Dataset Information

Flavonols improve thermotolerance in tomato pollen during germination and tube elongation by maintaining ROS homeostasis.

ABSTRACT: Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The Solanum lycopersicum anthocyanin reduced (are) mutant has a defect in the FLAVANONE 3 HYDROXYLASE (F3H) gene and impaired synthesis of flavonol antioxidants. We identified multiple aspects of pollen performance in are that were hypersensitive to elevated temperatures relative to the VF36 parental line, including heat-increased accumulation of reactive oxygen species (ROS). Transformation of are with an F3H transgene, or chemical complementation with flavonols, prevented temperature-dependent ROS accumulation in pollen and restored pollen performance to VF36 levels. Transformation of this F3H construct into VF36 (VF36-F3H-T3) prevented both temperature driven ROS increases and impaired pollen performance. RNA-Seq was performed at optimal and stress temperatures in are, VF36, and VF36-F3H-T3 at multiple timepoints across pollen tube emergence and elongation. All genotypes had increasing numbers of differentially expressed genes with duration of elevated temperature, with the largest number in are at all time points. These analyses also identified upregulated transcripts in are, relative to VF36, even at optimal temperatures, revealing a flavonol-regulated transcriptome. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that leads to reproductive failure and crop loss.

SUBMITTER: Postiglione AE

PROVIDER: S-EPMC10769439 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Flavonols improve thermotolerance in tomato pollen during germination and tube elongation by maintaining ROS homeostasis.

Postiglione Anthony E AE Delange Allison M AM Ali Mohammad Foteh MF Wang Eric Y EY Houben Maarten M Hahn Stacy L SL Khoury Maleana G MG Roark Colleen M CM Davis Molly M Reid Robert W RW Pease James B JB Loraine Ann E AE Muday Gloria K GK

bioRxiv : the preprint server for biology 20240507

Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The Solanum lycopersicum anthocyanin reduced ( are ) mutant has a FLAVANONE 3 HYDROXYLASE ( F3H ) gene mutation resulting in impaired synthesis of flavonol antioxidants. The are mutant has reduced pollen performance and seed set relative to the VF36 parental line, which is accentuated at elevated temperatures. Transformation of are with the wild-type ...[more]

PMID: 38187649

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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 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.

Project description:Pollen germination, along with pollen tube growth, is an essential process for the reproduction of flowering plants. The germinating pollen with tip-growth characteristics provides an ideal model system for the study of cell growth and morphogenesis. As an essential step towards a detailed understanding of this important process, the objective of this study was to comprehensively analyze the transcriptome changes during pollen germination and pollen tube growth. Using Affymetrix Arabidopsis ATH1 Genome Arrays, this study is the first to show the changes in the transcriptome from desiccated mature pollen grains to hydrated pollen grains and then to pollen tubes of Arabidopsis thaliana. The number of expressed genes, either for total expressed genes or for specifically expressed genes, increased significantly from desiccated mature pollen to hydrated pollen and again to growing pollen tubes, which is consistent with the finding that pollen germination and tube growth was significantly inhibited in vitro by a transcriptional inhibitor. The results of GO analyses showed that expression of genes related to cell rescue, transcription, signal transduction and cellular transport were significantly changed, especially for up-regulation, during pollen germination and tube growth, respectively. In particular, genes of the CaM/CML, CHX and Hsp families showed the most significant changes during pollen germination and tube growth. These results demonstrate that the overall transcription of genes, both in the number of expressed genes and in the levels of transcription, was increased. Furthermore, the appearance of many novel transcripts during pollen germination as well as tube growth indicates that these newly expressed genes may function in this complex process. SUBMITTER_CITATION: Yi Wang, Wen-Zheng Zhang, Lian-Fen Song, Jun-Jie Zou, Zhen Su, and Wei-Hua Wu. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. September 5, 2008; 10.1104/pp.108.126375 Experiment Overall Design: Three samples are analyzed in this experiment. They are desiccated mature pollen grains (MP), hydrated pollen grains (HP) and growing pollen tubes (PT) of Arabidopsis thaliana, respectively. Each sample has two biological replicates, so that there are 6 data sets of ATH1 array in this experiment.

Dataset Information

Flavonols improve thermotolerance in tomato pollen during germination and tube elongation by maintaining ROS homeostasis.

Publications

Flavonols improve thermotolerance in tomato pollen during germination and tube elongation by maintaining ROS homeostasis.

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