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Ploidy-specific transcriptomes shed light on the heterogeneous identity and metabolism of developing pericarp cells

ABSTRACT: Endoreduplication, during which cells increase their DNA content through successive rounds of full genome replication without cell division, is the major source of endopolyploidy in higher plants. Endoreduplication plays pivotal roles in plant growth and development and is associated with the activation of specific transcriptional programs that are characteristic to each cell type, thereby defining their identity. In plants, endoreduplication is found in numerous organs and cell types and especially in agronomically valuable ones, such as the fleshy fruit (pericarp) of tomato presenting high ploidy levels. We used the tomato pericarp tissue as a model system to explore the transcriptomes associated with endoreduplication progression during fruit growth. We confirmed that expression globally scales with ploidy level and identified sets of genes differentially expressed when comparing ploidy levels at a specific developmental stage. We found that non-endoreduplicated cells are defined by cell division state and cuticle synthesis while endoreduplicated cells are mainly defined by their metabolic activity changing rapidly over time. By combining this dataset with publicly available spatiotemporal pericarp expression data, we proposed a map describing the distribution of ploidy levels within the pericarp. These transcriptome-based predictions were validated by quantifying ploidy levels within the pericarp tissue. This in situ ploidy quantification revealed the dynamic progression of endoreduplication and its cell layer specificity during early fruit development. In summary, the study sheds light on the complex relationship between endoreduplication, cell differentiation, and gene expression patterns in the tomato pericarp.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE245923 | GEO | 2024/02/23

REPOSITORIES: GEO

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Project description:Fruits of transgenic tomato (Solanum lycopersicum) plants engineered with ripening-induced, yeast S-adenosylmethionine decarboxylase (ySAMdc) gene, accumulate the higher polyamines spermidine (Spd) and spermine (Spm) and demonstrate ameliorated phytonutrient content, juice quality, and prolonged vine life. Enhanced nitrogen-carbon interactions were revealed by comprehensive Nuclear Magnetic Resonance (NMR) spectroscopy-based metabolite profiling of the transgenics, suggesting that Spd and Spm are perceived as nitrogenous metabolites by the fruit cells (Mattoo et al., 2006). The recent work by our colleagues identified the effects of Spd/Spm accumulation on various functional classes of tomato genes affected during ripening by probing 1522 ESTs on a custom-made array (Srivastava et al., 2007). In this study we monitored alterations of genome-wide transcriptional patterns in pericarp of Spd/Spm-accumulating tomatoes by means of direct comparison with azygous controls using DNA-microarray technology. Consistent with the ySAMdc expression pattern, very minor transcriptional alterations were detected in mature green developmental stage. For both breaker and red stages, large mutual and unique gene sets displayed altered levels of transcript. Ontological term analysis of up- and down-regulated transcript groups revealed processes in cell metabolism that are regulated by increased levels of Spd/Spm in ripening tomato fruits. These processes mainly involve carbohydrate and amino acids metabolism and protein synthesis. Additionally, transcript levels of representative genes encoding structural enzymes for related biosynthetic pathways show strong relationship to specific metabolites that were identified as regulated in Spd/Spm-accumulating transgenics. Plants of both genotypes were grown in randomized blocks (3 blockes 8-10 plants each). At each of 3 developmental stages (mature green, breaker and pink-red) a single fruit was harvested from a randomly chosen plant of each genotype within each block. In each harvest different plants in each block were taken to represent each genotype. Following harvest, equal pericarp samples were cut from the equator region of each fruit. These samples were pooled according to genotype prior to RNA extraction, allowing equal representation of each block in the final sample. A total of 3 harvests taken from each genotype were eventually analyzed– each harvest representing a biological repeat.

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Ploidy-specific transcriptomes shed light on the heterogeneous identity and metabolism of developing pericarp cells

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