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.
Highlights
Most crop plants are exposed to HS during some stage of their life cycle
The results indicate that pre-treating the plants with ethephon caused a significant increase in the numbers of viable and germinating pollen grains following exposure to HS conditions, pointing to the involvement of ethylene in developing pollen grains’ thermotolerance
Ethephon-pretreatment caused heat-stressed pollen proteome to be closer to the proteome under non-stressful conditions: A higher abundance of proteins involved in those functions that were highly HS-affected/down-regulated was apparent
Summary
Most crop plants are exposed to HS during some stage of their life cycle. HS, defined as the temperatures above normal optimum, is expected to become a more frequent and acute problem in the coming years (Mittler et al, 2012; IPCC, 2014; Ghatak et al, 2017b). Plants encounter high temperature damage during spring and autumn when grown in the warmer regions of the world. During these seasons, short waves of high temperatures may be detrimental. Impaired pollen (the male gametophyte) development and functioning under high temperature conditions has been implicated in reduced yields across a large number of crop systems (Frank et al, 2009; Zinn et al, 2010; Bita and Gerats, 2013; Bokszczanin et al, 2013; Ghatak et al, 2017a). Heat-tolerant tomato cultivars (exhibiting higher yield under HS) produced larger numbers of high-quality pollen grains, exhibiting higher germination capacity, under HS compared with all tested heat-sensitive cultivars (Firon et al, 2006)
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