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Alterations in the transcriptome and translatome profiles of Arabidopsis pollen germinated under heat stress

ABSTRACT: Plant reproduction is one key biological process very sensitive to heat stress and, as a consequence, enhanced global warming imposes serious threats to sustain food safety worldwide. In this work we have focused on the molecular impact that high temperature conditions impose on gene expression of Arabidopsis pollen germinated in vitro. We have used a high-resolution ribosome profiling technology to provide, for the first time, a comprehensive study of how both the transcriptome and the translatome of germinated pollen respond to the increase in temperature. Although heat shock responses operate properly under high temperature conditions, we have uncovered important alterations under elevated temperature regimes down-regulating essential processes linked to cation/proton exchange and to carbohydrate/cation symport transport. These alterations provide molecular explanations to the dramatic alterations of pollen tube growth under heat stress. Overall a high correlation between transcriptional and translational responses to high temperature was found, but specific regulations at the translational level are also present in pollen subjected to temperature challenging conditions.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE145795 | GEO | 2020/12/15

REPOSITORIES: GEO

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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: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.

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Alterations in the transcriptome and translatome profiles of Arabidopsis pollen germinated under heat stress

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