ABSCISIC ACID INSENSITIVE 4 coordinates eoplast formation to ensure acquisition of seed longevity during maturation in Medicago truncatula

SUMMARY Seed longevity, the capacity to remain alive during dry storage, is pivotal to germination performance and is essential for preserving genetic diversity. It is acquired during late maturation concomitantly with seed degreening and the de‐differentiation of chloroplasts into colorless, non‐photosynthetic plastids, called eoplasts. As chlorophyll retention leads to poor seed performance upon sowing, these processes are important for seed vigor. However, how these processes are regulated and connected to the acquisition of seed longevity remains poorly understood. Here, we show that such a role is at least provided by ABSCISIC ACID INSENSITIVE 4 (ABI4) in the legume Medicago truncatula. Mature seeds of Mtabi4 mutants contained more chlorophyll than wild‐type seeds and exhibited a 75% reduction in longevity and reduced dormancy. MtABI4 was necessary to stimulate eoplast formation, as evidenced by the significant delay in the dismantlement of photosystem II during the maturation of mutant seeds. Mtabi4 seeds also exhibited transcriptional deregulation of genes associated with retrograde signaling and transcriptional control of plastid‐encoded genes. Longevity was restored when Mtabi4 seeds developed in darkness, suggesting that the shutdown of photosynthesis during maturation, rather than chlorophyll degradation per se, is a requisite for the acquisition of longevity. Indeed, the shelf life of stay green mutant seeds that retained chlorophyll was not affected. Thus, ABI4 plays a role in coordinating the dismantlement of chloroplasts during seed development to avoid damage that compromises the acquisition of seed longevity. Analysis of Mtabi4 Mtabi5 double mutants showed synergistic effects on chlorophyll retention and longevity, suggesting that they act via parallel pathways. Significance Statement Seed degreening occurs at final maturation, and is a process that is crucial for seed performance and longevity. Here, we demonstrate the importance of ABI4 and ABI5 in coordinating the dismantlement of chloroplasts during development, to avoid damage that otherwise compromises seed longevity during maturation drying.