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Histone methyltransferases SlSDG33 and SlSDG34 mediate organ-specific nitrogen responses in tomato

ABSTRACT: Histone posttranslational modifications play an important role in regulating plant responses to environmental cues, however, few studies have focused on the role of histone lysine methylation in regulating plant responses to nutrient availability, especially in agriculturally important species. Here, we describe the functions of two paralogous histone lysine methyltransferases, SET Domain Group 33 (SDG33) and SDG34, in mediating nitrogen responses in tomato through genetic and transcriptome analyses. Our transcriptome analysis comparing tomato lines demonstrated that SDG33 and SDG34 have overlapping yet distinctly regulated targets in tomato. Importantly, both SDG33 and SDG34 mediate gene regulation in response to changes in nitrogen level, with organ specificity. In roots, SDG33 and SDG34 are required for the regulation of a gene network that includes nitrate transporter NRT1.1, as well as auxin responsive SAUR genes. Consistently, mutations in sdg33 or sdg34 abolish the root growth response to N. In shoots, SDG33 and SDG34 affect the expression of photosynthesis genes and chlorophyll a/b ratio in response to nitrogen. Overall, we show that SDG33 and SDG34 regulate nitrogen responsive gene expression and hence physiological responses to nitrogen nutrients in an organ specific manner in the roots and shoots.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE195546 | GEO | 2022/08/01

REPOSITORIES: GEO

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Project description:In plants, environmental stimuli trigger rapid transcriptional reprogramming of relevant gene suites. Regulation occurs down to the local chromatin landscape of the genes, and while epigenetic modifications proceed in a manner dependent on specific organ and tissue contexts, detailed investigations at this level remain limited. To better understand the organ specificity of dynamic chromatin modifications in response to external signals, we treated nitrogen-limited tomato seedlings with a supply of nitrate and measured the genome-wide changes of four histone marks, the permissive histone marks H3K27ac, H3K4me3, and H3K36me3 and repressive mark H3K27me3, in shoots and roots separately. We observed dynamic histone acetylation and methylation events which are largely organ-specific in scope at functionally relevant gene loci. Integration of transcriptomic and epigenomic datasets generated from the same tissue samples revealed largely syngenetic relations between changes in transcript levels and histone modifications, with the exception of H3K27me3 where an increased level at genes up-regulated in response to nitrate supply is observed in only the shoots. This non-canonical pattern of H3K27me3 deposition could possibly function to prevent over-expression of certain activated genes. To study the determinant roles of histone code in predicting gene regulation at the genome-wide level we applied a machine learning approach. While gene regulation could be best predicted using all four histone marks together, we observed different rules regarding the importance of individual histone marks between shoots, where H3K36me3 is the most successful mark in predicting gene activation and repression events, and the roots, where H3K4me3 is the strongest individual predictor. In summary, our integrated study substantiates a view that during plant environmental responses, the histone code dynamics that govern relationships between chromatin modification and gene regulation are highly dependent on tissue specific contexts.

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Histone methyltransferases SlSDG33 and SlSDG34 mediate organ-specific nitrogen responses in tomato

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