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.

Figure 1

Transcript abundance and histone modifications after priming and potentiated activation of three WRKY transcription factor genes. Plants were treated with 100 μM BTH or wettable powder (control). After 72 h, half of the plants were stressed by infiltrating water into their leaves. After 3 h, leaves were collected and RNA and chromatin were isolated. (A–C) Transcript abundance as determined by RT–qPCR. Data are standardized for abundance of the Actin2 transcript. (D–F) H3K4 methylation (me) and histone acetylation (ac) on the gene promoters. Data are standardized for histone modification levels in the absence of inducer and stress treatment. Each data point is based on four independent replicates. Error bars indicate s.e.m. values. BTH, acibenzolar S-methyl; RT–qPCR, reverse transcriptase–quantitative PCR.

Figure 2

Pathogen-induced priming for augmented gene activation. (A) Lower leaves were infected with Psm. After 72 h, upper leaves were left untreated or stressed by the infiltration of water. After 3 h, upper leaves were collected and analysed for transcript abundance. Data are standardized for abundance of the Actin2 transcript. (B) Histone modifications in upper leaves 72 h after infection of lower leaves with Psm. Data are standardized for histone modification levels in the absence of pathogen infection. Each data point is based on at least three independent replicates. Error bars indicate s.e.m. values. ac, acetylation; me, methylation; Psm, Pseudomonas syringae pv. maculicola.

Figure 3

Potentiated gene activation and H3K4 trimethylation in npr1, sni1, cpr1 and edr1 mutants. Wild-type and mutant plants were treated with 100 μM BTH or wettable powder (control). After 72 h, some of the plants were additionally stressed by infiltrating water into their leaves. Three hours later, leaves were collected and RNA and chromatin were extracted. (A–C) Transcript abundance in wild-type and mutant plants as determined by RT–qPCR. Data are standardized for abundance of the Actin2 transcript. (D–F) Histone H3 Lys 4 trimethylation on gene promoters in wild-type and mutant plants. Data are standardized for wild-type histone modification levels in the absence of BTH. Data represent at least three independent replicates. Error bars indicate s.e.m. values. BTH, acibenzolar S-methyl; RT–qPCR, reverse transcriptase–quantitative PCR; wt, wild type.