In-Depth Temporal Transcriptome Profiling Reveals a Crucial Developmental Switch with Roles for RNA Processing and Organelle Metabolism That Are Essential for Germination in Arabidopsis

Narsai, Reena; Law, Simon R.; Carrie, Chris; Lin, Xu; Whelan, James

doi:10.1104/pp.111.183129

Cited by 175 publications

(224 citation statements)

References 89 publications

(153 reference statements)

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“…S1), predicted by the NLStradamus program (Nguyen Ba et al, 2009). A GFP fusion protein confirms that the SAUR36 protein is targeted to the nucleus (Narsai et al, 2011). Auxin can activate the 1-aminocyclopropane-1-carboxylate biosynthetic step to stimulate ethylene production, which in turn promotes senescence (Abel et al, 1995).…”

Section: Auxin May Promote Leaf Senescence In Arabidopsismentioning

confidence: 99%

SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis

2012

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Small Auxin Up RNA genes (SAURs) are early auxin-responsive genes, but whether any of them are involved in leaf senescence is not known. Auxin, on the other hand, has been shown to have a role in leaf senescence. Some of the external application experiments indicated that auxin can inhibit leaf senescence, whereas other experiments indicated that auxin can promote leaf senescence. Here, we report the identification and characterization of an Arabidopsis (Arabidopsis thaliana) leaf senescenceassociated gene named SAG201, which is highly up-regulated during leaf senescence and can be induced by 1-naphthaleneacetic acid, a synthetic auxin. It encodes a functionally uncharacterized SAUR that has been annotated as SAUR36. Leaf senescence in transfer DNA insertion saur36 knockout lines was delayed as revealed by analyses of chlorophyll content, F v /F m ratio (a parameter for photosystem II activity), ion leakage, and the expression of leaf senescence marker genes. In contrast, transgenic Arabidopsis plants overexpressing SAUR36 (without its 39 untranslated region [UTR]) displayed an early leaf senescence phenotype. However, plants overexpressing SAUR36 with its 39 UTR were normal and did not exhibit the early-senescence phenotype. These data suggest that SAUR36 is a positive regulator of leaf senescence and may mediate auxin-induced leaf senescence and that the 39 UTR containing a highly conserved downstream destabilizes the SAUR36 transcripts in young leaves.

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Section: Auxin May Promote Leaf Senescence In Arabidopsismentioning

confidence: 99%

SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis

2012

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“…Probe sets were considered present if they were detected in at least two replicates before GC-Robust Multiarray Average normalization was performed to obtain normalized intensities (39). From the 20, 24, 18, 20, 15, 10, 27, and 13 unambiguous Arabidopsis Gene Indexes (AGIs) of, respectively, Cluster 1 through Cluster 8 (supplemental Table S8), transcriptome data could be found for, respectively, 19, 22, 16, 17, 12, 6, 24, and 12 AGIs in the Arabidopsis transcriptome data set (18). For each gene, the corresponding normalized transcript value was divided by its maximum to reach a transcript abundance between 0 and 1.…”

Section: Methodsmentioning

confidence: 99%

“…Heat Maps of Transcript Abundance, Protein Neosynthesis, and Protein Abundance-An Affymetrix ATH1 data set focused on Arabidopsis seed physiology between harvest and seedling establishment stages was retrieved (18). Microarray Analysis Suite 5.0 (Affymetrix, Santa Clara, CA) normalization was first performed on raw CEL files to determine present/absent/marginal calls for each probe set (39).…”

Section: Methodsmentioning

confidence: 99%

“…A high proportion of the genome is already expressed in the mature dry Arabidopsis seed; over 10,000 transcripts have been detected (15)(16)(17)(18)(19). Proteomic studies disclosed that only protein translation is required for radicle protrusion, indicating that germination-specific proteins are translated from stored mRNAs (20,21).…”

mentioning

confidence: 99%

“…To this end, we employed a combined approach involving two-dimensional gel-based differential proteomics and dynamic radiolabeled proteomics. The integration of these proteomic results with publicly available transcriptomic data (18) provides an original perspective on the contribution of dynamic protein turnover and selective mRNA translation in seed germination.…”

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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

140

153

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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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Plant Mitochondria

Ghifari¹,

Murcha²

2020

Encyclopedia of Life Sciences

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Plant mitochondria, like the mitochondria of other eukaryotes, originated from an endosymbiotic event and have retained their own genome. Over a billion years of evolution, most mitochondrial genes are laterally transferred to the nucleus. Consequently, most proteins required for mitochondrial biogenesis and activity are synthesised in the cytosol and imported via specific protein import machineries. Mitochondria are energy‐generating organelles that via electron transfer chain (ETC), create a proton gradient and generate adenosine triphosphate (ATP), the energy chemical used by the cell for numerous biochemical reactions. Energy production can come at a cost as reactive oxygen species (ROS) are generated as by‐product. Plant mitochondria have alternative ETC pathways to regulate mitochondrial ROS (mtROS) through modulating the rate of redox reactions, proton gradient and ATP production. Although excessive ROS can damage cellular components and lead to programmed cell death, mtROS also play an important role as signalling molecules. mtROS are involved in nucleus–mitochondria communications (anterograde–retrograde signalling), mitochondrial autophagy (mitophagy) and play a role in the plant response to various environmental stimuli. Considering the pivotal roles of mitochondria in energy generation and cellular signalling, perturbation of mitochondrial biogenesis and activity renders plants to be more susceptible to various stresses and ultimately compromises plant growth, development and reproduction. Key Concepts Plant mitochondria are small (1–2 μm long) rod‐shaped organelle that undergo frequent fusion and fission events. The plant mitochondrial inner membrane houses protein complexes involved in the electron transfer chain (ETC) that creates a proton‐motive gradient across the intermembrane space to drive the production of adenosine triphosphate (ATP) through ATP synthase. The majority of plant mitochondrial proteins (approximately 2000) are encoded in the nuclear genome, whereas the plant mitochondrial genome contains around 50 genes encoding for ETC subunits, mitoribosomal translation machinery and transfer ribonucleic acids (tRNAs). The abundance of mtROS produced by the ETC is proportionally linked with the efficiency and rate of electron transfer and ATP production. Plant mitochondria have alternative ETC pathways to modulate ROS homeostasis, proton gradient and ATP production. mtROS can damage mitochondrial macromolecules and ultimately organelle function but are also important signalling molecules in various pathways, including stress response and anterograde–retrograde signalling. The nucleus controls mitochondrial gene expression through anterograde signalling, yet the mitochondria can also influence nuclear gene expression through retrograde signalling. Disrupted plant mitochondrial function often causes enhanced sensitivity to a number of stresses, disrupted pollen development in cytoplasmic male sterility and affects normal plant growth and development.

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In-Depth Temporal Transcriptome Profiling Reveals a Crucial Developmental Switch with Roles for RNA Processing and Organelle Metabolism That Are Essential for Germination in Arabidopsis

Cited by 175 publications

References 89 publications

SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis

SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis

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

Plant Mitochondria

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