Abscisic acid enhances non-photochemical quenching through SnRK2 and ABI3 in Physcomitrium patens.

Abstract

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.