Targeted mRNA Oxidation Regulates Sunflower Seed Dormancy Alleviation during Dry After-Ripening

Bazin, Jérémie; Langlade, Nicolas; Vincourt, Patrick; Arribat, Sandrine; Balzergue, Sandrine; El-Maarouf-Bouteau, Hayat; Bailly, Christophe

doi:10.1105/tpc.111.086694

Cited by 177 publications

(212 citation statements)

References 74 publications

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“…Further research will address the question of the spatiotemporal control of mRNA translation during seed germination, notably concerning translational control by small RNAs (133)(134)(135) and mRNA oxidation (136). However, an unanswered question regarding oxidized mRNAs and small RNAs concerns the identity and determinants of mRNA decay and translational repression.…”

Section: Conclusion and Prospectsmentioning

confidence: 99%

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Galland¹,

Huguet²,

Arc³

et al. 2014

Molecular & Cellular Proteomics

142

155

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During seed germination, the transition from a quiescent metabolic state in a dry mature seed to a proliferative metabolic state in a vigorous seedling is crucial for plant propagation as well as for optimizing crop yield. This work provides a detailed description of the dynamics of protein synthesis during the time course of germination, demonstrating that mRNA translation is both sequential and selective during this process. The complete inhibition of the germination process in the presence of the translation inhibitor cycloheximide established that mRNA translation is critical for Arabidopsis seed germination. However, the dynamics of protein turnover and the selectivity of protein synthesis (mRNA translation) during Arabidopsis seed germination have not been addressed yet. Based on our detailed knowledge of the Arabidopsis seed proteome, we have deepened our understanding of seed mRNA translation during germination by combining twodimensional gel-based proteomics with dynamic radiolabeled proteomics using a radiolabeled amino acid precursor, namely [35 S]-methionine, in order to highlight de novo protein synthesis, stability, and turnover. Our data confirm that during early imbibition, the Arabidopsis translatome keeps reflecting an embryonic maturation program until a certain developmental checkpoint. Furthermore, by dividing the seed germination time lapse into discrete time windows, we highlight precise and specific patterns of protein synthesis. These data refine and deepen our knowledge of the three classical phases of seed germination based on seed water uptake during imbibition and reveal that selective mRNA translation is a key feature of seed germination. Beyond the quantitative control of translational activity, both the selectivity of mRNA translation and protein turnover appear as specific regulatory systems, critical for timing the molecular events leading to successful germination and seedling establishment. Molecular & Cellular Proteomics 13: 10.1074/mcp.M113.032227, 252-268, 2014.Seed germination is a vital stage in the plant life cycle during which embryo cells experience a programmed transition from a quiescent to a highly active metabolic state. Accordingly, seed quality in terms of germination vigor is of paramount importance for both ecological aspects and practical applications, as it influences the level, timing, and uniformity of seedling emergence in a wide range of environmental conditions (1, 2). In efforts to decipher the complex molecular mechanisms that control seed germination, genetic, genomic, and postgenomic analyses have been developed on the model plant Arabidopsis thaliana (3-6). Germination is classically described as a sequential time course divided into three major phases of seed water uptake (7). Phase I is characterized by rapid seed imbibition, which is crucial for the transition from the quiescent metabolic state of the dry seed to the high metabolic activity of the hydrated seed. Phase II corresponds to a period during which the seed imbibition level remains const...

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Section: Conclusion and Prospectsmentioning

confidence: 99%

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Galland¹,

Huguet²,

Arc³

et al. 2014

Molecular & Cellular Proteomics

142

155

View full text Add to dashboard Cite

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“…The release of dormancy by after-ripening is an intriguing process because it occurs in dry seeds with very low humidity levels that prevent active metabolic processes. Nonenzymatic processes have been proposed to alleviate dormancy and experimental evidence for a role of reactive oxygen species in dormancy release by after-ripening in sunflower (Helianthus annuus) has been presented (Oracz et al, 2007;Bazin et al, 2011). An alternative, but not mutually exclusive, theory for the after-ripening mechanism is provided by indirect evidence for the occurrence of humid pockets within dry seeds that would enable transcription and translation of germination factors (Leubner-Metzger, 2005).…”

Section: Introductionmentioning

confidence: 99%

The Time Required for Dormancy Release in Arabidopsis Is Determined by DELAY OF GERMINATION1 Protein Levels in Freshly Harvested Seeds

et al. 2012

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Seed dormancy controls the start of a plant's life cycle by preventing germination of a viable seed in an unfavorable season. Freshly harvested seeds usually show a high level of dormancy, which is gradually released during dry storage (afterripening). Abscisic acid (ABA) has been identified as an essential factor for the induction of dormancy, whereas gibberellins (GAs) are required for germination. The molecular mechanisms controlling seed dormancy are not well understood. DELAY OF GERMINATION1 (DOG1) was recently identified as a major regulator of dormancy in Arabidopsis thaliana. Here, we show that the DOG1 protein accumulates during seed maturation and remains stable throughout seed storage and imbibition. The levels of DOG1 protein in freshly harvested seeds highly correlate with dormancy. The DOG1 protein becomes modified during after-ripening, and its levels in stored seeds do not correlate with germination potential. Although ABA levels in dog1 mutants are reduced and GA levels enhanced, we show that DOG1 does not regulate dormancy primarily via changes in hormone levels. We propose that DOG1 protein abundance in freshly harvested seeds acts as a timer for seed dormancy release, which functions largely independent from ABA.

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“…Oxidative processes affecting both proteins and transcripts during the storage of dry seeds have been shown to influence the release of dormancy (Oracz et al, 2007;Bazin et al, 2011;Gao et al, 2013). Posttranslational modifications during seed imbibition, such as oxidation, phosphorylation/ dephosphorylation, ubiquitination, and acetylation, affect protein function and are probably involved in the control of germination (Le et al, 1998;Buchanan and Balmer, 2005;Lu et al, 2008;Arc et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

REDUCED DORMANCY5Encodes a Protein Phosphatase 2C That Is Required for Seed Dormancy inArabidopsis

et al. 2014

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Seed dormancy determines germination timing and contributes to crop production and the adaptation of natural populations to their environment. Our knowledge about its regulation is limited. In a mutagenesis screen of a highly dormant Arabidopsis thaliana line, the reduced dormancy5 (rdo5) mutant was isolated based on its strongly reduced seed dormancy. Cloning of RDO5 showed that it encodes a PP2C phosphatase. Several PP2C phosphatases belonging to clade A are involved in abscisic acid signaling and control seed dormancy. However, RDO5 does not cluster with clade A phosphatases, and abscisic acid levels and sensitivity are unaltered in the rdo5 mutant. RDO5 transcript could only be detected in seeds and was most abundant in dry seeds. RDO5 was found in cells throughout the embryo and is located in the nucleus. A transcriptome analysis revealed that several genes belonging to the conserved PUF family of RNA binding proteins, in particular Arabidopsis PUMILIO9 (APUM9) and APUM11, showed strongly enhanced transcript levels in rdo5 during seed imbibition. Further transgenic analyses indicated that APUM9 reduces seed dormancy. Interestingly, reduction of APUM transcripts by RNA interference complemented the reduced dormancy phenotype of rdo5, indicating that RDO5 functions by suppressing APUM transcript levels.

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Targeted mRNA Oxidation Regulates Sunflower Seed Dormancy Alleviation during Dry After-Ripening

Cited by 177 publications

References 74 publications

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

The Time Required for Dormancy Release in Arabidopsis Is Determined by DELAY OF GERMINATION1 Protein Levels in Freshly Harvested Seeds

REDUCED DORMANCY5Encodes a Protein Phosphatase 2C That Is Required for Seed Dormancy inArabidopsis

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