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Plants thriving in desert environments are suitable for studying mechanisms for plant survival under extreme seasonal climate variation. We studied epigenetic mechanisms underlying seasonal growth cycles in the desert plant Zygophyllum dumosum Boiss., which was previously shown to be deficient in repressive markers of di-methyl and tri-methyl H3K9 and their association with factors regulating basic cell functions. We showed a contingent association between rainfall and seasonal growth and the epigenetic marker of dimethyl H3K4, which disappears upon entry into the dry season and the acquisition of a dormant state. DNA methylation is not affected by a lack of H3K9 di-methyl and tri-methyl. Changes in methylation can occur between the wet and dry season. Proteome analysis of acid soluble fractions revealed an extensive reduction in ribosomal proteins and in proteins involved in chloroplasts and mitochondrial activities during the dry seasons concomitantly with up-regulation of molecular chaperone HSPs. Our results highlight mechanisms underlying Z. dumosum adaptation to seasonal climate variation. Particularly, summer dormancy is associated with a loss of the permissive epigenetic marker dimethyl H3K4, which might facilitate genome compaction concomitantly with a significant reduction in proteins involved in basic cell functions. HSP chaperones might safeguard the integrity of cell components.