Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Jegadeesan S

PROVIDER: S-EPMC6240657 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Publications

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

Jegadeesan Sridharan S Chaturvedi Palak P Ghatak Arindam A Pressman Etan E Meir Shimon S Faigenboim Adi A Rutley Nicholas N Beery Avital A Harel Arye A Weckwerth Wolfram W Firon Nurit N

Frontiers in plant science 20181112

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 ...[more]

PMID: 30483278

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Project description:BACKGROUND:Agriculture is highly dependent on climate. Increases in temperature caused by global warming pose challenges for crop production. Heat stress induces oxidative damage to cell membranes and then causes cell death. Plants have developed various responses to elevated temperatures, including hormone signaling pathways and heat shock factors that elevate their thermotolerance. In response to heat stress, the gaseous hormone ethylene is produced through regulation of the expression of signaling-related genes to modulate resource allocation dynamics. For comprehensive understanding of the role of ethylene, this study used an ethylene precursor to analyze the ethylene signaling pathway involved in adjustment of the homeostasis of the antioxidant system and to evaluate heat shock factor expression in rice seedlings under heat stress. RESULTS:Levels of cell membrane oxidation and ion leakage were reduced in rice seedlings under heat treatment combined with ethylene precursor treatment, conferring enhanced thermotolerance. Reduction of the fresh weight and chlorophyll a/b ratio in rice seedlings was lower in rice seedlings under heat stress with ethylene precursor treatment than in those under heat stress only. Moreover, reduction of antioxidant response caused by heat stress was ameliorated by treatment with ethylene precursors such as catalase and total peroxidase. Quantitative reverse transcriptase-polymerase chain reaction showed higher expression levels of heat shock factors such as HSFA1a and HSFA2a, c, d, e, and f and ethylene-signaling-related genes such as ethylene insensitive 2, ethylene insensitive-like 1, and ethylene insensitive-like 2 in rice seedlings under heat stress with ethylene precursor treatment than in rice seedlings under heat stress only. CONCLUSION:Ethylene-mediated signaling was involved in the reduction of oxidative damage, maintenance of chlorophyll content, and enhancement of thermotolerance in rice seedlings under heat stress. Furthermore, this study revealed heat shock factors and ethylene-signaling-related genes involved in complex network regulation that confers thermotolerance to rice seedlings.

Project description: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 1355 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-pretreatment 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.

Project description:Global temperature increase poses a serious challenge for agricultural production worldwide, affecting yield in many crops including vegetable crops. While most crop plants can survive temperature increases during their vegetative growth periods, the reproduction phase is highly heat-stress (HS)-sensitive. Impaired pollen development and functioning under HS is implicated as the major cause for yield reduction. To better understand HS effect on pollen and identify pollen thermotolerance mechanisms, we established conditions that enable developing pollen grains to acquire thermotolerance (ATT conditions), using tomato as a model system. High-throughput sequencing at cDNA level was performed by Massive Analysis of 3’cDNA using Illumina HiSeq 2000 technology, generating a total of 6430 and 4660 transcripts differentially expressed (p ≤ 1e-05) during pollen development/maturation and following response of developing pollen to ATT, respectively. Gene Onthology functional analysis showed that transcripts related to maintenance of protein homeostasis (translation, proteolysis, protein folding) were enriched during pollen maturation and following the ATT treatment in our study, highlighting these processes as central for enabling pollen maturation and maintenance of pollen functioning under HS. The transcriptomic data was compared to available pollen proteomic data based on the same experimental setup and an overlap of 47% was detected between differentially expressed proteins and transcripts following ATT conditions, highlighting genes/proteins involved in protein folding, oxidation-reduction and translation, and validating transcriptomic results. Involvement of mitochondria and endoplasmic reticulum in pollen heat acclimation, and activation of several HSPs including sHSPs and HSP101, for protecting pollen cellular components including the translational machinery, are indicated. The results of this study can serve as a valuable resource of genes for future research on improving pollen thermotolerance.

Project description:Climate change is causing temperature increment in crop production areas worldwide, generating conditions of heat stress that negatively affect crop productivity. Tomato (Solanum lycopersicum), a major vegetable crop, is highly susceptible to conditions of heat stress. When tomato plants are exposed to ambient day/night temperatures that exceed 32 °C/20 °C, respectively, during the reproductive phase, fruit set and fruit weight are reduced, leading to a significant decrease in yield. Processing tomato cultivars are cultivated in open fields, where environmental conditions are not controlled; therefore, plants are exposed to multiple abiotic stresses, including heat stress. Nonetheless, information on stress response in processing tomatoes is very limited. Understanding the physiological response of modern processing tomato cultivars to heat stress may facilitate the development of thermotolerant cultivars. Here, we compared two tomato processing cultivars, H4107 and H9780, that we found to be constantly differing in yield performance. Using field and temperature-controlled greenhouse experiments, we show that the observed difference in yield is attributed to the occurrence of heat stress conditions. In addition, fruit set and seed production were significantly higher in the thermotolerant cultivar H4107, compared with H9780. Despite the general acceptance of pollen viability as a measure of thermotolerance, there was no difference in the percentage of viable pollen between H4107 and H9780 under either of the conditions tested. In addition to observations of similar pollen germination and bud abscission rates, our results suggest that processing tomato cultivars may present a particular case, in which pollen performance is not determining reproductive thermotolerance. Our results also demonstrate the value of combining controlled and uncontrolled experimental settings, in order to validate and identify heat stress-related responses, thus facilitating the development of thermotolerant processing tomato cultivars.

Dataset Information

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

Publications

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

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