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First published online August 27, 2008; 10.1104/pp.108.124529 Plant Physiology 148:1032-1041 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
BAH1/NLA, a RING-Type Ubiquitin E3 Ligase, Regulates the Accumulation of Salicylic Acid and Immune Responses to Pseudomonas syringae DC30001,[W],[OA]Department of Biology, Faculty of Sciences, Kyushu University, Hakozaki, Fukuoka 812–8581, Japan
Salicylic acid (SA) is a primary factor responsible for exerting diverse immune responses in plants and is synthesized in response to attack by a wide range of pathogens. The Arabidopsis (Arabidopsis thaliana) sid2 mutant is defective in a SA biosynthetic pathway involving ISOCHORISMATE SYNTHASE1 (ICS1) and consequently contains reduced levels of SA. However, the sid2 mutant as well as ICS-suppressed tobacco (Nicotiana benthamiana) still accumulate a small but significant level of SA. These observations along with previous studies suggest that SA might also be synthesized by another pathway involving benzoic acid (BA). Here we isolated a benzoic acid hypersensitive1-Dominant (bah1-D) mutant that excessively accumulated SA after application of BA from activation-tagged lines. This mutant also accumulated higher levels of SA after inoculation with Pseudomonas syringae pv tomato DC3000. Analysis of the bah1-D sid2 double mutant suggested that the bah1-D mutation caused both ICS1-dependent and -independent accumulation. In addition, the bah1-D mutant showed SA-dependent localized cell death in response to P. syringae pv tomato DC3000. The T-DNA insertional mutation that caused the bah1-D phenotypes resulted in the suppression of expression of the NLA gene, which encodes a RING-type ubiquitin E3 ligase. These results suggest that BAH1/NLA plays crucial roles in the ubiquitination-mediated regulation of immune responses, including BA- and pathogen-induced SA accumulation, and control of cell death.
Plants sense contacts with microbial pathogens and exert diverse immune responses, including defense responses triggered by the recognition of pathogen-associated molecular patterns (PAMPs) or microbial-associated molecular patterns, hypersensitive responses (HRs) mediated by resistance (R) proteins, and subsequent systemic acquired resistance. Salicylic acid (SA) plays crucial roles as a signaling molecule in acquiring resistance. The accumulation of SA is induced after infection with both virulent and avirulent pathogens (Spoel et al., 2003  ). A recent report showed that a PAMP derived from a bacterial pathogen, Pseudomonas syringae pv tomato (Pst) DC3000, induces SA accumulation (Tsuda et al., 2008). Pathogens eluding the PAMP-triggered immune responses dispatch effector proteins to the insides of plant cells through a type III secretion system to acquire virulence effects. Some effectors, called avirulence proteins, are recognized by R proteins and lead to the HR. SA is involved in the regulation of HR including the oxidative burst and programmed cell death (Draper, 1997; Mur et al., 1997; Shirasu et al., 1997). Endogenous and exogenous SA can activate signal transduction pathways to induce systemic acquired resistance and the expression of defense-related genes, for example, PR1 (Durrant and Dong, 2004). SA-deficient plants are compromised in all of these immune responses and accordingly become hypersusceptible to both avirulent and virulent pathogens (Delaney et al., 1994; Mur et al., 1997; Nawrath and Métraux, 1999; Dewdney et al., 2000; Wildermuth et al., 2001; Tsuda et al., 2008). Moreover, emerging evidence suggests that some effectors target SA-mediated signaling and SA biosynthesis to disturb host immune responses (DebRoy et al., 2004; Jelenska et al., 2007). Given these findings, SA is a fundamental factor in plant-pathogen interactions and provides a backbone to immune responses.
SA is assumed to be synthesized through the Phe ammonia-lyase (PAL) pathway in which Phe is converted to benzoic acid (BA) by several enzymes including PAL and subsequently BA is converted to SA by a putative enzyme BA 2-hydroxylase (BA2H; Leon et al., 1993
In this study, we isolated and characterized the benzoic acid hypersensitive1-Dominant (bah1-D) mutant, an activation-tagged line carrying a mutation in a RING-type ubiquitin E3 ligase, which accumulated excess amounts of SA. The bah1-D mutant was allelic to the nla mutant, which showed early senescence under low nitrogen condition (Peng et al., 2007
Isolation and Characterization of the bah1-D Mutant
Several SA-accumulating mutants show the dwarf phenotype, and the reduction of SA in these plants can restore the wild-type phenotype (Bowling et al., 1997
To analyze expression of the SA-inducible PR1 gene, leaves were harvested from wild-type and bah1-D plants grown on a media containing 50 µM BA. As expected, PR1 transcripts accumulated in both the wild-type and the bah1-D plants grown on the SA-containing medium. On the other hand, PR1 transcripts accumulated in the bah1-D plants but not the wild-type plants grown on the BA-containing medium (Fig. 1B). These results suggested that the accumulation of SA may be activated in bah1-D plants grown in the presence of BA. Free SA and conjugated SA levels were examined in leaves of 2-week-old seedlings that had been treated by spraying with 1 mM BA. The bah1-D plants showed slightly higher levels of free SA than wild-type plants without BA treatment (Fig. 1C). After BA treatment, the levels of free SA increased significantly in the bah1-D plants but only very slightly in the wild-type plants (Fig. 1C). This suggested that exogenously applied BA may infiltrate into the leaves of the bah1-D plants and then be converted to SA, or may stimulate the biosynthesis of SA. Both the basal level and the level after BA treatment of conjugated SA were significantly higher in the mutant than the wild-type plants (Fig. 1C). Possibly, basal SA biosynthesis might be enhanced in the bah1-D plants, resulting in the accumulation of conjugated SA, which is less toxic than free SA. This is supported by the observations that a small amount of PR1 transcript was detected in bah1-D plants grown on normal Murashige and Skoog medium, and a cDNA microarray analysis showed that PR1 expression was slightly up-regulated in bah1-D plants grown on normal medium (Fig. 1B; Supplemental Table S1).
The enhanced accumulation of basal SA in the bah1-D plants raises the possibility that basal disease resistance may be activated in the mutant. To study this possibility, the bah1-D plants were inoculated with Pst DC3000 strains and bacterial growth 3 d after inoculation was measured (Fig. 2A
). Bacterial growth in the bah1-D plants inoculated with Pst DC3000 (avrRpm1) was almost the same as that in the wild-type plants, indicating that the bah1-D plants are as resistant to Pst DC3000 (avrRpm1) as the wild-type plants. On the other hand, bacterial growth in the bah1-D plants inoculated with Pst DC3000 was significantly reduced compared with that in the wild-type plants. This enhanced resistance to Pst DC3000 may be attributable to high basal accumulation of SA and/or to Pst DC3000-inducible accumulation of SA in the bah1-D plants. Therefore, we examined the levels of SA in the bah1-D plants after inoculation with Pst DC3000. As previously reported, the levels of both free and conjugated SA increased in the wild-type plants 3 d after inoculation with Pst DC3000 (Spoel et al., 2003
The bah1-D sid2 Double Mutant Still Accumulates SA in Response to BA and Pst DC3000 The accumulation of total SA was examined in bah1-D sid2 double-mutant plants. SA levels in bah1-D sid2 plants were much lower than those in the bah1-D plants after treatment with BA (Fig. 3A ). Therefore, the high levels of SA in bah1-D plants may be synthesized by ICS1. However, detectable levels of total SA did accumulate in both sid2 and bah1-D sid2 plants, and the levels in the bah1-D sid2 plants were significantly higher than those in the sid2 plants (Fig. 3B). These results suggest that the majority of SA accumulation in the bah1-D plants is synthesized by the ICS1 pathway, but a residual amount of SA in both sid2 and bah1-D sid2 plants may be derived from an ICS1-independent pathway. Likewise, SA levels increased in both sid2 and bah1-D sid2 plants after inoculation with Pst DC3000 (Fig. 3C). This indicates that the sid2 mutant is still able to accumulate SA in response to Pst DC3000. SA levels in the bah1-D sid2 plants were higher than those in the sid2 plants after both mock inoculation and inoculation with Pst DC3000, suggesting that the bah1-D mutation causes basal and induced accumulation of SA independently of ICS1. While bah1-D plants accumulated approximately 3.6-fold higher levels of SA than the wild-type plants, bah1-D sid2 plants accumulated only approximately 1.5-fold higher levels of SA than sid2 plants (Figs. 2B and 3C). Therefore, the bah1-D mutation amplifies the accumulation of SA drastically if ICS1 exists. Taken together, BAH1 may be involved in inhibitory mechanisms underlying the ICS1-independent basal accumulation of SA and the ICS1-mediated amplification of SA.
The bah1-D Mutation Causes SA-Dependent Pathogen-Induced Localized Cell Death and SA-Independent Age-Related Cell Death Notably, localized cell death was observed in the bah1-D plants 2 d after inoculation with Pst DC3000 and resulted in a restriction of the spread of disease symptoms (Fig. 3D). On the other hand, characteristic chlorotic disease symptoms developed in the wild-type and the sid2 plants. The localized cell death was similar to, but occurred more slowly than, the R-gene-mediated HR cell death that occurred in response to Pst DC3000 (avrRpm1) inoculation (data not shown). In fact, the bah1-D mutant also accumulated higher levels of SA and was resistant to Pst DC3000 as if R-gene-mediated signals induced the resistance (Fig. 2). The localized cell death was abolished and disease symptoms developed in bah1-D sid2 plants, indicating that cell death required the ICS1-dependent accumulation of SA (Fig. 3D). The bah1-D plants also exhibited spontaneous cell death in leaves of bolted plants, but not in leaves of young plants before bolting (Fig. 3E). Once the senescence-like response started, it did not stop until the whole leaf was withered. Clusters of dead cells were visualized by trypan blue staining of bah1-D leaves (Fig. 3E). The age-related cell death was not abolished in the bah1-D sid2 plants (Fig. 3F). SA accumulated in the dying leaves of bah1-D plants without BA treatment and in BA-treated leaves of bah1-D plants that were not undergoing cell death (Fig. 1C; data not shown). Therefore, BA-related biosynthesis may be activated in the bah1-D plants irrespective of cell death. These results suggest that BAH1 regulates pathogen-induced localized cell death and age-related cell death in SA-dependent and SA-independent manners, respectively.
The sequences flanking the T-DNA insertion site were identified by plasmid rescue (Fig. 4A
). The insertion consisted of at least two T-DNA fragments connected inversely, with 4x 35S elements at each end, and was located in the 5'-untranslated region of the At1g02860 gene. Unexpectedly, reverse transcription (RT)-PCR analysis revealed that the expression of this gene was suppressed in the bah1-D mutant (Fig. 4B). No other neighboring genes were affected by this insertion. These results suggested that the bah1-D mutation may be caused by suppression of the At1g02860 gene. To confirm this, we generated RNAi plants (named bah1-R) in which the At1g02860 gene was suppressed (Fig. 5
). The bah1-R plants showed similar phenotypes to those of the bah1-D mutant, including growth inhibition in the presence of BA, accumulation of SA after treatment with BA, and age-related cell death. As a further confirmation, TILLING analysis was performed to screen for more bah1 alleles carrying point mutations. Mutant alleles with substituted amino acids in BAH1 were obtained and these plants showed bah1-like phenotypes (Fig. 4A; Supplemental Table S2; data not shown). The expression of the BAH1 gene was induced 24 h after application of BA and SA (Fig. 4C). SA accumulation coincided with suppressed expression of the BAH1 gene in the bah1-D mutant, suggesting that the BAH1 gene may play a role in SA-mediated negative feedback regulation of SA accumulation. BAH1 is predicted to contain a SPX (SYG1/Pho81/XPR1) domain and a RING-finger domain (Fig. 4A). The function of the SPX domain in plants is not yet known. The RING domain is a feature of the RING-type ubiquitin E3 ligases, but E3 ligase activity has not yet been confirmed in the BAH1 protein (Stone et al., 2005
Nitrogen Limitation Induces the Accumulation of SA in Both Wild Type and bah1-D Mutant
The nla mutant shows age-related cell death under conditions of nitrogen limitation (Peng et al., 2007
The levels of SA were substantially reduced by the sid2 mutation in Arabidopsis. However, detectable levels remained, and increased in the bah1-D sid2 double mutant after application of BA and after inoculation with Pst DC3000 (Fig. 3, B and C). These results demonstrate that the bah1-D mutation can cause the accumulation of SA independently of ICS1. Because the sid2 mutant has another functional ICS gene, ICS2, there is a possibility that ICS2 gene contributed to the accumulation of SA in the bah1-D sid2 mutant. According to the microarray analysis, ICS2 gene expression levels were almost the same in the bah1-D mutant and wild-type plants (Supplemental Table S1). Unlike ICS1, the expression of ICS2 gene is not induced after infection with the biotrophic fungus Erysiphe orontii (Wildermuth et al., 2001 ). Taken together, ICS2 induction may not be responsible for the accumulation of SA in defense responses or in the bah1-D mutant, but the ICS2 protein may be posttranscriptionally modulated to make a slight contribution to the accumulation of SA. More recently, Garcion et al. (2008) demonstrated the existence of an ICS-independent pathway using the mutant that lacks both the ICS1 and ICS2 genes.
An ICS-independent pathway is possibly activated by bah1-D mutation and may involve the BA2H. Actually, BA levels in the bah1-D mutant were less than those in the wild type (Fig. 6B), suggesting that some BA may be used for the synthesis of SA in the bah1-D mutant. Although the gene encoding BA2H has not yet been identified in any plant species, the BA2H protein has been studied in tobacco (Nicotiana tabacum). The tobacco BA2H is thought to be a 160-kD cytochrome P450 protein (Leon et al., 1995
In the bah1-D sid2 double mutant, the bah1-D mutation raised both the basal and Pst DC3000-inducible levels of SA, despite the lack of ICS1 (Fig. 3). In the bah1-D mutant with a functional ICS1, SA accumulated at an accelerated pace (Figs. 2B and 3A). These results suggest that BAH1/NLA is involved in the negative regulation of both the basal and the Pst DC3000-inducible accumulation of SA. The bah1-D sid2 mutation may be equivalent to a runaway car with a gear-change failure. The bah1-D mutation may cause the continuation of signals promoting SA production, despite the lack of ICS1 in the bah1-D sid2 mutant, as if an accelerator is kept pressed down in a car that is stuck in first gear. SA can overaccumulate in the bah1-D mutant, due to the presence of a functional ICS1, like a car with the accelerator pressed down in top gear. This raises the possibility that the basal accumulation may control the ICS1-dependent pathogen-inducible accumulation. Similarly, a low level of SA activates PAD4 expression and PAD4 stimulates SA accumulation, which further induces PAD4 expression, resulting in an amplifying loop (Jirage et al., 1999
It was reported recently that ICS1-dependent SA accumulation is induced by a PAMP from Pst DC3000 hrcC, which lacks the type III secretion system (Tsuda et al., 2008
Unlike the HR-like localized cell death, age-related cell death was not suppressed in the bah1-D sid2 mutant (Fig. 3F), suggesting that the induction of age-related cell death does not require SA. Even though SA levels in the bah1-D sid2 mutant were slightly higher than those in the sid2 mutant (Fig. 3B), it is unlikely that age-related cell death was affected by this difference, because it was not suppressed in the double mutant even though its SA levels were much lower than those in the bah1-D mutant (Fig. 3A). Therefore, the mechanisms leading to age-related cell death may be considerably different from those leading to HR-like cell death. When age-related cell death occurs in leaves, the regions in which cell death has yet to occur turn yellow simultaneously. Isochorismate is the major precursor for the biosynthesis of both SA and phylloquinone (Gross et al., 2006
Leaf senescence is a crucial strategy for recycling the degradation products of chlorophyll as nitrogen nutrients under conditions of nitrogen starvation (Smart, 1994 Rice (Oryza sativa) and Medicago truncatula have orthologs of BAH1/NLA (Supplemental Fig. S3). A reduction in nitrogen fertilizer application has been established as a traditional way to control disease in these agricultural plants. In line with this, we found that nitrogen limitation could induce the accumulation of SA even in wild-type Arabidopsis plants (Fig. 6B). Therefore, it will be important to elucidate the roles of BAH1/NLA orthologs in SA accumulation and disease resistance in various agricultural plants, and to understand the role that nitrogen plays in the action of these genes.
Similar to the bah1-D mutant, the npr1 mutant also accumulates higher levels of SA after inoculation with a pathogen (Delaney et al., 1995 If BAH1/NLA acts as a RING-type E3 ligase, the SPX domain might be a binding site for substrate proteins. In fact, the bah1-D phenotypes were also observed in the bah1-4 allele that has an amino acid change in the SPX domain, demonstrating the importance of this domain in the BAH1/NLA protein. Because the function of the SPX domain remains unclear, it will be crucial to identify proteins that bind to it to better understand the function of this unknown E3 ligase in plant immune responses.
Plant Materials and Growth Conditions
Arabidopsis (Arabidopsis thaliana) plants were grown on Jiffy-7 peat pellets (Jiffy Products International AS) under continuous light in a growth chamber at 23°C. Seeds of the Weigel activation-tagged collection were obtained from the Arabidopsis Biological Resource Center (Weigel et al., 2000
Leaves of 17-d-old plants were syringe inoculated with Pst DC3000 (empty vector or avrRpm1) at a titer of 106 colony forming units (cfu) per mL. Bacterial growth assays and trypan blue staining were carried out as described previously (Yaeno et al., 2004
Leaves of 1.5- to 2-week-old plants were harvested 1 week after treatment with 1 mM BA solution containing 0.01% Tween 20. Leaves of 17-d-old plants were harvested 3 d after syringe inoculation with Pst (106 cfu/mL). Approximately 0.2 g of tissue was used for analyses of the wild-type and bah1-D plants, and 1 g of tissue was used for analyses of the sid2 and bah1-D sid2 plants. Extraction and measurement of SA was carried out as described previously (Yaeno et al., 2006
RNA was extracted from 2-week-old plants grown on Murashige and Skoog medium containing 50 µM BA or SA. RNA gel-blot analysis of the PR1 expression was performed as described previously (Yaeno et al., 2006
The bah1-D mutant was backcrossed three times with the wild-type Col-7. The T-DNA contains the Basta resistance gene as a selectable marker. A homozygous mutant line was established by analyzing the segregation of Basta resistance and BA sensitivity. DNA gel-blot analysis along with the segregation analyses revealed that there was one T-DNA insertion in the bah1-D mutant. The restriction enzymes EcoRI and XhoI were used for plasmid rescue. Three independent plasmids were obtained and sequenced by primer walking.
For the RNAi construction, antisense and sense fragments were prepared using the primer sets, 5'-TCTAGACCAGATTCCTTCTTAGATTC-3'/5'-GGATCCTGCTCAGAAGCTTCTTGAGC-3' and 5'-GGCGCGCCTGCTCAGAAGCTTCTTGAGC-3'/5'-GAGCTCCCAGATTCCTTCTTAGATTC-3'. These fragments were cleaved at prepared restriction sites and inserted along with a linker fragment and the 35S promoter into the vector pBIH101 as described previously (Yaeno et al., 2006 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers NM_100167, NM_129450, NM_001057323, NM_001067141, and ABE85047.
The following materials are available in the online version of this article.
We are grateful to Dr. Jeff Dangl and Dr. Ken Shirasu for useful advice and discussions on the manuscript. Received June 10, 2008; accepted August 25, 2008; published August 27, 2008.
1 This work was supported by Core Research for Evolutional Science and Technology of the Japan Science and Technology Agency and by the Japan Society of the Promotion of Science (grant no. 17370019). 
2 Present address: RIKEN Plant Science Center, Yokohama 230–0045, Japan. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Koh Iba (koibascb{at}mbox.nc.kyushu-u.ac.jp).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.124529 * Corresponding author; e-mail koibascb{at}mbox.nc.kyushu-u.ac.jp.
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