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Exposure of meiosis-to-microspore-stage tomato flowers to long-term mild heat results in pollen failure after mitosis.

ABSTRACT: Crop reproductive success is significantly challenged by heatwaves, which are increasing in frequency globally. The main reason is reduced male fertility due to abnormal pollen development, but the mechanism behind the developmental deviation is not well understood. Here, long-term mild heat (LTMH) treatment, mimicking a heatwave, was applied to flowers or whole plants and followed up by cytological, transcriptomic and biochemical analyses. LTMH was shown to act directly on the flowers and not via a systemic effect on other plant tissue. The meiosis to early microspore stage was the most to LTMH and three to four days of LTMH exposure around this period was sufficient to significantly reduce pollen viability. Extensive cytological analysis showed that abnormalities in pollen development could first be observed after pollen mitosis I and tapetum development appeared unaffected. Transcriptomic and biochemical analyses suggested that pollen development suffers from tapetal ER stress, with a limited role for oxidative stress. These characteristics differentiate the response of developing anthers and pollen to LTMH from that to severe heat stress.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE180168 | GEO | 2021/07/17

REPOSITORIES: GEO

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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 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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Exposure of meiosis-to-microspore-stage tomato flowers to long-term mild heat results in pollen failure after mitosis.

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