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Ploidy-dependent changes in the epigenome of symbiotic cells correlate with specific patterns of gene expression

Abstract : Legume plants are able to interact with soil bacteria from the Rhizobiaceae family. This interaction leads to the development of a specialized organ called root nodule. Inside the symbiotic nodule cells, rhizobia are capable to fix atmospheric nitrogen and convert it to ammonia, which is a usable nitrogen source for the plant. In the legume Medicago truncatula the symbiotic cells produce high amounts of Nodule-Specific Cysteine-Rich (NCR) peptides which induce differentiation of the rhizobia into enlarged, polyploid and non-cultivable bacterial cells. NCRs are similar to innate immunity antimicrobial peptides. The NCR gene family is extremely large in Medicago with about 600 genes. The expression analysis of 334 NCR genes in 267 different experimental conditions using the Medicago truncatula Gene Expression Atlas (MtGEA) revealed that all the NCR genes except five are exclusively expressed in nodules. No NCR expression is induced in any other plant organ or in response to biotic, abiotic stress tested or to Nod factors. The NCR genes are activated in consecutive waves during nodule organogenesis, which correlated with a specific spatial localization of their transcripts from the apical to the proximal nodule zones. Moreover, we showed that NCRs are not induced during nodule senescence. According to their Shannon entropy, a metric for tissue specificity, NCR genes are among the most specifically and highest expressed genes in M. truncatula. Thus, NCR gene expression is subject to an extreme tight regulation since they are only activated during nodule organogenesis in the polyploid symbiotic cells. This analysis suggested the involvement of epigenetic regulation of the NCR genes. The formation of the symbiotic cells is driven by endoreduplication and is associated with transcriptional reprogramming. Using sorted nodule nuclei according to their DNA content, we demonstrated that the transcriptional waves correlate with growing ploidy levels and investigated how the epigenome changes during endoreduplication cycles. We studied genome-wide DNA methylation and chromatin accessibility as well as the presence of repressive H3K27me3 and activating H3K9ac histone tail modifications on selected genes. Differential DNA methylation was found only in a small subset of symbiotic nodule-specific genes, including over half of the NCR genes, while in most genes DNA methylation was unaffected by the ploidy levels and was independent of the genes’ active or repressed state. On the other hand, expression of these genes correlated with ploidy-dependent opening of the chromatin and in a subset of tested genes with reduced H3K27me3 levels combined with enhanced H3K9ac levels. Our results suggest that endoreduplication-dependent epigenetic changes contribute to transcriptional reprogramming in differentiation of symbiotic cells.
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https://tel.archives-ouvertes.fr/tel-01707868
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Submitted on : Tuesday, February 13, 2018 - 11:07:05 AM
Last modification on : Monday, February 10, 2020 - 6:13:59 PM
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  • HAL Id : tel-01707868, version 1

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Marianna Nagymihály. Ploidy-dependent changes in the epigenome of symbiotic cells correlate with specific patterns of gene expression. Vegetal Biology. Université Paris-Saclay; University of Szeged (Hongrie), 2017. English. ⟨NNT : 2017SACLS399⟩. ⟨tel-01707868⟩

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