Cited by 135Seed Germination and PhysiologyMitochondrial Function and PathologyAutophagy in Disease and Therapy

Arabidopsis seed mitochondria are bioenergetically active immediately upon imbibition and specialize via biogenesis in preparation for autotrophic growth.

Open access
Paszkiewicz, Gaël, Gualberto, José M., Benamar, Abdelilah, Macherel, David, Logan, David C.·2017·The Plant Cell

Abstract

Seed germination is a vital developmental transition for production of progeny by sexual reproduction in spermatophytes. Quiescent cells in nondormant dry embryos are reawakened first by imbibition and then by perception of germination triggers. Reanimated tissues enter into a germination program requiring energy for expansion growth. However, germination requires that embryonic tissues develop to support the more energy-demanding processes of cell division and organogenesis of the new seedling. Reactivation of mitochondria to supply the required energy is thus a key process underpinning germination and seedling survival. Using live imaging, we investigated reactivation of mitochondrial bioenergetics and dynamics using Arabidopsis thaliana as a model. Bioenergetic reactivation, visualized by presence of a membrane potential, is immediate upon rehydration. However, reactivation of mitochondrial dynamics only occurs after transfer to germination conditions. Reactivation of mitochondrial bioenergetics is followed by dramatic reorganization of the chondriome (all mitochondrial in a cell, collectively) involving massive fusion and membrane biogenesis to form a perinuclear tubuloreticular structure enabling mixing of previously discrete mitochondrial DNA nucleoids. The end of germination coincides with fragmentation of the chondriome, doubling of mitochondrial number, and heterogeneous redistribution of nucleoids among the mitochondria, generating a population of mitochondria tailored to seedling growth.

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  • The imbibition period is crucial for seed germination, allowing activation of cellular metabolism including mobilization of food reserves and activation of mitochondria and protein synthesis.

    “Since it provides the required water to hydrate the cellular constituents, the imbibition period is crucial for seed germination, allowing the activation of cellular metabolism which includes the mobilization of food reserves and the activation of mitochondria and protein synthesis (Galland et al., 2014; Paszkiewicz et al., 2017).”

    From Exploring the Applicability of Calorespirometry to Assess Seed Metabolic Stability Upon Temperature Stress Conditions—Pisum sativum L. Used as a Case Study (2022) · cites this paper as Paszkiewicz et al., 2017

    The section “Seed Embryo Mitochondria Are Metabolically Reactivated within Minutes of Hydration” reports that mitochondria rapidly regain metabolic activity upon imbibition. The paper mentions a storage-lipid mobilization program and later insertion of new polypeptides, but the passages do not establish that imbibition activates food-reserve mobilization and protein synthesis as the sentence claims. (LLM, conf=0.83)

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Research works printed but not linked: 6

  1. Arimura, S., Yamamoto, J., Aida, G.P., Nakazono, M., and Tsutsumi, N. (2004). Frequent fusion and fission of plant mito- chondria with unequal nucleoid distribution. Proc. Natl. Acad. Sci. USA 101: 7805-7808.
  2. Baskin, C.C., and Baskin, J.M. (2014). Seeds: Ecology, Bio- geography, and Evolution of Dormancy and Germination. (Cam- bridge, MA: Academic Press).
  3. Dickinson, H.G., and Li, F.L. (1988). Organelle behaviour during ga- metogenesis. In Division and Segregation of Organelles, and S.A. Boffey and D. Lloyd, eds (Cambridge,UK: Cambridge University Press), pp. 131-148.
  4. Lonsdale, D.M., Brears, T., Hodge, T.P., Melville, S.E., and Rottmann, W.H. (1988). The plant mitochondrial genome: Homol- ogous recombination as a mechanism for generating heterogeneity. Philos. Trans. R. Soc. London Ser. B Biol. Sci. 319: 149-163.
  5. Preston, C. (2009). Thomas Browne and the Writing of Early Modern Science. (Cambridge, UK: Cambridge University Press).
  6. Ueda, H., Yokota, E., Kutsuna, N., Shimada, T., Tamura, K., Shimmen, T., Hasezawa, S., Dolja, V.V., and Hara-Nishimura, I. (2010). Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc. Natl. Acad. Sci. USA 107: 6894-6899.

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Authors
Paszkiewicz, G., Gualberto, J. M., Benamar, A., Macherel, D., & Logan, D. C.
Affiliations
  • Institut Agro Rennes-Angers (FR)
  • Centre National de la Recherche Scientifique (FR)
Venue
The Plant Cell
Published
2017-01
Volume
29
Issue
1
Pages
109-128
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
OpenAlex
W2568995559
Cited by
135
References
3
Citations by year
2026: 13 · 2025: 10 · 2024: 15 · 2023: 8 · 2022: 24 · 2021: 17 · 2020: 21 · 2019: 10 · 2018: 10 · 2017: 7
FWCI
12.93
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • The Plant Cell (publishedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • HAL (submittedVersion, other-oa)
Funders
Agence Nationale de la Recherche (ANR-11-LABX-0057)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Seed Germination and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords
seed germination, mitochondrial bioenergetics, mitochondrial dynamics, mitochondrial biogenesis, mitochondrial membrane potential, mitochondrial fusion, mitochondrial fragmentation, Arabidopsis thaliana, seed imbibition, seedling growth, live imaging
MeSH terms
Energy Metabolism, Mitochondria, Seeds, Water, Arabidopsis, Gene Expression Regulation, Plant, Gene Expression Regulation, Developmental, Germination, Microscopy, Confocal, Reverse Transcriptase Polymerase Chain Reaction, Arabidopsis Proteins, Plants, Genetically Modified, Seedlings, Time-Lapse Imaging

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