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

European beech is an important component of European lowland forests in terms of ecology, and produces irregular seeds categorized as intermediate due to their limited longevity. Removal of the excess of reactive oxygen species is crucial for redox homeostasis in growing plant tissues. Hydrogen pero...

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Main Authors: Ewa Marzena Kalemba, Shirin Alipour, Natalia Wojciechowska
Format: Article
Language:English
Published: MDPI AG 2021-12-01
Series:Antioxidants
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Online Access:https://www.mdpi.com/2076-3921/10/12/2021
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author Ewa Marzena Kalemba
Shirin Alipour
Natalia Wojciechowska
author_facet Ewa Marzena Kalemba
Shirin Alipour
Natalia Wojciechowska
author_sort Ewa Marzena Kalemba
collection DOAJ
description European beech is an important component of European lowland forests in terms of ecology, and produces irregular seeds categorized as intermediate due to their limited longevity. Removal of the excess of reactive oxygen species is crucial for redox homeostasis in growing plant tissues. Hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) is detoxified via the plant-specific ascorbate-glutathione cycle, and enzymatically, mainly by catalase (CAT). The reduced and oxidized (redox) forms of ascorbate (AsA, DHA) and glutathione (GSH, GSSG) decreased during maturation as the content of redox forms of nicotinamide adenine dinucleotide (NADH, NAD<sup>+</sup>) phosphate (NADPH, NADP<sup>+</sup>), cofactors of ascorbate–glutathione enzymes, declined and limited this cycle. The degree of oxidation of glutathione peaked at approximately 80%, at the exact time when the NADP content was the lowest and the NADPH/NADP<sup>+</sup> ratio reached the highest values. The glutathione pool was reflected in changes in the NADP pool, both in embryonic axes (R<sup>2</sup> = 0.61) and in cotyledons (R<sup>2</sup> = 0.98). A large excess of NADPH was reported in embryonic axes, whereas cotyledons displayed more unified levels of NADP redox forms. As a result, anabolic redox charge and reducing power were higher in embryonic axes. CAT was recognized as two proteins, and the abundance of the 55 kDa protein was correlated with all redox forms of ascorbate, glutathione, NAD, and NADP, whereas the 37 kDa protein was oppositely regulated in embryonic axes and cotyledons. Here, we discuss the role of NAD(P) in the regulation of the ascorbate–glutathione cycle, catalase, and seed longevity concerning a putative role of NAD(P)H as a redox biomarker involved in predefining seed quality, because NAD(P)H-derived redox homeostasis was found to be better controlled in embryonic axes than cotyledons.
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spelling doaj.art-39a98eacfe67489195fd0778750602802023-11-23T03:34:28ZengMDPI AGAntioxidants2076-39212021-12-011012202110.3390/antiox10122021NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and CotyledonsEwa Marzena Kalemba0Shirin Alipour1Natalia Wojciechowska2Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, PolandInstitute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, PolandInstitute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, PolandEuropean beech is an important component of European lowland forests in terms of ecology, and produces irregular seeds categorized as intermediate due to their limited longevity. Removal of the excess of reactive oxygen species is crucial for redox homeostasis in growing plant tissues. Hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) is detoxified via the plant-specific ascorbate-glutathione cycle, and enzymatically, mainly by catalase (CAT). The reduced and oxidized (redox) forms of ascorbate (AsA, DHA) and glutathione (GSH, GSSG) decreased during maturation as the content of redox forms of nicotinamide adenine dinucleotide (NADH, NAD<sup>+</sup>) phosphate (NADPH, NADP<sup>+</sup>), cofactors of ascorbate–glutathione enzymes, declined and limited this cycle. The degree of oxidation of glutathione peaked at approximately 80%, at the exact time when the NADP content was the lowest and the NADPH/NADP<sup>+</sup> ratio reached the highest values. The glutathione pool was reflected in changes in the NADP pool, both in embryonic axes (R<sup>2</sup> = 0.61) and in cotyledons (R<sup>2</sup> = 0.98). A large excess of NADPH was reported in embryonic axes, whereas cotyledons displayed more unified levels of NADP redox forms. As a result, anabolic redox charge and reducing power were higher in embryonic axes. CAT was recognized as two proteins, and the abundance of the 55 kDa protein was correlated with all redox forms of ascorbate, glutathione, NAD, and NADP, whereas the 37 kDa protein was oppositely regulated in embryonic axes and cotyledons. Here, we discuss the role of NAD(P) in the regulation of the ascorbate–glutathione cycle, catalase, and seed longevity concerning a putative role of NAD(P)H as a redox biomarker involved in predefining seed quality, because NAD(P)H-derived redox homeostasis was found to be better controlled in embryonic axes than cotyledons.https://www.mdpi.com/2076-3921/10/12/2021antioxidantscatalase<i>Fagus sylvatica</i>pyridine nucleotidesredox statusseed maturation
spellingShingle Ewa Marzena Kalemba
Shirin Alipour
Natalia Wojciechowska
NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
Antioxidants
antioxidants
catalase
<i>Fagus sylvatica</i>
pyridine nucleotides
redox status
seed maturation
title NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
title_full NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
title_fullStr NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
title_full_unstemmed NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
title_short NAD(P)H Drives the Ascorbate–Glutathione Cycle and Abundance of Catalase in Developing Beech Seeds Differently in Embryonic Axes and Cotyledons
title_sort nad p h drives the ascorbate glutathione cycle and abundance of catalase in developing beech seeds differently in embryonic axes and cotyledons
topic antioxidants
catalase
<i>Fagus sylvatica</i>
pyridine nucleotides
redox status
seed maturation
url https://www.mdpi.com/2076-3921/10/12/2021
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AT nataliawojciechowska nadphdrivestheascorbateglutathionecycleandabundanceofcatalaseindevelopingbeechseedsdifferentlyinembryonicaxesandcotyledons