JMJ704 positively regulates rice defense response against Xanthomonas oryzae pv. oryzae infection via reducing H3K4me2/3 associated with negative disease resistance regulators
© Hou et al. 2015
Received: 6 September 2015
Accepted: 3 December 2015
Published: 9 December 2015
Jumonji C (JmjC) domain-containing proteins are a group of functionally conserved histone lysine demethylases in Eukaryotes. Growing evidences have shown that JmjCs epigenetically regulate various biological processes in plants. However, their roles in plant biotic stress, especially in rice bacterial blight resistance have been barely studied so far.
In this study, we found that the global di- and tri-methylation levels on multiple lysine sites of histone three were dramatically altered after being infected by bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Xoo). Xoo infection induced the transcription of 15 JmjCs, suggesting these JmjCs are involved in rice bacterial blight defense. Further functional characterization of JmjC mutants revealed that JMJ704 is a positive regulator of rice bacterial blight resistance as the jmj704 became more susceptible to Xoo than the wild-type. In jmj704, the H3K4me2/3 levels were significantly increased; suggesting JMJ704 may be involved in H3K4me2/3 demethylation. Moreover, JMJ704 suppressed the transcription of the rice defense negative regulator genes, such as NRR, OsWRKY62 and Os-11N3, by reducing the activation marks H3K4me2/3 on them.
JMJ704 may be a universal switch controlling multiple genes of the bacterial blight resistance pathway. JMJ704 positively regulates rice defense by epigenetically suppressing master negative defense regulators, presenting a novel mechanism distinct from its homolog JMJ705 which also positively regulates rice defense but via activating positive defense regulators.
KeywordsRice (Oryza sativa L.) Xanthomonas oryzae pv. oryzae JmjC domain-containing demethylase Histone modification
Histone methylation is a very important post-translational modification and plays an essential role in chromatin remodeling, gene transcription and genome stability in eukaryotic cells [1–3]. Mono-, di- or tri-methylation for histone H3 at lysine 4, 9, 27, 36(H3K4me1/me2/me3,H3K9me1/me2/me3,H3K27me1/me2/me3,H3K36me1/me2/me3) has been implicated in epigenetic gene regulation . Generally, H3K4 and H3K36 methylations are associated with actively transcribed genes, whereas methylations of H3K9 and H3K27 have the transcriptional repressing function [4, 5]. Histone lysine methylation can be reversed by histone lysine demethylases (KDMs) . KDMs contain two known evolutionarily conserved types: lysine specific demethylase1 (LSD1)  and histone demethylases featured with the jumonji C (JmjC) domain [8, 9]. LSD1 has been demonstrated to be responsible for H3K4 demethylation . In Arabidopsis, the three homologues LSD1-like 1 (LDL1), LSD1-like 2 (LDL2) and FLOWERING LOCUS D (FLD) were shown to repress FLOWERING LOCUS C (FLC) expression via demethylating mono- and di-methylated H3K4 . FLD is also required to systemic acquired resistance [11, 12]. The JmjC domain-containing histone demethylases are generally conserved in yeast, animal and plant [8, 13]. JmjC proteins preferentially remove di- and tri-methylations in histone lysines through ferrous ion and α-ketoglutaric acid-dependent oxidative reactions . For examples, JHDM1 specifically demethylates H3K36me2 in human and yeast , while Arabidopsis JMJ14, JMJ15 and JMJ18 are H3K4me2/me3 demethylases [14–16]. In rice, there are totally 20 JmjC domain-containing proteins named JMJ701-JMJ720 [17–20]. JMJ701-JMJ720 are classified into five different groups on the basis of the JmjC domain and the overall protein domain architecture, including JmjC domain-containing histone demethylase 2 (JHDM2), JmjC domain-containing 2 (JMJD2), JmjC protein containing AT-rich interaction domain (JARID), JmjC domain only and N-terminal FY-rich_C-terminal FY-rich ( FYRN_FYRC) .
Recently, emerging evidence has shown that JmjCs participate in various aspects of rice developmental processes and response to stresses. In FYRN_FYRC group, JMJ703 was reported to be a H3K4 demethylase. The jmj703 mutant displayed pleiotropic phenotypes such as dwarf, erected leaves, less secondary panicles and smaller grain size. In addition, JMJ703 could repress the retrotransposon activity by demethylating the lysine 4 site of histone 3, which is the main mechanism to maintain the rice genome stability [21, 22]. JMJ706, a JMJD2 group member, was identified as a H3K9 demethylase and involved in the regulation of floral development . Recently, it was found that JMJ705, a H3K27 di- and tri-methylation demethylase was involved in plant defense response to the bacterial blight (BB) disease pathogen (Xanthomonas oryzae pv. oryzae, Xoo) infection. Mutation of JMJ705 reduced rice resistance to Xoo, while overexpression of JMJ705 enhanced rice resistance to Xoo. It was suggested that JMJ705 demethylase activity is subject to the methyl jasmonate induction during the pathogen infection, and the induced JMJ705 may remove H3K27me3 from marked defense-related genes and enhance the rice disease resistance . Interestingly, JMJ705 is not the sole case in which plant immunity to pathogens is subjected to epigenetic regulation. Previous studies have demonstrated that the Arabidopsis (Arabidopsis thaliana) histone H3K36 methyltransferase SET DOMAIN GROUP8 (SDG8) and H3K4 methyltransferase TRITHORAX1 (ATX1) play crucial roles in biotic stress as well. Mutation of SDG8 reduced resistance to the necrotrophic fungal pathogens Alternaria brassicicola and Botrytis cinerea [24, 25], and down-regulated the expression of resistance (R) gene against Pst DC3000 [25, 26]. In atx1 mutant, the salicylic acid (SA)-responsive pathway was suppressed, while the ethylene (ET)/ jasmonic acid (JA) responsive pathway was elevated to against Pst DC3000 infection [25, 27, 28]. The research on JMJ705, SDG8 and ATX1 fully supported the hypothesis that histone demethylation/methylation are involved in plant defense to pathogens.
Bacterial blight (BB) of rice caused by Xoo infection is one of the most devastating diseases for rice production as the yield loss can be up to 50 % . Though many BB resistance genes, such as Xa4, xa5, xa13 and Xa21, have been identified and applied in breeding by single gene introduction or gene pyramiding , the acquired resistance could be soon lost as the pathogen evolves very quickly to overcome the resistance. Therefore, discovery of novel BB resistant genes, especially epigenetic genes controlling the reprogramming of gene transcription, would be of great importance to obtain sustainable BB resistance in rice breeding. In this work, we examined the global level of various histone methylation modifications under Xoo infection. The Xoo infection induced expression patterns indicated that JmjC demethylase genes are involved in BB resistance. Knock-down of JMJ704, a potential H3K4me2/3 demethylase, significantly increased the plant susceptibility to Xoo infection when compared with the wild-type. Meanwhile, several negative master regulators of rice disease resistance, including NRR, OsWRKY62 and Os-11N3, were up-regulated in jmj704, suggesting that JMJ704 positively regulates rice BB resistance via epigenetically suppressing the transcription of negative regulators during the pathogen infection.
The global histone lysine methylation dynamics in response to Xoo infection
The Xoo infection induced expression profile of rice JmjC genes
The characteristics of JmjC genes identified in rice
Known histone substrate
Stem elongation transposon silencing
JmjC domain only
JmjC domain only
JmjC domain only
JmjC domain only
JmjC domain only
JmjC domain only
JmjC domain only
Knock-down of JMJ704 reduced the rice resistance to Xoo infection
Di- and tri-methylation levels of H3K4 were increased in jmj704
JMJ704 regulates the expression of rice BB defense-related genes
To evaluate the effects of JMJ704 mutation on rice gene expression, RNA-seq experiment was performed for the ZH11 and jmj704-1 mutant young seedlings at two weeks after germination using Illumina HiSeqTM 2500 platform. A total of 446 genes were found to be differentially expressed between the mutant and wild-type, including 271 genes which showed over 2 fold up-regulation and 175 genes were down-regulated in jmj704 (|log 2Ratio| ≥1; FDR <0.001) (Additional file 2: Table S1). Among these DEGs (Differentially Expressed Genes), several have been known to be plant defense-related. For examples, NRR (LOC_Os01g03940), OsWRKY62 (LOC_Os09g25070) and Os-11N3 (LOC_Os11g31190) were reported to be negative regulators for Xoo resistance in rice [33–35]. In jmj704, all these three genes were significantly up-regulated which is in accordance to the phenotype that jmj704 became more susceptible to BB.
Gene ontology (GO) analysis of DEGs revealed 8 categories of enriched genes. In particular, category of “response to stress” was significantly enriched for the up-regulated genes (20 of 271; P < 0.05) and down-regulated genes (54 of 175; P < 0.05) (Additional file 3: Table S2). These results suggested that JMJ704 might be a regulator of stress-responsive gene expression. Moreover, pathway analysis also found that DEGs were preferentially involved in metabolic pathway, plant-pathogen interaction and biosynthesis of secondary metabolites (Additional file 4: Figure S2).
qRT-PCR validations of 12 randomly selected genes from the differentially expressed genes in the RNA-seq results
Ratio in RNA-seq (before inoculation)
Fold-change in qRT-PCR (before inoculation)
Fold-change in qRT-PCR (24 h after inoculation)
Negative regulator of disease resistance , expressed protein
OsGH3.3-Probable indole-3-acetic acid-amido synthetase, expressed
nodulin MtN3 family protein, putative, expressed
receptor kinase, putative, expressed
WAX2, putative, expressed
Superfamily of TFs having WRKY and zinc finger domains, expressed
receptor-like protein kinase precursor, putative, expressed
OsWRKY62 - Superfamily of TFs having WRKY and zinc finger domains, expressed
NBS-LRR type disease resistance protein, putative, expressed
disease resistance protein RPM1, putative
nodulin MtN3 family protein, putative, expressed
pathogenesis-related Bet v I family protein, putative, expressed
H3K4me2/3 on NRR, OsWRKY62 and Os-11N3 were increased in jmj704
Histone modifications are extensively involved in the plant disease resistance
Recently, emerging evidences have shown that histone modifications such as H3K4me3, H3K9me2, H3K9ac, H3K23ac, H3K27ac, H3K27me3, and H4ac, may be an important mechanism controlling various biological processes. For instance, the acetylation levels of histone H3K18, H3K27, and H4K5 were found to be significantly elevated in rice when drought stress was applied, while the H3K9 acetylation level remained unchanged . In this study, a survey of the global methylation levels of various lysine sites on histone 3 revealed that the di-and tri-methylation levels of H3K4, H3K9, H3K27 and H3K36 were obviously altered at different time points after Xoo infection, indicating that histone modification play a vital role in plant disease resistance. Indeed, previous reports have demonstrated that H3K4, H3K27 and H3K36 methylations were involved in defense response upon pathogen attack in Arabidopsis and rice [23–28, 37–39]. Loss-of-function of histone methyltransferase SDG8 reduced the Arabidopsis resistance to necrotic fungi pathogen infection. Evidences also showed that SDG8 is involved in the JA/ET signaling pathway . Histone deacetylase HDA19 plays a positive role in Arabidopsis basal defense to pathogens by repressing the transcription factors WRKY38 and WRKY62 . Meanwhile, as a master regulator of disease resistance in Arabidopsis, HDA19 represses the SA biosynthesis and SA-mediated defense to prevent overreaction of the plant when under unnecessary circumstances, thus to assure successful growth and development . In rice, HDT701, a histone H4 deacetylase plays a negative role in plant defense to Magnaporthe oryzae and Xoo. In the rice HDT701 overexpression lines, the global histone H4 acetylation level was reduced and plants became more susceptible to the rice pathogens M. oryzae and Xoo. Further evidence suggested that HDT701 physically binds to and modulates the levels of histone H4 acetylation of pattern recognition receptor (PRR) and defense-related genes, such as MAPK6 and WRKY53 .
Roles of JmjC genes in rice BB resistance
A stress-inducible expression pattern of a gene usually indicates its function in the stress. In this work, we provided the expression profiles of 20 JmjC demethylase genes in response to Xoo infection in rice. Interestingly, 15 JmjC genes could be induced by Xoo, which strongly hinted that they may be involved in plant defense response to BB. On the other hand, it has been clear that JmjC domain-containing demethylases preferentially remove di-methylation and tri-methylation of histone lysines through ferrous ion [Fe ] andα-ketoglutaric acid-dependent oxidative reactions . Given the JmjC gene induced expression profiles and the histone methylation dynamics in the process of Xoo infection, it is rational for us to hypothesize that JmjCs-mediated histone modification plays important roles in rice BB resistance. In 2013, a literature already reported that JMJ705 encoding a JmjC demethylase regulates rice defense response to Xoo by removing histone H3K27 tri-methylation of JA-induced genes, which well supported our speculation. In this study, we, for the first time, reported that JMJ704 positively regulates the rice resistance to Xoo infection, as indicated by the Xoo inoculation assay results that multiple jmj704 lines exhibited increased susceptibility to Xoo infection than the wild-type. Moreover, we found that the global level of H3K4me2/3 in jmj704 was increased when compared with the wild-type, implying that JMJ704 is involved in H3K4me2/3 demethylation. Even though JMJ704 and JMJ705 both play the same positive role in plant defense response, the mechanisms underlying their roles are distinct. JMJ705 activates positive defense related genes by removing the suppressing modification H3K27me3 on them, which finally enhances the plant resistance. Nevertheless, JMJ704 suppresses the transcription of the negative regulator genes by reducing the activation marks H3K4me2/3 on them, but reaches the same goal as JMJ705. Therefore, the JmjCs regulate BB resistance via a dual pathway including up-regulation of positive regulators as well as the down-regulation of negative regulators. Considering the strong Xoo inducible expression pattern that was detected on many other rice JmjCs such as JMJ702, JMJ712, and JMJ716, we believe that these genes may also be potentially involved in the rice BB resistance, which will be explored in our future study. It is also noteworthy that the majority of the Xoo inducible JmjCs were maximally induced at 24 h after induction, this stage would be a key time point for the histone modification regulation in plant disease resistance.
JMJ704-regulated bacterial blight defense pathway in rice
JMJ704 positively regulates rice defense by epigenetically suppressing master negative defense regulators, presenting a novel mechanism distinct from its homolog JMJ705 which also positively regulates rice defense but via activating positive defense regulators. All this data indicates that chromatin remodeling accomplished through histone modifications is a key process in the orchestration of plant biotic stress responses, and histone-modifying enzymes are critical regulators to plant defense to pathogen attack. On the other hand, to figure out the direct target genes of JMJ704 from the DEGs would be of great importance in elucidating the regulatory network in plant disease resistance. High through-put techniques such as ChIP-sequencing will be employed for this purpose in our near future work.
Rice cultivars (Oryza sativa spp japonica) Nipponbare, Zhonghua11 and Hwayoung were used in this study. The T-DNA insertion mutants jmj704-1 (03Z11EQ18) and jmj704-2 (1C-14923) were obtained from the RMD rice mutant database (http://rmd.ncpgr.cn/) [31, 44] and Postech rice mutant database respectively . The insertions in two jmj704 mutants were confirmed by PCR using the primers (F1+ R1+ NTLB5; F2 + R2 + 2707 L) (seen in Additional file 5: Table S3). All the plants were grown in the greenhouse of China National Rice Research Institute. Four-week-old Nipponbare plants were subjected to tissue expression and stress analysis. T-DNA mutants, ZH11 and HY plants in booting-stage were used for Xoo inoculation assay.
Rice bacterial blight inoculation
Chinese Xoo strain (Zhe173) was used for the inoculation assay. Briefly, plants in four-week-old and booting-stage were inoculated with Zhe173 (3 × 108 /ml) by the leaf clipping method in growth chambers (90 % relative humidity, 30/28 °C, 14 h light/10 h dark cycle) . Plant tissues were harvested in the proper time after inoculation, and immediately kept in liquid nitrogen until use. Disease was scored (3 to 5 leaves for each plant) as the percent lesion area (lesion length/leaf length) at 15 days after inoculation. The bacterial growth rate for Zhe173 strain was also analyzed by counting colony-forming units as the previous study .
RNA isolation and quantitative RT-PCR (qRT-PCR)
Total RNA of various tissues was isolated using Trizol (Invitrogen) according to the manufacturer’s manual. Four micrograms of total RNA was reverse transcribed using first strand cDNA synthesis Kit (Toyobo). For real-time quantitative RT-PCR, all the primers used are listed in Additional file 5: Table S3, and an ubiquitin gene was used as an internal control. Quantitative RT-PCR was performed in a total reaction volume of ten microliter (5 μL THUNDERBIRD SYBR® qPCR Mix [Toyobo], 0.5μLcDNA, 0.5μLprimers, and 4μLwater) on the LightCycler 4.80 real-time PCR detection system (Roche). Expression was assessed by evaluating threshold cycle (CT) values. The relative expression level of tested genes was normalized to ubiquitin gene and calculated by the 2-ΔΔCT method . The experiment was performed in technical triplicates.
Histone-enriched proteins were extracted from rice leaves using the sulfuric acid–extraction method as described previously . Briefly, nuclei were isolated from 1 g of rice leaf tissue with buffer containing 50 mM Tris pH8.0, 60 mM KCl, 5 mM MgCl2, 15 mM NaCl, 1 mM CaCl2, 0.25 M sucrose, 0.8 % triton X-100, 2 mM dithiothreitol (DTT) and 2 mM phenylmethylsulfonyl fluoride (PMSF). Then, isolates were incubated in 6 N H2SO4 for 4–6 h at 4 °C and precipitated in 100 % acetone overnight. Lastly, the pellets were washed in acetone and re-suspended in 1X SDS loading buffer.
Western blot analysis
The methylation modification status of histones was analyzed by Western blot. The extracted histone proteins were resolved on 15 % SDS-polyacrylamide gels, and subsequently transferred onto polyvinylidene fluoride fluoropolymer (PVDF) membrane using an electrophoretic blotting system (Bio-Rad). Membrane was blocked with 5 % (w/v) bovine serum albumin followed by incubation with the rabbit polyclonal primary antibodies against histone H3 (ab1791, Abcam), H3K4me2 (07–030, Millipore), H3K4me3 (07–473, Millipore), H3K9me2 (07–441, Millipore), H3K9me3 (07–442, Millipore), H3K27me2 (07–452, Millipore), H3K27me3 (07–449, Millipore), H3K36me2 (ab9049, Abcam), H3K36me3 (ab9050, Abcam) and then a goat anti-rabbit IgG secondary antibody conjugated to horseradish peroxidase (IH-0011, Dingguo). The antibody complexes on the membrane were detected by the enhanced chemilluminescence (Pierce) method. Quantification of the band intensities on the immunoblots was performed using the ImageJ software according to the instructions (http://rsb.info.nih.gov/ij/docs/menus/analyze.html#gels). All the sample intensities were first normalized to the loading control histone 3, and then calculated based on the ratio to set the intensity level of 0 h (Fig. 1) or ZH11 (Fig. 4) samples into 1.
For RNA-seq analysis, 14-day-old seedlings of JMJ704 T-DNA mutant and wild-type plants ZH11 under normal growth conditions were harvested for RNA-seq analysis. RNA samples were extracted using TRIzol according to the manufacturer’s instructions (Invitrogen). cDNA library that was constructed as previously described and sequenced by using Illumina HiSeqTM 2500 platform . Gene expression changes between the samples were analyzed by SOAP aligner/SOAP2 software. For GO analysis of RNA-seq data, we used the GO::TermFinder software to find different expression gene enrichment , and choose P < 0.05 as the cutoff for significant GO terms.
Chromatin immuno-precipitation (ChIP) and ChIP-PCR
ChIP was performed as described previously . Briefly, chromatin was isolated from 2 g of leaves of JMJ704 T-DNA mutant and wild-type plants respectively. After fragment sonication, the DNA/protein complex was immune-precipitated with ChIP-grade antibody against H3K4me2 (07–030, Millipore) and H3K4me3 (07–473, Millipore). After reverse cross-linking and proteinase K treatment, the immunoprecipitated DNA was extracted with phenol/chloroform. The immunoprecipitated and input DNA was performed for quantitative PCR using gene-specific primers (Additional file 5: Table S3) as described above. The quantitative PCR results were analyzed by following a method reported in the manual of Magna ChIP™ HiSens kit (Millipore). All the quantitative ChIP-PCR was performed in three biological replicates.
Availability of supporting data
The RNA-seq data described in this article have been deposited into the NCBI’s GEO database (GSE74670). Nucleic acid sequence data can be found in the Rice Genome Annotation Project website (http://rice.plantbiology.msu.edu/). The accession numbers: JMJ704 (LOC_Os05g23670), NRR (LOC_Os01g03940), OsWRKY62 (LOC_Os09g25070) and Os-11N3 (LOC_Os11g31190).
- Xoo :
Xanthomonas oryzae pv. oryzae
Di- or tri-methylation for histone H3 at lysine 4
Histone lysine demethylases
JmjC domain-containing histone demethylase 2
JmjC domain-containing 2
JmjC protein containing AT-rich interaction domain
N-terminal FY-rich _ terminal FY-rich
Differentially Expressed Genes
We thank Dr. Hana Mujahid of Mississippi State University, U.S.A. for the critical reviewing of the manuscript. This work was supported by Agricultural Sciences and Technologies Innovation Program, Chinese Academy of Agricultural Sciences to Shiwen Huang (Rice Pests Management Research Group) and Jian Zhang (Rice Reproductive Developmental Biology Group), and the Special Transgenic Program of the Chinese Ministry of Agriculture (2013ZX08010005).
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