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Histone posttranslational modifications rather than DNA methylation underlie gene reprogramming in pollination-dependent and pollination-independent fruit set in tomato.

ABSTRACT: Fruit formation comprises a series of developmental transitions among which the fruit set process is essential in determining crop yield. Yet, our understanding of the epigenetic landscape remodelling associated with the flower-to-fruit transition remains poor. We investigated the epigenetic and transcriptomic reprogramming underlying pollination-dependent and auxin-induced flower-to-fruit transitions in the tomato (Solanum lycopersicum) using combined genomewide transcriptomic profiling, global ChIP-sequencing and whole genomic DNA bisulfite sequencing (WGBS). Variation in the expression of the overwhelming majority of genes was associated with change in histone mark distribution, whereas changes in DNA methylation concerned a minor fraction of differentially expressed genes. Reprogramming of genes involved in processes instrumental to fruit set correlated with their H3K9ac or H3K4me3 marking status but not with changes in cytosine methylation, indicating that histone posttranslational modifications rather than DNA methylation are associated with the remodelling of the epigenetic landscape underpinning the flower-to-fruit transition. Given the prominent role previously assigned to DNA methylation in reprogramming key genes of the transition to ripening, the outcome of the present study supports the idea that the two main developmental transitions in fleshy fruit and the underlying transcriptomic reprogramming are associated with different modes of epigenetic regulations.

SUBMITTER: Hu G

PROVIDER: S-EPMC7821339 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Histone posttranslational modifications rather than DNA methylation underlie gene reprogramming in pollination-dependent and pollination-independent fruit set in tomato.

Hu Guojian G Huang Baowen B Wang Keke K Frasse Pierre P Maza Elie E Djari Anis A Benhamed Moussa M Gallusci Philippe P Li Zhengguo Z Zouine Mohamed M Bouzayen Mondher M

The New phytologist 20201027 2

Fruit formation comprises a series of developmental transitions among which the fruit set process is essential in determining crop yield. Yet, our understanding of the epigenetic landscape remodelling associated with the flower-to-fruit transition remains poor. We investigated the epigenetic and transcriptomic reprogramming underlying pollination-dependent and auxin-induced flower-to-fruit transitions in the tomato (Solanum lycopersicum) using combined genomewide transcriptomic profiling, global ...[more]

PMID: 32875585

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Project description:In flowering plants, pollination, pollen tube growth, and fertilization are regarded as the first hierarchical processes of producing offspring. However, their independent contributions to fruit set and development remain unclear. In this study, we examined the effect of three different types of pollen, intact pollen (IP), soft X-ray-treated pollen (XP) and dead pollen (DP), on pollen tube growth, fruit development and gene expression in "Micro-Tom" tomato. Normal germination and pollen tube growth were observed in flowers pollinated with IP; pollen tubes started to penetrate the ovary at 9 h after pollination, and full penetration was achieved after 24 h (IP24h), resulting in ~94% fruit set. At earlier time points (3 and 6 h after pollination; IP3h and IP6h, respectively), pollen tubes were still in the style, and no fruit set was observed. Flowers pollinated with XP followed by style removal after 24 h (XP24h) also demonstrated regular pollen tubes and produced parthenocarpic fruits with ~78% fruit set. As expected, DP could not germinate and failed to activate fruit formation. Histological analysis of the ovary at 2 days after anthesis (DAA) revealed that IP and XP comparably increased cell layers and cell size; however, mature fruits derived from XP were significantly smaller than those derived from IP. Furthermore, there was a high correlation between seed number and fruit size in fruit derived from IP, illustrating the crucial role of fertilization in the latter stages of fruit development. RNA-Seq analysis was carried out in ovaries derived from IP6h, IP24h, XP24h and DP24h in comparison with emasculated and unpollinated ovaries (E) at 2 DAA. The results revealed that 65 genes were differentially expressed (DE) in IP6h ovaries; these genes were closely associated with cell cycle dormancy release pathways. Conversely, 5062 and 4383 DE genes were obtained in IP24h and XP24h ovaries, respectively; top enriched terms were mostly associated with cell division and expansion in addition to the 'plant hormone signal transduction' pathway. These findings indicate that full penetration of pollen tubes can initiate fruit set and development independently of fertilization, most likely by activating the expression of genes regulating cell division and expansion.

Project description:UNLABELLED:Epigenetic gene regulation has emerged as a major mechanism for gene regulation in all eukaryotes. Histones are small, basic proteins that constitute the major protein component of chromatin, and posttranslational modifications (PTM) of histones are essential for epigenetic gene regulation. The different combinations of histone PTM form the histone code for an organism, marking functional units of chromatin that recruit macromolecular complexes that govern chromatin structure and regulate gene expression. To characterize the repertoire of Toxoplasma gondii histone PTM, we enriched histones using standard acid extraction protocols and analyzed them with several complementary middle-down and bottom-up proteomic approaches with the high-resolution Orbitrap mass spectrometer using collision-induced dissociation (CID), higher-energy collisional dissociation (HCD), and/or electron transfer dissociation (ETD) fragmentation. We identified 249 peptides with unique combinations of PTM that comprise the T. gondii histone code. T. gondii histones share a high degree of sequence conservation with human histones, and many modifications are conserved between these species. In addition, T. gondii histones have unique modifications not previously identified in other species. Finally, T. gondii histones are modified by succinylation, propionylation, and formylation, recently described histone PTM that have not previously been identified in parasitic protozoa. The characterization of the T. gondii histone code will facilitate in-depth analysis of how epigenetic regulation affects gene expression in pathogenic apicomplexan parasites and identify a new model system for elucidating the biological functions of novel histone PTM. IMPORTANCE:Toxoplasma gondii is among the most common parasitic infections in humans. The transition between the different stages of the T. gondii life cycle are essential for parasite virulence and survival. These differentiation events are accompanied by significant changes in gene expression, and the control mechanisms for these transitions have not been elucidated. Important mechanisms that are involved in the control of gene expression are the epigenetic modifications that have been identified in several eukaryotes. T. gondii has a full complement of histone-modifying enzymes, histones, and variants. In this paper, we identify over a hundred PTM and a full repertoire of PTM combinations for T. gondii histones, providing the first large-scale characterization of the T. gondii histone code and an essential initial step for understanding how epigenetic modifications affect gene expression and other processes in this organism.

Dataset Information

Histone posttranslational modifications rather than DNA methylation underlie gene reprogramming in pollination-dependent and pollination-independent fruit set in tomato.

Publications

Histone posttranslational modifications rather than DNA methylation underlie gene reprogramming in pollination-dependent and pollination-independent fruit set in tomato.

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