Histone methyltransferases SDG33 and SDG34 regulate organ-specific nitrogen responses in tomato

Abstract

Histone posttranslational modifications shape the chromatin landscape of the plant genome and affect gene expression in response to developmental and environmental cues. To date, the role of histone modifications in regulating plant responses to environmental nutrient availability, especially in agriculturally important species, remains largely unknown. We describe the functions of two histone lysine methyltransferases, SET Domain Group 33 (SDG33) and SDG34, in mediating nitrogen (N) responses of shoots and roots in tomato. By comparing the transcriptomes of CRISPR edited tomato lines sdg33 and sdg34 with wild-type plants under N-supplied and N-starved conditions, we uncovered that SDG33 and SDG34 regulate overlapping yet distinct downstream gene targets. In response to N level changes, both SDG33 and SDG34 mediate gene regulation in an organ-specific manner: in roots, SDG33 and SDG34 regulate a gene network including Nitrate Transporter 1.1 (NRT1.1) and Small Auxin Up-regulated RNA (SAUR) genes. In agreement with this, mutations in sdg33 or sdg34 abolish the root growth response triggered by an N-supply; In shoots, SDG33 and SDG34 affect the expression of photosynthesis genes and photosynthetic parameters in response to N. Our analysis thus revealed that SDG33 and SDG34 regulate N-responsive gene expression and physiological changes in an organ-specific manner, thus presenting previously unknown candidate genes as targets for selection and engineering to improve N uptake and usage in crop plants.

Recent Advances in Studying the Regulation of Fruit Ripening in Tomato Using Genetic Engineering Approaches

“…Mutants heterozygous for these genes exhibited parthenocarpic fruits. The function of other histone lysine methyltransferases SDG33 and SDG34 was revealed in [109]. They were found to regulate the expression of nitrogen-responsive genes and physiological changes in an organ-specific manner.…”

Epigenetic Regulation of Nitrogen Signaling and Adaptation in Plants

“…Altering the expression levels of genes related to N transport, assimilation, and signaling using transgenic approaches can significantly enhance crop yield or NUE [ 31 , 32 , 33 , 34 , 35 ]. Recent studies have highlighted the impact of chromatin regulation, including histone modification and chromatin structure, in modulating the activity of N transporters [ 17 , 23 , 36 ].…”

“…sdg8 mutants have shown lower nitrate acquisition than wild-type plants under high N conditions [ 38 ]. In tomatoes ( Solanum lycopersicum ), the homologs of SDG8 , namely SlSDG33 and SlSDG34 , regulate SlNRT1.1 in an N-dependent manner that is associated with the root response to N treatments [ 36 ] ( Figure 1 ). Moreover, polycomb repressive complex 2 (PRC2), responsible for the addition of methyl groups to H3K27, directly targets and downregulates AtNRT2.1 expression in Arabidopsis [ 6 ].…”

Recent Advances in Studying the Regulation of Fruit Ripening in Tomato

“…Mutants heterozygous for these genes exhibited parthenocarpic fruits. The function of other histone lysine methyltransferases SDG33 and SDG34 was revealed in [48]. They were found to regulate the expression of nitrogen-responsive genes and physiological changes in an organ-specific manner.…”