Histone lysine methylations (HLMs) are implicated in control of gene expression in different eukaryotes. However, the role of HLMs in regulating desirable crop traits and the enzymes involved in these modifications are poorly understood.We studied the functions of tomato histone H3 lysine methyltransferases SET Domain Group 33 (SDG33) and SDG34 in biotic and abiotic stress responses. SDG33 and SDG34 gene edited mutants were altered in H3K36 and H3K4 methylations, and expression of genes involved in diverse processes and responses to biotic and abiotic stimuli.The double but not the single mutants show resistance to the fungal pathogen Botrytis cinerea. Interestingly, single mutants were tolerant to drought and the double mutant showed superior tolerance and plant growth consistent with independent and additive functions. Mutants maintained higher water status during drought and improved recovery and survival after lapse of drought.Notably, diminution of H3K4 and H3K36 trimethylation and expression of negative regulators in challenged plants contributes to stress tolerance of the mutants. Mutations in SDG33 and SDG34 are likely to remove predisposition to biotic and abiotic stress by disrupting permissive transcriptional context promoting expression of negative regulatory factors. These allows improvement of stress and pathogen tolerance, without growth trade-offs, through modification of histone epigenetic marks.

Histone lysine methylations (HLMs) are implicated in control of gene expression in different eukaryotes. However, the role of HLMs in regulating desirable crop traits and the enzymes involved in these modifications are poorly understood. We studied the functions of tomato histone H3 lysine methyltransferases Set Domain Group 33 (SDG33) and SDG34 in biotic and abiotic stress responses. SDG33 and SDG34 mutants were altered in H3K36 and H3K4 methylations, and expression of genes involved in diverse processes and responses to biotic and abiotic stimuli. The double but not the single mutants show resistance to the fungal pathogen Botrytis cinerea. Interestingly, single mutants were tolerant to drought and the double mutant showed superior tolerance consistent with independent and additive functions. Mutants maintained higher water status during drought and improved recovery and survival after lapse of drought. Notably, diminution of H3K4 and H3K36 trimethylation and expression of negative regulators in challenged plants contributes to stress tolerance of the mutants. Mutations in SDG33 and SDG34 remove predisposition to biotic and abiotic stress by disrupting permissive transcriptional context promoting expression of negative regulatory factors. These allows improvement of stress and pathogen tolerance through modification of histone epigenetic marks.

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.

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