Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response

Abstract

Priming of defence genes for amplified response to secondary stress can be induced by application of the plant hormone salicylic acid or its synthetic analogue acibenzolar S-methyl. In this study, we show that treatment with acibenzolar S-methyl or pathogen infection of distal leaves induce chromatin modifications on defence gene promoters that are normally found on active genes, although the genes remain inactive. This is associated with an amplified gene response on challenge exposure to stress. Mutant analyses reveal a tight correlation between histone modification patterns and gene priming. The data suggest a histone memory for information storage in the plant stress response.

A Genome-Wide Chronological Study of Gene Expression and Two Histone Modifications, H3K4me3 and H3K9ac, during Developmental Leaf Senescence

“…2C). A cooperative interaction between H3K4me3 and H3K9ac modifications is suggested by the high degree of colocalization, which has been noted previously (Kim et al, 2008(Kim et al, , 2012Anzola et al, 2010;Jaskiewicz et al, 2011;Roudier et al, 2011;Malapeira et al, 2012).…”

Multiple exposures to drought 'train' transcriptional responses in Arabidopsis

“…However, maintenance of these stress-induced chromatin changes after the removal of the initial signal has not been reported, except for some plant defence-response genes. H3K4me3 accumulates on the nucleosomes of defence-response genes before their induction by a pathogen attack 33 or upon chemical priming 6,7 . Priming leads to an increased systemic immunity response on subsequent treatments and stronger transcriptional induction of response-related genes relative to non-exposed plants 6,7,34,35 .…”

“…H3K4me3 accumulates on the nucleosomes of defence-response genes before their induction by a pathogen attack 33 or upon chemical priming 6,7 . Priming leads to an increased systemic immunity response on subsequent treatments and stronger transcriptional induction of response-related genes relative to non-exposed plants 6,7,34,35 . Elevated H3K4me3 levels in the primed state and the subsequent stronger transcriptional response from primed defence genes resembles the transcriptional memory described here.…”

“…Elevated H3K4me3 levels in the primed state and the subsequent stronger transcriptional response from primed defence genes resembles the transcriptional memory described here. A major difference, however, is that priming establishes H3K4me3 before activation of transcription from defence genes 6,7 . As such, the H3K4me3 does not occur as a mark retained from a previously active state (as with trainable genes) but, rather, appears as a 'preparatory' mark for future inductions 33 .…”

“…Altered responses to consecutive stresses imply that plants exercise a form of 'stress memory' 4 . For example, tobacco plants pre-exposed to methyl jasmonate increased nicotine pools 2 days earlier when exposed again as compared with plants without previous exposure 5 ; Pretreatment of plants with salicylic acid or its synthetic analogue, benzothiadiazole S-methylester, resulted in increased transcription from a subset of genes upon a subsequent stress 6,7 . Some stress memory effects could be perpetuated to the next generation, as observed with flagellin or ultraviolet radiation 8 treatments.…”