Abstract
BackgroundPollen development is central for plant reproduction and is assisted by changes of the transcriptome and proteome. At the same time, pollen development and viability is largely sensitive to stress, particularly to elevated temperatures. The transcriptomic and proteomic changes during pollen development and of different stages in response to elevated temperature was targeted to define the underlying molecular principles.ResultsThe analysis of the transcriptome and proteome of Solanum lycopersicum pollen at tetrad, post-meiotic and mature stage before and after heat stress yielded a decline of the transcriptome but an increase of the proteome size throughout pollen development. Comparison of the transcriptome and proteome led to the discovery of two modes defined as direct and delayed translation. Here, genes of distinct functional processes are under the control of direct and delayed translation. The response of pollen to elevated temperature occurs rather at proteome, but not as drastic at the transcriptome level. Heat shock proteins, proteasome subunits, ribosomal proteins and eukaryotic initiation factors are most affected. On the example of heat shock proteins we demonstrate a decoupling of transcript and protein levels as well as a distinct regulation between the developmental stages.ConclusionsThe transcriptome and proteome of developing pollen undergo drastic changes in composition and quantity. Changes at the proteome level are a result of two modes assigned as direct and delayed translation. The response of pollen to elevated temperature is mainly regulated at the proteome level, whereby proteins related to synthesis and degradation of proteins are most responsive and might play a central role in the heat stress response of pollen.
Highlights
Pollen development is central for plant reproduction and is assisted by changes of the transcriptome and proteome
The chosen treatment temperature is within the optimum temperature range (37 to 40 °C) to induce the tomato heat stress (HS) response such as accumulation of Heat shock protein (Hsp) [33]
For genes with delayed translation we observed high assignment to ‘chaperones & protein turnover’ (Fig. 7 tetrads delay; Additional file 5: Table S4). Among these genes we identified a member of the Hsp100 and a member Hsp70 family, which might contribute to a developmental priming of post-meiotic pollen
Summary
Pollen development is central for plant reproduction and is assisted by changes of the transcriptome and proteome. The transcriptomic and proteomic changes during pollen development and of different stages in response to elevated temperature was targeted to define the underlying molecular principles. The diploid pollen mother cell, known as microsporocyte, undergoes meiotic division to give rise to a tetrad of four haploid microspores. After release of the post-meiotic microspores from the tetrad, Keller and Simm BMC Genomics (2018) 19:447 and in particular in tomato (Solanum lycopersicum) have been conducted [9]. One of these studies was focused on the proteomic profiling of five pollen developmental stages of tomato, namely microsporocyte, tetrads, microspores, polarized microspores and mature pollen [10]. For example the proteome content of mature pollen is enriched for proteins associated with carbohydrate and energy metabolism, which was not apparent in the transcriptome [11]
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