We propose that the integration of ABA signaling and NPQ represent a critical evolutionary milestone, enabling early land plants to adapt and thrive in terrestrial environments.
在苔藓植物阶段,绿色谱系中的植物从水生环境向陆地环境的转变标志着进化中的一个关键点。成功的陆地化需要进化出适应恶劣且多变光照条件的能力,在陆地环境中,直接照射比水生环境更强。为应对这些挑战,植物进化出调控机制来控制细胞活动。其中一种适应方式是快速可逆的、依赖能量的非光化学猝灭(NPQ),它将多余的光能以热量形式耗散,以保护光合机构。另一项关键创新是脱落酸(ABA)信号传导,据信最早出现在苔藓植物中。在此,我们揭示了苔藓植物中这两种关键适应方式之间的潜在联系。我们证明,外源ABA在小立碗藓中诱导NPQ,增加关键NPQ调节因子LHCSR的水平,同时降低PsbS。外源ABA还增强了叶黄素循环色素,促进了NPQ。在缺乏ABA信号成分的突变体中,包括SNF1相关激酶2(SnRK2)和转录因子脱落酸不敏感3(ABI3),ABA诱导的NPQ、LHCSR和PsbS表达以及叶黄素循环色素积累显著减少。这些发现表明,外源ABA通过促进LHCSR表达和叶黄素循环色素产生,通过SnRK2和ABI3介导的信号通路增强NPQ。我们提出,ABA信号传导和NPQ的整合代表了一个关键的进化里程碑,使早期陆地植物能够在陆地环境中适应并茁壮成长。