Dataset Information

The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen

ABSTRACT: Pollen development is central for plant reproduction and is assisted by changes of the transcriptome and the proteome. At the same time, pollen is largely heat sensitive, particularly at early developmental stages. To define the changes during development and the response of different stages to elevated temperatures we investigated the transcriptome and proteome of pollen at tetrad, post-meiotic and mature stage before and after application of elevated temperatures. We used Solanum lycopersicum as an economically important crop. We demonstrate that the number of transcripts declines from tetrad to mature stage, while the protein content shows the opposite trend. Comparison of the transcriptome and proteome led to the discovery of two translational modes assigned as direct translation – transcripts increased in a specific pollen stage lead to increased translation in the same stage – and delayed translation – transcripts are produced for translation in later stages. The response to elevated temperatures is with ~5% of all genes being upregulated comparable to general plant behavior. The alteration at proteome level marked the mature pollen as least responsive and the post-meiotic stages as most responsive with altered levels of 40% of the identified proteins. For a subset of the genes with direct translation we observed a downregulation of protein levels after heat stress, whereas some of the genes with delayed translation showed a shift from delayed to direct translation when heat stress is applied. Further, Hsps, proteasome subunits, ribosomal proteins as well as eukaryotic initiation factors are the most drastically affected groups. On the example of Hsps we document that the response at transcriptome and proteome levels in e.g. the post-meiotic and mature stage does not correlate. Moreover, while all stages respond to heat stress with regulation of transcript abundance of Hsps in a comparable manner, changes at proteome level are distinct. Thus, we demonstrate that the difference in heat stress response in different stages of pollen development is rather manifested by significant changes of protein than transcript abundance.

INSTRUMENT(S): LTQ Orbitrap

ORGANISM(S): Solanum Lycopersicum

TISSUE(S): Plant Cell, Pollen

SUBMITTER: Stefan Simm

LAB HEAD: Enrico Schleiff

PROVIDER: PXD008762 | Pride | 2015-05-15

REPOSITORIES: Pride

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Publications

The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen.

Keller Mario M Simm Stefan S

BMC genomics 20180608 1

<h4>Background</h4>Pollen 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.<h4>Results</h4>The analysis of the transcriptome and prot ...[more]

PMID: 29884134

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Project description:Pollen development is central for plant reproduction and is assisted by changes of the transcriptome and the proteome. At the same time, pollen is largely heat sensitive, particularly at early developmental stages. To define the changes during development and the response of different stages to elevated temperatures we investigated the transcriptome and proteome of pollen at tetrad, post-meiotic and mature stage before and after application of elevated temperatures. We used Solanum lycopersicum as an economically important crop. We demonstrate that the number of transcripts declines from tetrad to mature stage, while the protein content shows the opposite trend. Comparison of the transcriptome and proteome led to the discovery of two translational modes assigned as direct translation – transcripts increased in a specific pollen stage lead to increased translation in the same stage – and delayed translation – transcripts are produced for translation in later stages. The response to elevated temperatures is with ~5% of all genes being upregulated comparable to general plant behavior. The alteration at proteome level marked the mature pollen as least responsive and the post-meiotic stages as most responsive with altered levels of 40% of the identified proteins. For a subset of the genes with direct translation we observed a downregulation of protein levels after heat stress, whereas some of the genes with delayed translation showed a shift from delayed to direct translation when heat stress is applied. Further, Hsps, proteasome subunits, ribosomal proteins as well as eukaryotic initiation factors are the most drastically affected groups. On the example of Hsps we document that the response at transcriptome and proteome levels in e.g. the post-meiotic and mature stage does not correlate. Moreover, while all stages respond to heat stress with regulation of transcript abundance of Hsps in a comparable manner, changes at proteome level are distinct. Thus, we demonstrate that the difference in heat stress response in different stages of pollen development is rather manifested by significant changes of protein than transcript abundance. ------------------------------------------------------- Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium

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:Pollen development from the microspore involves a series of coordinated cellular events, and the resultant mature pollen is specialized in function that it can quickly germinate and produces a polar-growth pollen tube derived from the vegetative cell to deliver two sperms for fertilization. Understanding the molecular program underlying pollen development and germination still remains a major challenge for plant biology. We used Affymetrix GeneChip Rice Genome Array to comprehensively analyzed the dynamic changes in the transcriptomes of rice pollen at five sequential developmental stages from microspores to germinated pollen. Among the 51,279 transcripts on the array, we found 25,062 pollen-preferential transcripts, among which 2,203 were development stage-enriched. The diversity of transcripts decreased greatly from microspores to mature and germinated pollen, whereas the number of stage-enriched transcripts displayed a U-type change, with the lowest at the bicellular pollen stage; and a transition of overrepresented stage-enriched transcript groups associated with different functional categories, which indicates a shift in gene expression program at the bicellular pollen stage. About 54% of the now-annotated rice F-box protein genes were expressed preferentially in pollen. The transcriptome profile of germinated pollen was significantly and positively correlated with that of mature pollen. Analysis of expression profiles and coexpressed features of the pollen-preferential transcripts related to cell cycle, transcription, the ubiquitin/26S proteasome system, phytohormone signalling, the kinase system and defense/stress response revealed five expression patterns, which are compatible with changes in major cellular events during pollen development and germination. A comparison of pollen transcriptomes between rice and Arabidopsis revealed that 56.6% of the rice pollen preferential genes had homologs in Arabidopsis genome, but 63.4% of these homologs were expressed, with a small proportion being expressed preferentially, in Arabidopsis pollen. Rice and Arabidopsis pollen had non-conservative transcription factors each. These results supply novel insights into the molecular program and key components of the regulatory network regulating pollen development and germination. KEYWORDS: rice (Oryza sativa L.), pollination and fertilization, stigma, molecular functions, signaling, microarray, stress response

Dataset Information

The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen

Publications

The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen.

Similar Datasets

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