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

Abstract

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.

Seed Longevity and Ageing: A Review on Physiological and Genetic Factors with an Emphasis on Hormonal Regulation

“…A role for ABI4 in longevity of M. truncatula and Solanum lycopersicum (tomato) seeds had previously been hinted at by gene co-expression analyses [ 116 , 148 ]. Indeed, Arabidopsis and M. truncatula abi4 mutants have reduced longevity compared to wild-type when stored at intermediate ageing conditions, and also showed elevated chlorophyll levels and reduced dormancy [ 170 ].…”

“…Abi5 mutant seeds of pea and M. truncatula retained some chlorophyll and exhibited decreased longevity [ 171 ]. Moreover, the analysis of Mtabi5 Mtabi4 double mutants showed synergistic effects on chlorophyll retention and longevity, suggesting that they act via parallel pathways [ 170 ]. Consequently, ABI4 is hypothesized to coordinate the dismantling of chloroplasts during seed maturation and the subsequent attainment of seed longevity, acting in synergy with ABI5.…”

Involvement of Abscisic Acid in Transition of Pea (Pisum sativum L.) Seeds from Germination to Post-Germination Stages

“…As result, ABI3 , ABI4 , and ABI5 were expressed in the embryonic axis before radicle protrusion but downregulated at the post-germination stage. Given that ABI3 , ABI4 , and ABI5 are central transcriptional factors in seed-specific events, including maturation, dormancy, longevity, germination, and post-germination growth [ 16 , 40 , 41 ], we propose that PsABI3 , PsABI4 , and PsABI5 also play a role in regulating the P. sativum seed-to-seedling transition [ 4 , 9 ].…”

BASIC PENTACYSTEINE1 regulates ABI4 by modification of two histone marks H3K27me3 and H3ac during early seed development of Medicago truncatula

“…However, ABI4 is involved in a wider range of processes including flowering control, root development, plant defense, antagonism between abscisic acid and gibberellins or lipid mobilization during seedling establishment ( Penfield et al., 2006 ; Cantoro et al., 2013 ; León et al., 2013 ; Shu et al., 2016 ; Barczak-Brzyżek et al., 2017 ; Shu et al., 2018 ; Zhu et al., 2020 ). Recently, we identified a role for ABI4 in the regulation of dormancy and longevity, in part via the coordinated dismantlement of chloroplasts during seed development, to avoid damage and interference with the acquisition of seed vigor traits ( Zinsmeister et al., 2023 ).…”