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. 2018 Aug 29:9:1228.
doi: 10.3389/fpls.2018.01228. eCollection 2018.

BABA-Primed Histone Modifications in Potato for Intergenerational Resistance to Phytophthora infestans

Barbara Meller  1 , Daniel Kuźnicki  1 , Magdalena Arasimowicz-Jelonek  2 , Joanna Deckert  2 , Jolanta Floryszak-Wieczorek  1
Affiliations

BABA-Primed Histone Modifications in Potato for Intergenerational Resistance to Phytophthora infestans

Barbara Meller et al. Front Plant Sci. .

Abstract

In this paper we analyzed β-aminobutyric acid (BABA)-primed epigenetic adjustment of potato cv. "Sarpo Mira" to Phytophthora infestans. The first stress-free generation of the potato genotype obtained from BABA-primed parent plants via tubers and seeds showed pronounced resistance to the pathogen, which was tuned with the transcriptional memory of SA-responsive genes. During the early priming phase before the triggering stress, we found robust bistable deposition of histone marks (H3K4me2 and H3K27me3) on the NPR1 (Non-expressor of PR genes) and the SNI1 gene (Suppressor of NPR1, Inducible), in which transcription antagonized silencing. Switchable chromatin states of these adverse systemic acquired resistance (SAR) regulators probably reprogrammed responsiveness of the PR1 and PR2 genes and contributed to stress imprinting. The elevated levels of heritable H3K4me2 tag in the absence of transcription on SA-dependent genes in BABA-primed (F0) and its vegetative and generative progeny (F1) before pathogen challenge provided evidence for the epigenetic mark for intergenerational memory in potato. Moreover, our study revealed that histone acetylation was not critical for maintaining BABA-primed defense information until the plants were triggered with the virulent pathogen when rapid and boosted PRs gene expression probably required histone acetyltransferase (HAT) activity both in F0 and F1 progeny.

Keywords: histone modifications; intergenerational SAR; late blight; potato leaves; priming.

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Figures

FIGURE 1
FIGURE 1
Intergenerational resistance in potato progeny unprimed and BABA-primed to P. infestans. Schematic representation of the experimental design (A); the parental line of “Sarpo Mira” potato genotype (F0) was treated once with 5 mM BABA (B0). The progeny (F1) grown from tubers or seeds were not again treated with BABA, but only inoculated with P. infestans - at the stage of 10 compound leaves. Abbreviations mean: the parental F0 line BABA-primed – B0, the offspring of primed plants of the vegetative F1 line – BV, and the generative F1 line – BG. Three days after BABA-exposure or water treatment (C0) potato leaves were challenged with P. infestans and disease development was assayed at day 5 after P. infestans inoculation (dpi). BABA-induced resistance against P. infestans in the parental (F0) line (B), intergenerational resistance in the vegetative F1 progeny (C), and in the generative F1 progeny (D). Disease index is based on a 1–4 point scale, which represents the percentage of leaf area covered by late blight symptoms. Values represent means of at least three independent experiments, each with at least three biological replicates. Asterisks indicate values that differ significantly from unprimed (water treated) or unprimed and P. infestans inoculated potato leaves at P < 0.05 (∗), respectively.
FIGURE 2
FIGURE 2
Treatment with BABA reprograms SA-dependent gene transcription. The RT-qPCR analysis of PR1 and PR2 gene expression in BABA primed leaves of potato plants followed by challenge inoculation with P. infestans (at 72 h after BABA treatment) in parental line F0 (A,B). Analyses were performed at 0–48 h after 5 mM BABA exposure and 1–48 hpi after challenge inoculation. Transcriptional priming of PR1 and PR2 gene expression after P. infestans inoculation in the offspring of BABA-primed F1- vegetative line (C), and F1- generative line (D). Light columns refer to unprimed, while dark columns - to primed plant progeny. Values represent means of data ± SD of at least three independent experiments. Asterisks indicate values that differ significantly from unprimed (water treated) or unprimed and P. infestans inoculated potato leaves at P < 0.05 (∗), respectively.
FIGURE 3
FIGURE 3
Priming for defense is supported by enhanced expression of both H3, H4, and CAF-1 histone chaperon genes in F0 potato progeny. The qRT-PCR analysis of H3 (A), H4 (B), and CAF1 (C) gene expression in BABA-primed leaves of potato plants followed by challenge inoculation with P. infestans (at 72 h after BABA treatment). Analyses were performed at 0–48 h after 5 mM BABA exposure (white background) and 1–48 hpi after challenge inoculation (gray background). Light columns refer to unprimed, while dark columns – to primed plants. Values represent means of data ± SD of at least three independent experiments. Asterisks indicate values that differ significantly from unprimed (water treated) or unprimed and P. infestans inoculated potato leaves at P < 0.05 (∗), respectively.
FIGURE 4
FIGURE 4
Expression patterns of histone acetylation and deacetylation upon exposure to BABA and biotic stress. Transcriptional analysis of HDAC (A) and HAT (B) gene expression in BABA-primed leaves of potato plants followed by challenge inoculation with P. infestans (at 72 h after BABA treatment). Analyses were performed at 0–48 h after 5 mM BABA exposure (white background) and 1–48 hpi after challenge inoculation (gray background). Light columns refer to unprimed, while dark columns - to primed plants. Values represent means of data ± SD of at least three independent experiments. Asterisks indicate values that differ significantly from unprimed (water treated) or unprimed and P. infestans inoculated potato leaves at P < 0.05 (∗), respectively.
FIGURE 5
FIGURE 5
Histone lysine methyltransferases and demethylase are required for BABA-triggered immunity. Transcription changes in TrxG, SUVH4, and JMJ706 gene expression in BABA-primed leaves of F0 potato plants followed by challenge inoculation with P. infestans (A). Analyses were performed at 1–48 h after 5 mM BABA exposure (white background) and 1–48 hpi after challenge inoculation (gray background). Transcriptional priming of TrxG, SUVH4, and JMJ706 gene expression after P. infestans inoculation in the offspring of BABA-primed F1- vegetative line (B), and F1- generative line (C). Light columns refer to unprimed, while dark columns - to primed plants progeny. Values represent means of data ± SD of at least three independent experiments. Asterisks indicate values that differ significantly from unprimed (water treated) or unprimed and P. infestans inoculated potato leaves at P < 0.05 (∗), respectively.
FIGURE 6
FIGURE 6
Switchable deposition of chromatin marks on the NPR1 and SNI1 gene, in which transcription antagonized silencing. Time-dependent H3 methylation profiles on NPR1 (A) and SNI1 (B) and their transcript levels (C) in the prime state before the triggering stress. ChIP-qPCR and RT-qPCR analysis of NPR1 and SNI1 gene expression were performed at 3, 24, 48, and 72 h after 5 mM BABA treatment. Each experiment was repeated three times and the data are presented as percentages of input DNA. Asterisks indicate values that differ significantly from unprimed (water treated) potato leaves at P < 0.05 (∗).
FIGURE 7
FIGURE 7
Epigenetic marks on SA-dependent genes in response to BABA-priming. Distribution levels of H3K4me2 and H3K9me3 on the gene body region of WRKY1 (A), PR1 (B) and PR2 (C) at the stage before the second challenge. ChIP-qPCR analyses were performed after 5 mM BABA (BABA-primed) or water treatment (unprimed), in the parental line (F0) and its descendants (F1) derived from tubers (F1/V) or seeds (F1/G). Each experiment was repeated three times and the data are presented as percentages of input DNA. Asterisks indicate values that differ significantly from unprimed (water treated) potato leaves at P < 0.05 (∗).
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