Water content, adenylate kinase, and mitochondria drive adenylate balance in dehydrating and imbibing seeds

Raveneau, Marie-Paule; Benamar, Abdelilah; Macherel, David

doi:10.1093/jxb/erx182

Cited by 27 publications

(22 citation statements)

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“…2B). Those observations are in contrast to the previous postulate that a maturation phase is required for respiratory incompetent protomitochondria before respiration can commence (41), but in agreement with recent observations in pea and Arabidopsis seeds (42,43). Work in lettuce seed extracts has pinpointed the early establishment of adenylate charge, but the in vivo dynamics of the response could not be resolved (44).…”

Section: Discussionsupporting

confidence: 81%

Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

Nietzel

Mostertz

Ruberti

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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113

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Seeds preserve a far developed plant embryo in a quiescent state. Seed metabolism relies on stored resources and is reactivated to drive germination when the external conditions are favorable. Since the switchover from quiescence to reactivation provides a remarkable case of a cell physiological transition we investigated the earliest events in energy and redox metabolism ofArabidopsisseeds at imbibition. By developing fluorescent protein biosensing in intact seeds, we observed ATP accumulation and oxygen uptake within minutes, indicating rapid activation of mitochondrial respiration, which coincided with a sharp transition from an oxidizing to a more reducing thiol redox environment in the mitochondrial matrix. To identify individual operational protein thiol switches, we captured the fast release of metabolic quiescence in organello and devised quantitative iodoacetyl tandem mass tag (iodoTMT)-based thiol redox proteomics. The redox state across all Cys peptides was shifted toward reduction from 27.1% down to 13.0% oxidized thiol. A large number of Cys peptides (412) were redox switched, representing central pathways of mitochondrial energy metabolism, including the respiratory chain and each enzymatic step of the tricarboxylic acid (TCA) cycle. Active site Cys peptides of glutathione reductase 2, NADPH-thioredoxin reductase a/b, and thioredoxin-o1 showed the strongest responses. Germination of seeds lacking those redox proteins was associated with markedly enhanced respiration and deregulated TCA cycle dynamics suggesting decreased resource efficiency of energy metabolism. Germination in aged seeds was strongly impaired. We identify a global operation of thiol redox switches that is required for optimal usage of energy stores by the mitochondria to drive efficient germination.

show abstract

Section: Discussionsupporting

confidence: 81%

Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

Nietzel

Mostertz

Ruberti

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

113

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“…This, as well as our observation of fluorescently labeled mitochondria in embryo cells after 10 min of imbibition ( Fig. 2B), is in contrast to the previous postulate that a maturation phase is required for respiratory incompetent proto-mitochondria before respiration can commence (40), but in agreement with recent observations in pea and Arabidopsis seeds (41,42). Work in lettuce seed extracts has pinpointed the early establishment of adenylate charge, but the in vivo dynamics of the response could not be resolved (43).…”

Section: Discussionsupporting

confidence: 93%

Redox-mediated Kick-Start of Mitochondrial Energy Metabolism drives Resource-efficient Seed Germination

Nietzel

Mostertz

Ruberti

et al. 2019

Preprint

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Seeds preserve a far developed plant embryo in a quiescent state. Seed metabolism relies on stored resources and is re-activated to drive germination when the external conditions are favorable. Since the switchover from quiescence to re-activation provides a remarkable case of a cell physiological transition we investigated the earliest events in energy and redox metabolism of Arabidopsis seeds at imbibition. By developing fluorescent protein biosensing in intact seeds, we observed ATP accumulation and oxygen uptake within minutes, indicating rapid activation of mitochondrial respiration, which coincided with a sharp transition from an oxidizing to a more reducing thiol redox environment in the mitochondrial matrix. To identify individual operational protein thiol switches, we captured the fast release of metabolic quiescence in organello and devised quantitative iodoacetyl tandem mass tag-based (iodoTMT) thiol redox proteomics. The redox state across all Cys-peptides was shifted towards reduction from 27.1 % to 13.0 %. A large number of Cys-peptides (412) were redox-switched, representing central pathways of mitochondrial energy metabolism, including the respiratory chain and each enzymatic step of the tricarboxylic acid cycle (TCA). Active site Cys-peptides of glutathione reductase 2, NADPH-thioredoxin reductase a/b and thioredoxin-o1 showed the strongest responses. Germination of seeds lacking those redox proteins was associated with markedly enhanced respiration and deregulated TCA cycle dynamics suggesting decreased resource efficiency of energy metabolism. Germination in aged seeds was strongly impaired. We identify a global operation of thiol redox switches that is required for optimal usage of energy stores by the mitochondria to drive efficient germination.

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“…Together with late embryogenesis abundant proteins (LEA), sHSPs are generally expressed during late seed development and are thus expected to be involved in desiccation tolerance [57][58][59][60]. The protection of mitochondria in dry seeds appears to be of primordial importance because of their bioenergetic role, which has to resume very early during imbibition to fuel metabolism [61,62]. Besides HSP22, pea seed mitochondria were also found to accumulate in their matrix LEAM, a LEA protein shown to protect the inner membrane during desiccation [63,64].…”

Section: Introductionmentioning

confidence: 99%

The Mitochondrial Small Heat Shock Protein HSP22 from Pea is a Thermosoluble Chaperone Prone to Co-Precipitate with Unfolding Client Proteins

Avelange‐Macherel

Rolland

Hinault

et al. 2019

IJMS

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The small heat shock proteins (sHSPs) are molecular chaperones that share an alpha-crystallin domain but display a high diversity of sequence, expression, and localization. They are especially prominent in plants, populating most cellular compartments. In pea, mitochondrial HSP22 is induced by heat or oxidative stress in leaves but also strongly accumulates during seed development. The molecular function of HSP22 was addressed by studying the effect of temperature on its structural properties and chaperone effects using a recombinant or native protein. Overexpression of HSP22 significantly increased bacterial thermotolerance. The secondary structure of the recombinant protein was not affected by temperature in contrast with its quaternary structure. The purified protein formed large polydisperse oligomers that dissociated upon heating (42 • C) into smaller species (mainly monomers). The recombinant protein appeared thermosoluble but precipitated with thermosensitive proteins upon heat stress in assays either with single protein clients or within complex extracts. As shown by in vitro protection assays, HSP22 at high molar ratio could partly prevent the heat aggregation of rhodanese but not of malate dehydrogenase. HSP22 appears as a holdase that could possibly prevent the aggregation of some proteins while co-precipitating with others to facilitate their subsequent refolding by disaggregases or clearance by proteases.Int. J. Mol. Sci. 2020, 21, 97 2 of 23 range in size from 12 to 42 kDa and generally assemble into multimers of 12 to over 32 monomers [5]. All sHSPs share a 90-amino acids beta-sheet domain called alpha-crystallin domain (ACD), by reference to alphaA-and alphaB-crystallin of mammalian eye lens [6]. The ACD is followed by a non-conserved short C-terminal extension, which is involved in sHSP oligomerization [7]. A variable N-terminal region forms a disordered and flexible arm, which interacts with protein substrates [8]. There is mounting evidence that ACD, N-, and C-terminal regions contribute all together to sHSP structure and molecular chaperone activity [3,9]. sHSPs have been suggested to bind denatured proteins in an ATP-independent manner, limiting aggregation and allowing subsequent refolding in cooperation with other chaperones, such as HSP70 [1,10]. sHSPs were qualified as holdase chaperones by contrast to foldases that assist protein folding by ATP-dependent mechanisms [11]. Most sHSPs are strongly induced upon heat shock and more generally by abiotic stress [2,12,13].Although they are almost ubiquitous, sHSPs are especially prominent in plants [3] with, for instance, 19 sHSP genes identified in Arabidopsis thaliana [14] and 94 in cotton [15]. Based on their intracellular localization, sequence homology, and immunological cross-reactivity, 11 subfamilies of plant sHSPs were defined: six nuclear/cytoplasmic localized subfamilies (CI to CVI) and five organelle localized subfamilies (for review, see [16]. Several reports showed that sHSP overexpression could protect microorganisms, animals, and...

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Water content, adenylate kinase, and mitochondria drive adenylate balance in dehydrating and imbibing seeds

Abstract: AMP accumulation in dry seeds, which powers the rapid resumption of energy flow during imbibition, is driven by dehydration through the interplay between ATP demand, adenylate kinase, and oxidative phosphorylation.

Cited by 27 publications

References 62 publications

Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination

Redox-mediated Kick-Start of Mitochondrial Energy Metabolism drives Resource-efficient Seed Germination

The Mitochondrial Small Heat Shock Protein HSP22 from Pea is a Thermosoluble Chaperone Prone to Co-Precipitate with Unfolding Client Proteins

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