NAD(P)-Driven Redox Status Contributes to Desiccation Tolerance in Acer seeds

Abstract

Desiccation tolerance is a developmental program enabling seed survival in a dry state and is common in seeds categorized as orthodox. We focused on NAD and its phosphorylated form (NADP) because their continual switching between reduced (NAD(P)H) and oxidized (NAD(P)+) forms is involved in the modulation of redox signaling and the determination of the reducing power and further antioxidant responses. Norway maple and sycamore seeds representing the orthodox and recalcitrant categories, respectively, were used as models in a comparison of responses to water loss. The process of desiccation up to 10% water content (WC) was monitored in Norway maple seeds, while dehydration up to 30% WC was monitored in desiccation-sensitive sycamore seeds. Norway maple and sycamore seeds, particularly their embryonic axes, exhibited a distinct redox status during dehydration and desiccation. High NADPH levels, NAD+ accumulation, low and stable NAD(P)H/NAD(P)+ ratios expressed as reducing power and high NADPH-dependent enzyme activity were reported in Norway maple seeds and were considered attributes of orthodox-type seeds. The contrasting results of sycamore seeds contributed to their low antioxidant capacity and high sensitivity to desiccation. NADPH deficiency, low NADPH-dependent enzyme activity and lack of NAD+ accumulation were primary features of sycamore seeds, with implications for their NAD(P)H/NAD(P)+ ratios and reducing power and with effects on many seed traits. Thus, we propose that the distinct levels of pyridine nucleotides and their redox status contribute to orthodox and recalcitrant phenotype differentiation in seeds by affecting cellular redox signaling, metabolism and the antioxidant system.

Peptide-Bound Methionine Sulfoxide (MetO) Levels and MsrB2 Abundance Are Differentially Regulated during the Desiccation Phase in Contrasted Acer Seeds

“…Consistently, an increased MetO level was thus noticed in the Arabidopsis catalase 2 mutant [31]. MetO levels, when compared to NAD(P) concentrations and their redox status, assumed as involved in desiccation tolerance in Acer seeds [51], displayed important correlations with Norway maple seeds (Table S1), underlining that MetO levels, similarly to pyridine nucleotides [51], are involved in desiccation tolerance.…”

“…MetO levels (Figure 2), when compared to NAD(P) concentrations and their redox status reported in Norway maple and sycamore seeds at identical dehydration and desiccation stages [51], were negatively correlated with NAD(P)H/NAD(P) ratios only in Norway maple seeds (Table S1). MetO levels were also correlated with NAD(P)H levels only in Norway maple seeds (Table S1), underlining that MetO levels, similarly to pyridine nucleotides [51], are involved in desiccation tolerance. Besides, MetO levels were correlated with the activity of NADH − or NADPH-dependent reductases solely in Norway maple seeds (Table S1)…”

“…The abundance of MsrB2 was correlated with changes in dehydration, ROS levels and the AsA/DHA ratio. Results presented in this report were also compared to NAD(P) concentrations and their redox status reported in Norway maple and sycamore seeds at identical dehydration and desiccation stages [51] and are shown in Table S1. MetO levels (Figure 2), when compared to NAD(P) concentrations and their redox status reported in Norway maple and sycamore seeds at identical dehydration and desiccation stages [51], were negatively correlated with NAD(P)H/NAD(P) ratios only in Norway maple seeds (Table S1).…”

“…Results presented in this report were also compared to NAD(P) concentrations and their redox status reported in Norway maple and sycamore seeds at identical dehydration and desiccation stages [51] and are shown in Table S1. MetO levels (Figure 2), when compared to NAD(P) concentrations and their redox status reported in Norway maple and sycamore seeds at identical dehydration and desiccation stages [51], were negatively correlated with NAD(P)H/NAD(P) ratios only in Norway maple seeds (Table S1). MetO levels were also correlated with NAD(P)H levels only in Norway maple seeds (Table S1), underlining that MetO levels, similarly to pyridine nucleotides [51], are involved in desiccation tolerance.…”

“…Two Acer species, Norway maple (Acer platanoides L.) and sycamore (Acer pseudoplatanus L.), that grow under similar conditions in the temperate zone produce orthodox pollen [43] but also orthodox and recalcitrant seeds, respectively [44,45], and the seeds of both species are characterized as undergoing deep physiological dormancy [46]. These two species are, therefore, excellent models for studying the differences enabling the production of seeds with contrasting physiology during development [41,42,47], dormancy [38,48], and drying and desiccation [44,47,[49][50][51]. In this work, we focused on the response to the gradual drying in these two opposite seed types: orthodox (Norway maple) and recalcitrant (sycamore).…”