Nicotinamide adenine dinucleotides are associated with distinct redox control of germination in Acer seeds with contrasting physiology

Abstract

Seed germination is a complex process enabling plant reproduction. Germination was found to be regulated at the proteome, metabolome and hormonal levels as well as via discrete post-translational modification of proteins including phosphorylation and carbonylation. Redox balance is also involved but less studied. Acer seeds displaying orthodox and recalcitrant characteristics were investigated to determine the levels of redox couples of nicotinamide adenine dinucleotide (NAD) phosphate (NADP) and integrated with the levels of ascorbate and glutathione. NAD and NADP concentrations were higher in Norway maple seeds and exceptionally high at the germinated stage, being the most contrasting parameter between germinating Acer seeds. In contrast, NAD(P)H/NAD(P)+ ratios were higher in sycamore seeds, thus exhibiting higher reducing power. Despite distinct concentrations of ascorbate and glutathione, both seed types attained in embryonic axes and cotyledons had similar ratios of reduced/oxidized forms of ascorbate and half-cell reduction potential of glutathione at the germinated stage. Both species accomplished germination displaying different strategies to modulate redox status. Sycamore produced higher amounts of ascorbate and maintained pyridine nucleotides in reduced forms. Interestingly, lower NAD(P) concentrations limited the regeneration of ascorbate and glutathione but dynamically drove metabolic reactions, particularly in this species, and contributed to faster germination. We suggest that NAD(P) is an important player in regulating redox status during germination in a distinct manner in Norway maple and sycamore seeds.

NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons

“…Recalcitrant seeds displayed higher concentrations of Asc than orthodox seeds [ 72 , 73 ]. The accumulation of Asc in recalcitrant Acer seeds is a compensation strategy applied to resist oxidative damage [ 25 ]. The progressive decline in the content of Asc detected in beech seeds ( Figure 1 a,b) was in line with previous results [ 65 ] and declining patterns of Asc reported in orthodox seeds [ 22 ].…”

“…Recently, thiol metabolism in developing beech seeds was found to affect their storage capacity [ 18 ], indicating that the redox regulatory network modifies the control of metabolic and developmental plant processes [ 19 ]. Controlled oxidation is a well-known mechanism of the regulation of plant growth and development [ 20 , 21 ], including seed development [ 22 ], dehydration [ 23 , 24 ], and germination [ 25 , 26 ]. Cellular redox homeostasis is needed during organ formation, comprising a synchronized sequence of events enabling cell cycle progression, cell proliferation, cell differentiation, and organ architecture formation to attain physiological maturity and function [ 14 , 27 ].…”

“…Redox balance is achieved differentially in developing orthodox and recalcitrant seeds [ 22 ], but little is known about this in intermediate seeds. Importantly, the NAD(P) content and redox status contribute to the desiccation tolerance of seeds [ 23 ], further affecting NAD(P)H-dependent reactions, including the ascorbate–glutathione cycle [ 24 , 25 ]. These data encouraged us to investigate whether NAD(P) modulates the ascorbate–glutathione cycle, especially when a method for the determination of redox forms of ascorbate, glutathione, and NAD(P) can be applied to the same sample [ 47 ].…”

Distinct redox state regulation in the seedling performance of Norway maple and sycamore

“…The combination of methods described by Hewitt and Dickes (Hewitt and Dickes 1961 ) and Queval and Noctor (Queval and Noctor 2007 ) that were successfully applied in Acer seeds (Alipour et al 2021 ) were used for the ascorbate determination. Total ascorbate (Asc = AsA + DHA) was measured by reducing the extract with 25 mM dithiothreitol at pH 4.7.…”

“…Plant growth and development are controlled by redox reactions; more precisely, reactive oxygen species (ROS) initiate redox signals for plant organ morphogenesis based on the transitions between the ascorbate (Asc), glutathione and nicotinamide adenine dinucleotide (NAD) phosphate (NADP) redox couples (Considine and Foyer 2014;Huang et al 2019). Norway maple (orthodox) and sycamore (recalcitrant) seeds, which are physiologically contrasted in terms of their desiccation tolerance, display contrasting NAD(P) contents and redox states during the seed development (Stolarska et al 2020), desiccation (Alipour et al 2020) and particularly at the germination stage, the two species exhibited different redox strategies, which was related to the accumulation of ascorbate in sycamore, and accumulation of glutathione and higher levels of pyridine in Norway maple nucleotides (Alipour et al 2021). Both NAD and NADP (NAD(P)) are important signaling molecules in plants and function in catabolic and anabolic reactions, respectively, thus orchestrating cellular redox homeostasis (Gakière et al 2018;Hunt et al 2004;Mahalingam et al 2007;Pétriacq et al 2013).…”