ROS Accumulation as a Hallmark of Dehydration Stress in Primed and Overprimed Medicago truncatula Seeds

Abstract

Seed priming protocols implement incomplete imbibition phases, as well as physical, chemical or biological treatments, to activate pre-germinative metabolism and stress response, thus improving germination performances, seedling establishment and stress tolerance according to agricultural productivity requirements. The dehydration phase following priming treatments represents a critical variable, since an excessively prolonged imbibition (overpriming) impairs desiccation tolerance, compromising seed viability and seedling establishment. Priming protocols generally optimize imbibition-dehydration timing empirically to avoid overpriming. Hence, a better understanding of the dynamics underlying the loss of desiccation tolerance represents a promising route to test and develop efficient and cost-effective priming techniques. In the present work, priming and overpriming conditions were defined to explore the role of desiccation tolerance in seed priming efficiency in the model legume Medicago truncatula. The positive effects of hydropriming and kinetin-mediated hormopriming on germination parameters were screened in combination with conditions of short/prolonged priming and mild/severe overpriming. Biometric analyses highlighted contrasting responses in terms of germination performances and seedling development, while ROS (reactive oxygen species) levels measured during dehydration positively correlate with the loss of desiccation tolerance in early seedlings, suggesting possible applications to monitor priming progression and predict overpriming occurrence.

Molecular dynamics of seed priming at the crossroads between basic and applied research

“…2 ) is used to represent the treatment (controlled seed imbibition followed by desiccation or dry-back) routinely applied in standard seed vigorization protocols. Such a concept represents an ideal biological context to explore some critical issues of the technique, related to loss and gain of desiccation tolerance (Fabrissin et al 2021 ; Farooq et al 2019 ; Paparella et al 2015 ; Pagano et al 2022a , 2022b ). Some of the main conventional seed priming techniques (hydropriming, solid matrix priming, osmopriming, chemopriming, hormopriming, thermopriming) are briefly described in this paragraph along with hybrid methodologies and the most recent applications based on nanomaterials.…”

“…3 ). The impact of different seed priming techniques has been evaluated in terms of antioxidant response in cereals (Hameed et al 2019 ; Cao et al 2019 ; Sen and Puthur 2020 ; Khan et al 2020a ; Shah et al 2021 ; Guo et al 2022 ), legumes (Kesharvarz et al 2017 ; Lilya et al 2019 ; Forti et al 2020b ; Chen et al 2021 ; Pagano et al 2022a , 2022b ), Solanaceae (Anand et al 2019 ; Ali et al 2019 ; Bali et al 2020 ; Forti et al 2020a , 2021 ), and tree species (Zhai et al 2022 ). The beneficial effects of seed priming can extend beyond germination and seedling development since these treatments contribute to enhancing the antioxidant defense in field-grown plants (Fig.…”

“…The most frequent oxidation product is 8-oxoguanine, removed by either the 8-oxoguanine DNA glycosylase/lyase (OGG1) or formamidopyrimidine-DNA glycosylase (FPG) (Córdoba-Cañero et al 2014 ). Upregulation of OGG1 and FPG genes has been reported in hydroprimed and bioprimed M. truncatula seeds (Forti et al 2020a , b ; Pagano et al 2022a ), and osmoprimed eggplant ( Solanum melongena L.) seeds (Kiran et al 2020 ). Seed priming triggers DSBs repair through non-homologous end joining (NHEJ) and homologous recombination (HR), as well as mismatch repair (MMR) pathways (Kiran et al 2020 ).…”

“…Seed priming triggers DSBs repair through non-homologous end joining (NHEJ) and homologous recombination (HR), as well as mismatch repair (MMR) pathways (Kiran et al 2020 ). Upregulation of SOG1 gene, encoding the master regulator of DDR in plants, was reported along dry-back in hydroprimed M. truncatula seeds, indicating active DNA damage-dependent signaling (Pagano et al 2022a ). Despite these pieces of evidence, the current knowledge about DNA repair and genome maintenance mechanisms activated by seed priming still needs to be deeply explored.…”

“…Along with seed imbibition, increased levels of 7,8-dihydro-8-oxoguanine (8-oxodG) can be detected (Macovei et al 2010 , 2011a , 2011b ; Balestrazzi et al 2011 ). Upregulation of several BER genes, e.g., OGG1 (8-oxoguanine DNA glycosylase), FPG1 (formamidopyrimidine-DNA glycosylase), and TDP1 (tyrosyl-DNA phosphodiesterase) associated with metabolic resumption has been reported in imbibed seeds of Medicago truncatula (Pagano et al 2017 , 2019 , 2022a ; Forti et al 2020b ), Arabidopsis (Chen et al 2012a ; Cordoba-Canero et al 2014 ), and eggplant (Forti et al 2020a ; Kiran et al 2020 ). To date, reports that investigate the use of the expression profiles of DNA repair genes, e.g., BER genes, as early indicators of the seed response to priming have highlighted both genotype- and seed lot-dependent variability (Forti et al 2020a , 2021 ).…”