An Arabidopsis ATP-Dependent, DEAD-Box RNA Helicase Loses Activity upon IsoAsp Formation but Is Restored by PROTEIN ISOASPARTYL METHYLTRANSFERASE

Nayak, Nihar R.; Putnam, Andrea; Addepalli, Balasubrahmanyam; Lowenson, Jonathan D.; Chen, Tingsu; Jankowsky, Eckhard; Perry, Sharyn E.; Dinkins, Randy D.; Limbach, Patrick A.; Clarke, Steven; Downie, A. Bruce

doi:10.1105/tpc.113.113456

Cited by 26 publications

(22 citation statements)

References 56 publications

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“…Overall, high PIMT activity in developing and mature, quiescent, rice seeds is essential, possibly because of the repair of those proteins playing an important role in the preservation of the structural and functional integrity of membranes, DNA and protein molecules during germination. To support this hypothesis, various protective molecules, such as HSPs, LEA and enzymes such as RNA helicase, which are important for seed desiccation, longevity and germination in Arabidopsis, have been shown to be susceptible to isoAsp accumulation (Chen et al ., ; Nayak et al ., ). Further, seeds also possess large numbers of antioxidative enzymes and proteins to restrict ROS accumulation in seeds (Bailly, ; Rajjou & Debeaujon, ).…”

Section: Discussionmentioning

confidence: 97%

Rice PROTEIN l‐ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity

et al. 2016

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SummaryPROTEIN L-ISOASPARTYL O-METHYLTRANSFERASE (PIMT) is a protein-repairing enzyme involved in seed vigor and longevity. However, the regulation of PIMT isoforms during seed development and the mechanism of PIMT-mediated improvement of seed vigor and longevity are largely unknown.In this study in rice (Oryza sativa), we demonstrate the dynamics and correlation of isoaspartyl (isoAsp)-repairing demands and PIMT activity, and their implications, during seed development, germination and aging, through biochemical, molecular and genetic studies.Molecular and biochemical analyses revealed that rice possesses various biochemically active and inactive PIMT isoforms. Transcript and western blot analyses clearly showed the seed development stage and tissue-specific accumulation of active isoforms. Immunolocalization studies revealed distinct isoform expression in embryo and aleurone layers. Further analyses of transgenic lines for each OsPIMT isoform revealed a clear role in the restriction of deleterious isoAsp and age-induced reactive oxygen species (ROS) accumulation to improve seed vigor and longevity.Collectively, our data suggest that a PIMT-mediated, protein repair mechanism is initiated during seed development in rice, with each isoform playing a distinct, yet coordinated, role. Our results also raise the intriguing possibility that PIMT repairs antioxidative enzymes and proteins which restrict ROS accumulation, lipid peroxidation, etc. in seed, particularly during aging, thus contributing to seed vigor and longevity.

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Section: Discussionmentioning

confidence: 97%

Rice PROTEIN l‐ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity

et al. 2016

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“…Recent studies have reported that some genes associated with nucleic acid pathways—including RNA helicases—are involved in abiotic stress responses (Guan et al, ; Khan et al, ; Tuteja, Sahoo, Garg, & Tuteja, ). RNA helicases are ubiquitous enzymes found in prokaryotes and eukaryotes, and they catalyse the unwinding of duplex RNA secondary structures (Emery, de la Cruz, Rocak, Deloche, & Linder, ; Nayak et al, ; Rocak & Linder, ). At the sequence level, RNA helicases are divided into five groups—SF1 to SF5.…”

Section: Introductionmentioning

confidence: 99%

A DEAD‐box RNA helicase, RH8, is critical for regulation of ABA signalling and the drought stress response via inhibition of PP2CA activity

Baek

Lim

Lee

2018

Plant Cell & Environment

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Abscisic acid (ABA) is major plant hormone involved in regulating abiotic stress responses. Several studies have established that an ABA-signalling transduction pathway-from ABA perception to response-functions in plant cells. The group A PP2Cs constitute core components of ABA signalling, and they negatively regulate ABA signalling and stress responses. Recent studies have identified and functionally analysed regulators of PP2C activity; however, the precise regulatory mechanisms remain unclear. In the present study, we used a yeast 2-hybrid (Y2H) screening analysis to identify the DEAD-box RNA helicase RH8, which interacted with PP2CA in the nucleus. rh8 knockout mutants exhibited ABA hyposensitivity and drought-susceptible phenotypes characterized by high levels of transpirational water loss via reduced stomatal closure and decreased leaf temperatures. However, rh8/pp2ca double mutants showed ABA hypersensitivity and drought-tolerant phenotypes, indicating that RH8 and PP2CA function in the same ABA-signalling pathway in the drought stress response; moreover, RH8 functions upstream of PP2CA. In vitro phosphatase and kinase assays revealed that RH8 inhibits PP2CA phosphatase activity. Our data indicate that RH8 and its interacting partner PP2CA modulate the drought stress response via ABA-dependent signalling.

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“…Two independent studies in Arabidopsis identified isoAsp repair by PIMT1 as critical for seed quality (Ogé et al, 2008;Nayak et al, 2013). PIMT overexpression lines showed reduced levels of proteins with isoAsp residues, whereas reduced PIMT1 lines showed increased levels.…”

Section: Deamidationmentioning

confidence: 99%

“…Consistently, PIMT1 levels corresponded with prolonging seed lifetime and germination vigor (Ogé et al, 2008). Nayak et al (2013) focused specifically on the function of a DEAD box RNA helicase (plant RNA helicase75 [PRH75]) that is important in translation upon imbibition in seeds. PRH75 becomes inactivated upon the formation of isoAsp, and the study showed that PIMT1 is essential to convert isoAsp to Asp, thereby restoring PRH75 function.…”

Section: Deamidationmentioning

confidence: 99%

Update: Post-translational protein modifications in plant metabolism

2015

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ORCID ID: 0000-0001-9536-0487 (K.J.v.W.).Posttranslational modifications (PTMs) of proteins greatly expand proteome diversity, increase functionality, and allow for rapid responses, all at relatively low costs for the cell. PTMs play key roles in plants through their impact on signaling, gene expression, protein stability and interactions, and enzyme kinetics. Following a brief discussion of the experimental and bioinformatics challenges of PTM identification, localization, and quantification (occupancy), a concise overview is provided of the major PTMs and their (potential) functional consequences in plants, with emphasis on plant metabolism. Classic examples that illustrate the regulation of plant metabolic enzymes and pathways by PTMs and their cross talk are summarized. Recent large-scale proteomics studies mapped many PTMs to a wide range of metabolic functions. Unraveling of the PTM code, i.e. a predictive understanding of the (combinatorial) consequences of PTMs, is needed to convert this growing wealth of data into an understanding of plant metabolic regulation.The primary amino acid sequence of proteins is defined by the translated mRNA, often followed by Nor C-terminal cleavages for preprocessing, maturation, and/or activation. Proteins can undergo further reversible or irreversible posttranslational modifications (PTMs) of specific amino acid residues. Proteins are directly responsible for the production of plant metabolites because they act as enzymes or as regulators of enzymes. Ultimately, most proteins in a plant cell can affect plant metabolism (e.g. through effects on plant gene expression, cell fate and development, structural support, transport, etc.). Many metabolic enzymes and their regulators undergo a variety of PTMs, possibly resulting in changes in oligomeric state, stabilization/degradation, and (de)activation (Huber and Hardin, 2004), and PTMs can facilitate the optimization of metabolic flux. However, the direct in vivo consequence of a PTM on a metabolic enzyme or pathway is frequently not very clear, in part because it requires measurements of input and output of the reactions, including flux through the enzyme or pathway. This Update will start out with a short overview on the major PTMs observed for each amino acid residue (Table I), followed by a brief discussion of techniques for the characterization of protein PTMs, including determination of the localization within proteins (i.e. the specific residues) and occupancy. Challenges in dealing with multiple PTMs per protein and cross talk between PTMs will be briefly outlined. We then describe the major physiological PTMs observed in plants as well as PTMs that are nonenzymatically induced during sample preparation (Table II). Finally, this Update is completed with a number of well-studied, classical examples of the regulation of plant metabolism by PTMs, in particular for enzymes in primary metabolism (Calvin cycle, glycolysis, and respiration) and the C4 shuttle accommodating photosynthesis in C4 plants (Table III). As will be ev...

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An Arabidopsis ATP-Dependent, DEAD-Box RNA Helicase Loses Activity upon IsoAsp Formation but Is Restored by PROTEIN ISOASPARTYL METHYLTRANSFERASE

Cited by 26 publications

References 56 publications

Rice PROTEIN l‐ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity

Rice PROTEIN l‐ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity

A DEAD‐box RNA helicase, RH8, is critical for regulation of ABA signalling and the drought stress response via inhibition of PP2CA activity

Update: Post-translational protein modifications in plant metabolism

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