Deciphering plastid retrograde signals and their roles in plant development

Plastids are multifunctional plant organelles, acting as crucial environmental sensors and metabolic hubs that influence plant development and responses to environmental cues. This integration depends on bidirectional communication between plastids and the nucleus. While anterograde regulation is extensively characterized, biogenic retrograde signaling arising during plastid differentiation, remains incompletely understood. Traditionally focused on chloroplasts, studies have identified tetrapyrroles such as heme as key signals. However, recent findings support carotenoid-derived apocarotenoids, particularly those from acyclic cis-carotenes, as emerging retrograde signals. These signals function not only under stress but also during normal chloroplast developmental transitions, such as de-etiolation, and can act as either positive or negative regulators depending on the context. Evidence from grasses suggests that chloroplast differentiation proceeds through sequential, stage-specific signals serving as developmental checkpoints. Moreover, biogenic signaling tunes nuclear gene expression through transcription factors, chromatin remodeling and posttranslational regulation. This review synthesizes current knowledge on biogenic retrograde signaling, highlighting its role in plastid differentiation, development and adaptation. We emphasize the emerging roles of apocarotenoids, highly sensitive to metabolic and environmental conditions, as potential retrograde signals. We highlight that broader studies on different plastid types, novel metabolites and regulatory networks are essential to unravel the complexity of plastid-to-nucleus communication and its key roles in plant morphogenesis and adaptation to environmental changes.