Seeds are the reproductive units of higher plants. They have a significant place in agriculture and plant diversity maintenance. Because they are dehydrated, they can remain viable in the environment for centuries. The dry seed is a metabolically inactive organism, but well organized to protect its components and enter intensive repair to restore metabolic activities upon imbibition for the completion of germination.
If water is the matrix of life [5], dry seeds can hardly be considered as alive and yet they bear life in the form of the embryo. Water is an essential participant in the chemistry of life by sustaining the biochemistry of the cell. It acts as a liquid and solvent for biochemical reactions, but also influences macromolecule structures [6]. Water participates in the catalytic function of proteins and nucleic acids and physically in hydrophobic associated protein folding and complex formation through the hydrogen bond [7]. It was shown that in desiccated Arabidopsis seeds the chromatin is highly condensed and can be de-condensated after hydration [8]. The property of the seed to undergo a reversible chromatin condensation/de-condensation enables to withstand desiccation and the entry in active metabolism during imbibition.
Thus, high water binding forces in dry seeds are responsible for the lack of stability and activity of biomolecules causing low metabolism and energy. As membrane reorganization is one of the first events in the initiation of cell energization, more water (>24%) is needed to activate protein reorganization and activity for full plasma membrane and mitochondrial energy restoration (Figure 3).
After-ripening has fascinated researchers because dormancy is alleviated in dry conditions, suggesting that some processes operate in the dry seed. Biological reactions have been investigated and transcriptional programs have been proposed to be involved in the regulation of after-ripening-mediated seed dormancy alleviation in several seeds [34][35][36][37][38]. Given the restricted molecular mobility due to the glassy state in dry seed cells, the existence of a hydrated pocket within the cell enabling gene transcription has been hypothesized [34]. To address this issue, Meimoun et al. [3] investigated transcriptomic changes after the after-ripening period in sunflower seeds using two protocols, one allowing dormancy alleviation but not the other, in order to differentiate between changes in gene expression associated with dormancy alleviation and those associated with storage only. They showed that there is no significant variation between conditions, suggesting that gene expression did not take place during after-ripening, in agreement with the absence of metabolic activity in dry seeds [3].
Non-enzymatic oxidations are possible in low hydrated seeds and represent the most plausible lead to explain the observed molecular changes reported during after-ripening [39]. Indeed, mRNA oxidation was shown to be associated with dormancy release during after-ripening in sunflower and wheat [40][41], which alters the stability of stored mRNAs, being finally degraded or translated into non-functional proteins [42]. However, if a fraction of stored mRNA is inactivated, the one involved in germination has to be protected from oxidation.
Environmental factors are of high importance in the awakening of the seed. Their effect on seed performance was shown to surpass genetic impact [47]. Temperature and soil moisture oscillations are the major players under natural conditions. Indeed, alternating temperatures more than constant ones can promote germination via the interplay between ROS signaling and hormones [48]. On the other hand, light and nitrate also play important roles. Their effects are associated in dormancy cycling [49][50][51]. Seed sensitivity to both of them depends on the season and depth of dormancy. A low concentration of nitrate (around 0.1 mM) is able to promote seed germination in several species [49]. Several evidences converge towards nitrate induction of CYP707A2 leading to ABA decrease more than GA biosynthesis in dormancy breakdown [49]. However, GA biosynthesis gene involvement has also been reported in response to environmental cues in Arabidopsis seeds from lab but also soil seed bank experiences [52][53]. Moreover, the analysis of the whole transcriptome change by nitrate treatment during seed imbibition showed the upregulation of genes involved in nitrate assimilation and transport, hormone metabolism, and energy, such as Glucose-6-phosphate dehydrogenase2, highlighting the importance of the pentose phosphate pathway [54]. In fact, dormancy is tightly regulated in natural conditions as in the soil, when seeds experience several scenarios of temperature, light, nitrate, and moisture, as well as microbial environment. The latter corresponds to a wide range of microbes, as pathogenic ones can induce decrease in seed longevity due to infection, and others can influence seed dormancy by breaking down the seed coat [55][56].
Seed ageing was defined as the loss of seed quality and viability over time [57]. Aged seeds germinate poorly giving abnormal seedlings or ultimately are unable to germinate. Orthodox seeds are resistant to ageing for very long time because they have a very low water content, resulting in reduced cell metabolism especially respiration which is responsible for the major production of ROS [58]. Indeed, as for the dry after-ripening process described above, enzymatic reactions and respiration are restricted by the lack of free available water preventing cellular damage. It was shown that long term storage resulting in seed loss of viability is associated with the impairment of mitochondrial activity and protein synthesis machinery [59][60]. Mitochondrion membrane integrity was identified as the primary target for ageing leading to the deregulation of its oxidative properties [61]. ROS are considered as the major cause of seed deterioration due to the oxidation of its components [62].
Seeds possess effective repair machinery to cope with ageing-associated oxidative damage. Several non-enzymatic antioxidants have been proposed to be determinant in seed longevity, e.g., glutathione or ascorbic acid [63][64]. The antioxidant enzymes are also of importance in ROS detoxification, such as catalase, superoxide dismutase, ascorbate peroxidase, or glutathione reductase [65][66]. Other enzymes acting on specific macromolecules are also activated, such as DNA or protein repair enzymes [67][68][69]. Such machinery operates when seed hydration occurred, and its efficiency depends on the plant species and the extent of ageing damage. Based on this feature, a priming technique has been developed to improve seed quality from alterations caused by several stresses. Priming treatment consists of seed pre-hydration with a controlled amount of water which does not allow radicle elongation, i.e., a water amount corresponding phase II of the germination sensu stricto, which is sufficient to trigger the reparation processes. The addition of beneficial molecules, such as antioxidants or hormones, during priming treatment can further increase seed reparation and subsequent quality. Several priming techniques have been developed depending on the plant species and subsequent use. They all lead to an improvement of seed performance under variable environmental conditions [70]. It was shown that repair mechanisms and oxidative management in primed seeds represent the main processes associated with priming induced germination improvement, but DNA replication, cell cycle advancement, the modification of the membrane structure, and restoration of mitochondrial integrity were also proposed to explain the priming effect in germination improvement [71]. In fact, the seed engages growth preparation processes during imbibition while maintaining the desiccation tolerance machinery which allowed a successful dehydration after the priming treatment. The dried primed seed is ready to grow better, even under stress conditions.
Understanding the successful entry and exit from desiccation is fundamental for the improvement of seed germination in the coming challenging conditions due to global warming. The application in plant germplasm conservation in seed banks is of high importance in the maintenance of genetic resources for food and environment security. In this review, several layers of regulations of seed performance were shown, from the organization and physical protection of cell components to the regulation of several signaling processes in a coordinated crosstalk. However, their implementation and coordination of these mechanisms during seed development deserve more investigations.