Circadian oscillation and development-dependent expression of glycine-rich RNA binding proteins in tomato fruits

Müller, Gabriela; Triassi, Agustina; Álvarez, Catalina; Ferreyra, Marı́a Lorena Falcone; Andreo, Carlos S.; Lara, Marı́a V.; Drincovich, Marı́a F.

doi:10.1071/fp13239

Cited by 4 publications

(14 citation statements)

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“…High HS-down-regulation (28-fold) was observed for an RNA-binding glycine-rich protein (GRP1, solyc10g051390; Table 2 ). Tomato GRP1 was recently shown to be expressed in tomato fruit and was suggested to be linked to circadian processes and to function as an RNA chaperone ( Müller et al, 2014 ). The Arabidopsis homologue, AtGRP8, was shown to be oxidative stress-responsive, participate in cold stress adaptation, serve as an output gene of the circadian clock and suggested as an RNA chaperone ( Ciuzan et al, 2015 ).…”

Section: Resultsmentioning

confidence: 99%

Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains

et al. 2018

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Heat stress is a major cause for yield loss in many crops, including vegetable crops. Even short waves of high temperature, becoming more frequent during recent years, can be detrimental. Pollen development is most heat-sensitive, being the main cause for reduced productivity under heat-stress across a wide range of crops. The molecular mechanisms involved in pollen heat-stress response and thermotolerance are however, not fully understood. Recently, we have demonstrated that ethylene, a gaseous plant hormone, plays a role in tomato (Solanum lycopersicum) pollen thermotolerance. These results were substantiated in the current work showing that increasing ethylene levels by using an ethylene-releasing substance, ethephon, prior to heat-stress exposure, increased pollen quality. A proteomic approach was undertaken, to unravel the mechanisms underlying pollen heat-stress response and ethylene-mediated pollen thermotolerance in developing pollen grains. Proteins were extracted and analyzed by means of a gel LC-MS fractionation protocol, and a total of 1,355 proteins were identified. A dataset of 721 proteins, detected in three biological replicates of at least one of the applied treatments, was used for all analyses. Quantitative analysis was performed based on peptide count. The analysis revealed that heat-stress affected the developmental program of pollen, including protein homeostasis (components of the translational and degradation machinery), carbohydrate, and energy metabolism. Ethephon-pre-treatment shifted the heat-stressed pollen proteome closer to the proteome under non-stressful conditions, namely, by showing higher abundance of proteins involved in protein synthesis, degradation, tricarboxylic acid cycle, and RNA regulation. Furthermore, up-regulation of protective mechanisms against oxidative stress was observed following ethephon-treatment (including higher abundance of glutathione-disulfide reductase, glutaredoxin, and protein disulfide isomerase). Taken together, the findings identified systemic and fundamental components of pollen thermotolerance, and serve as a valuable quantitative protein database for further research.

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Section: Resultsmentioning

confidence: 99%

Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains

et al. 2018

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“…Over the years, many studies have shown that GR-RBP genes are highly upregulated in response to cold stress, and examples include AtRZ-1a, GR-RBP4, AtRZ-1b , and AtRZ-1c from Arabidopsis ( Kim et al, 2005 , 2010a ; Kwak et al, 2005 ), BnGRP1 from B. napus ( Kim et al, 2012 ), three GRP2s ( Kwak et al, 2013 ), and GRP7 from C. sativa ( Kwak et al, 2016 ). There are also exceptions, and the accumulation of transcripts and proteins of all the LeGRP1a-c genes from harvested tomato fruit did not increase at 4°C ( Müller et al, 2014 ). In the current study, based on the responses to cold stress conditions, the six cucumber CsGR-RBP s genes could be divided into two categories, with CsGR-RBP2 being enhanced, and the other five not upregulatedby cold stress ( Figure 2 ).…”

Section: Discussionmentioning

confidence: 99%

A Glycine-Rich RNA-Binding Protein, CsGR-RBP3, Is Involved in Defense Responses Against Cold Stress in Harvested Cucumber (Cucumis sativus L.) Fruit

Wang

Shen

et al. 2018

Front. Plant Sci.

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Plant glycine-rich RNA-binding proteins (GR-RBPs) have been shown to play important roles in response to abiotic stresses in actively proliferating organs such as young plants, root tips, and flowers, but their roles in chilling responses of harvested fruit remains largely unknown. Here, we investigated the role of CsGR-RBP3 in the chilling response of cucumber fruit. Pre-storage cold acclimation at 10°C (PsCA) for 3 days significantly enhanced chilling tolerance of cucumber fruit compared with the control fruit that were stored at 5°C. In the control fruit, only one of the six cucumber CsGR-RBP genes, CsGR-RBP2, was enhanced whereas the other five, i.e., CsGR-RBP3, CsGR-RBP4, CsGR-RBP5, CsGR-RBP-blt801, and CsGR-RBP-RZ1A were not. However, in the fruit exposed to PsCA before storage at 5°C, CsGR-RBP2 transcript levels were not obviously different from those in the controls, whereas the other five were highly upregulated, with CsGR-RBP3 the most significantly induced. Treatment with endogenous ABA and NO biosynthesis inhibitors, tungstate and L-nitro-arginine methyl ester, respectively, prior to PsCA treatment, clearly downregulated CsGR-RBP3 expression and significantly aggravated chilling injury. These results suggest a strong connection between CsGR-RBP3 expression and chilling tolerance in cucumber fruit. Transient expression in tobacco suggests CsGR-RBP3 was located in the mitochondria, implying a role for CsGR-RBP3 in maintaining mitochondria-related functions under low temperature. Arabidopsis lines overexpressing CsGR-RBP3 displayed faster growth at 23°C, lower electrolyte leakage and higher Fv/Fm ratio at 0°C, and higher survival rate at -20°C, than wild-type plants. Under cold stress conditions, Arabidopsis plants overexpressing CsGR-RBP3 displayed lower reactive oxygen species levels, and higher catalase and superoxide dismutase expression and activities, compared with the wild-type plants. In addition, overexpression of CsGR-RBP3 significantly upregulated nine Arabidopsis genes involved in defense responses to various stresses, including chilling. These results strongly suggest CsGR-RBP3 plays a positive role in defense against chilling stress.

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“…Plants and storage conditions: S. lycopersicum WT and PG::preLeGRP1a transgenic lines were grown from seeds as described in Müller et al (2014). Flowers were tagged after pollination and fruits were allowed to develop until different stages according to the number of days after anthesis (DAA) and harvested for analysis or used for the postharvest treatments.…”

Section: Plasmid Construct and Plant Transformationmentioning

confidence: 99%

“…In our previous work, a GR-RBP family, which was called LeGRP1, was characterized in tomato fruits (Müller et al 2014). Three highly homologous LeGRP1 genes (LeGRP1a-c) were identified.…”

Section: Introductionmentioning

confidence: 99%

“…Differential circadian profiles of expression, dependent on the fruit developmental stage, have been found for each LeGRP1 form. During ripening of fruits harvested at the mature green (MG) stage of the vine, the content of all Legrp1a-c forms increases considerably; however, incubation at 4 ºC prevents such an increase (Müller et al 2014).…”

Section: Introductionmentioning

confidence: 99%

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Overexpression of glycine-rich RNA-binding protein in tomato renders fruits with higher protein content after cold storage

et al. 2018

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Glycine-rich RNA-binding proteins (GR-RBPs) are involved in RNA processing and also some of them are output signals of the circadian clock. In tomato, one GR-RBP gene family (LeGRP1) is composed by three highly homologous genes (LeGRP1a-c); each one rendering three transcriptional products: the un-spliced pre-RNA (preLegrp1a-c), the mature mRNA (mLegrp1a-c) and the alternatively spliced mRNA (asLegrp1a-c). To get insight into their regulation and impact on RNA metabolism in fruits, Solanum lycopersicum cv. Micro-Tom was transformed with preLeGRP1a fused to the polygalacturonase promoter, which drives expression to fruits from the mature green stage. Our results demonstrated a complex positive regulation of LeGRPs, in which LeGRP1a overexpression led to the induction of the others LeGRP1 members. Even though the LeGRP1 transcription and the content of three LeGRPs proteins were affected, the overall LeGRP protein circadian rhythm profile was similar in transgenic and wild type (WT) fruits. However, when the fruits were kept at a chilling temperature after harvest, total protein content was significantly higher in transgenic than in WT fruits, and the content of some free amino acids was modified. The results obtained suggest a probable role of LeGRP1s: structural rearrangements and/or stabilization of mRNA to allow efficient processing of fruits under cold conditions.

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Circadian oscillation and development-dependent expression of glycine-rich RNA binding proteins in tomato fruits

Cited by 4 publications

References 67 publications

Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains

Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains

A Glycine-Rich RNA-Binding Protein, CsGR-RBP3, Is Involved in Defense Responses Against Cold Stress in Harvested Cucumber (Cucumis sativus L.) Fruit

Overexpression of glycine-rich RNA-binding protein in tomato renders fruits with higher protein content after cold storage

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