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Pollination type recognition from a distance in the ovary is revealed by a global transcriptomic analysis.

ABSTRACT: Sexual reproduction in flowering plants involves intimate interactions between the growing pollen tube and the female reproductive structure. These interactions start immediately after pollen landing on the stigma and continue during the pollen tube journey through the style and the ovary. Thus, well before fertilization, genes in the gynoecium are affected by the growing pollen tubes. Genes activated at a distance in the ovary before pollen tubes arrival represent one class of such genes. Using a global transcriptomic approach, expression profiles obtained from compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations revealed that these pollinations are perceived differently from a distance in the ovary. As the pollen tubes grew along the style, more and more genes became specific for each pollination type, although even early on when no difference could be observed in pollen tube growth rates, each pollination type already displayed its specific signature. Wounding experiments as well as methyl jasmonate treatment were also conducted to determine if transmitting tissue cell death caused by pollen tube growth in the style could also activate gene expression at distance in the ovary. Our data suggest that pollen tube growth in the style is at least partially perceived as a wounding aggression, and that a SI pollination is more akin to a wound response than the other pollination type tested, suggesting similarities in the signaling pathways controlling pollen recognition and stress responses. More importantly, our transcriptomic analysis reveals a highly specific recognition of various pollination types that is relayed from a distance to the ovary ahead of fertilization.

ORGANISM(S): Solanum chacoense

PROVIDER: GSE21957 | GEO | 2010/05/26

SECONDARY ACCESSION(S): PRJNA126761

REPOSITORIES: GEO

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Project description:Sexual reproduction in flowering plants involves intimate interactions between the growing pollen tube and the female reproductive structure. These interactions start immediately after pollen landing on the stigma and continue during the pollen tube journey through the style and the ovary. Thus, well before fertilization, genes in the gynoecium are affected by the growing pollen tubes. Genes activated at a distance in the ovary before pollen tubes arrival represent one class of such genes. Using a global transcriptomic approach, expression profiles obtained from compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations revealed that these pollinations are perceived differently from a distance in the ovary. As the pollen tubes grew along the style, more and more genes became specific for each pollination type, although even early on when no difference could be observed in pollen tube growth rates, each pollination type already displayed its specific signature. Wounding experiments as well as methyl jasmonate treatment were also conducted to determine if transmitting tissue cell death caused by pollen tube growth in the style could also activate gene expression at distance in the ovary. Our data suggest that pollen tube growth in the style is at least partially perceived as a wounding aggression, and that a SI pollination is more akin to a wound response than the other pollination type tested, suggesting similarities in the signaling pathways controlling pollen recognition and stress responses. More importantly, our transcriptomic analysis reveals a highly specific recognition of various pollination types that is relayed from a distance to the ovary ahead of fertilization. To determine on a more global scale if interorgan communication during pollen-pistil interactions is a widespread phenomenon and does not only involve few specialized genes, we used a 7.7K cDNA microarray comprising ~6500 ovule-derived unigenes in duplicata from Solanum chacoense, a self-incompatible wild potato species (Germain et al., 2005), to conduct gene expression analyses through cDNA microarray hybridizations. Profiles obtained from compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations as well as from wounding treatments were all analyzed using the same minimal expression level critera (p < 0.05, fold change ≥± 1.5). Four independent biological replicates were produced from each time points. Ovules were collected at 6, 24 and 48 hours after each treatment and used for RNA extraction and probe preparation . compatible (SC), incompatible (SI), semi-compatible (SeC) and interspecific (IS) pollinations as well as from wounding treatments mRNA preparations were individually hybridized against unpollinated ovule mRNAs . All data was substracted from the touch control. Althought Methanol treated ovules RNA were hybridized against unpollinated ovule mRNAs from plant in closed chamber. To estimate reproducibility and to produce control data for statistical analysis, a large number of unfertilized ovules were isolated and separated between seven independent control groups. RNA from randomly selected pairs of control was hybridized on six microarrays.

Project description:Background: Tomato (Solanum lycopersicum) self-compatibility (SC) is defined as self-pollen tubes that can penetrate their own stigma, elongate in the style and fertilize their own ovules. Self-incompatibility (SI) is defined as self-pollen tubes that are prevented from developing in the style. To determine the influence of gene expression on style self-pollination, a transcriptome-wide comparative analysis of SC and SI tomato unpollinated/pollinated styles was performed using RNA-sequencing (RNA-seq) data. Results: Transcriptome profiles of 24-h unpollination (UP) and self-pollination (P) styles from SC and SI tomato species were generated using high-throughput next generation sequencing. From the comparison of SC self-pollinated and unpollinated styles, 1341 differentially expressed genes (DEGs) were identified, of which 753 were downregulated and 588 were upregulated. From the comparison of SI self-pollinated and unpollinated styles, 804 DEGs were identified, of which 215 were downregulated and 589 were upregulated. Nine gene ontology (GO) terms were enriched significantly in SC and 78 GO terms were enriched significantly in SI. A total of 105 enriched Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were identified in SC and 80 enriched KEGG pathways were identified in SI, among which “Cysteine and methionine metabolism pathway” and “Plant hormone signal transduction pathway” were significantly enriched in SI. Conclusions: This study is the first global transcriptome-wide comparative analysis of SC and SI tomato unpollinated/pollinated styles. Advanced bioinformatic analysis of DEGs uncovered the pathways of “Cysteine and methionine metabolism” and “Plant hormone signal transduction”, which are likely to play important roles in the control of pollen tubes growth in SI species. 24-h unpollination (UP) and self-pollination (P) styles mRNA profiles from SC and SI tomato species were generated by deep sequencing, in triplicate, using Illumina Hiseq 2500 platform.

Project description:Gametophytic self-incompatibility is the primary cause of low fruit set in almond. The mechanism of recognition that determines whether the gametophyte is successfully fertilized between pollen tube SCF (F-box-SSK1-Cul1-Rbx1) protein and pistil S-RNase protein during fertilization is unclear. In this study, the pistils of two almond cultivars 'Wanfeng' and 'Nonpareil' were used as the experimental materials after selfing- and nonselfing/cross-pollination, and pistils from the stamen-removed flowers were used as controls. We used fluorescence microscopy to observe the development of pollen tubes after pollination and 4-dimensional label-free quantitation (4D-LFQ) to detect the protein expression profiles of 'Wanfeng' and 'Nonpareil' pistils and in controls. The results showed that it took 24-36 h for the development of the pollen tube to 1/3 of the pistil, and a total of 7684 differentially accumulated proteins (DAPs) were identified in the pistil after pollinating 36 h, of which 7022 were quantifiable. The up- and down-regulation of the 12 differential protein expressions identified by parallel reaction monitoring (PRM) was the same as that identified by 4D-LFQ, with an average fold-change difference of 14.34%, a maximum of 31.37% and a minimum of 3.68%. Bioinformatics analysis based on the function of the differential proteins, including classification, enrichment, and clustering, identified RNA polymerases (4 DAPs), autophagy (3 DAPs), oxidative phosphorylation (3 DAPs), and homologous recombination (2 DAPs) pathways associated with the self-incompatibility process. The interaction between the serine/threonine kinase (MARK2) protein E3 ubiquitin ligase and the microtubule protein component microtubule-associated protein tau (MAPT/ACT) was found using the STRING database, which demonstrated the involvement of the MARK2 protein in the reaction of pollen tube recognition the nonself- and the self-S-RNase protein. It provides a new way to reveal the mechanism by which almond pollen tubes recognize the self and nonself S-RNase enzyme protein.

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Pollination type recognition from a distance in the ovary is revealed by a global transcriptomic analysis.

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