JXB Advance Access originally published online on February 13, 2008
Journal of Experimental Botany 2008 59(2):177-186; doi:10.1093/jxb/erm345
Focus Review |
Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach
1Institute for Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, Munich, Germany
2Genomatix Software GmbH, Munich, Germany
To whom correspondence should be addressed. E-mail: durner{at}gsf.de
Received 19 June 2007; Revised 19 November 2007 Accepted 10 December 2007
 |
Abstract |
|---|
 Top Abstract IntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Due to its high reactivity and its ability to diffuse and permeate the cell membrane, nitric oxide (NO) and its exchangeable redox-activated species are unique biological messengers in animals and in plants. Although an increasing number of reports indicate that NO is an essential molecule in several physiological processes, there is not a clear picture of its method of action. Studies on the transcriptional changes induced by NO permitted identification of genes involved in different functional processes such as signal transduction, defence and cell death, transport, basic metabolism, and reactive oxygen species (ROS) production and degradation. The co-expression of these genes can be explained by the co-operation of a set of transcription factors that bind a common region in the promoter of the regulated genes. The present report describes the search for a common transcription factor-binding site (TFBS) in promoter regions of NO-regulated genes, based on microarray analyses. Using Genomatix Gene2Promotor and MatInspector, eight families of TFBSs were found to occur at least 15% more often in the promoter regions of the responsive genes in comparison with the promoter regions of 28 447 Arabidopsis control genes. Most of these TFBSs, such as ocs element-like sequences and WRKY, have already been reported to be involved in particular stress responses. Furthermore, the promoter regions of genes involved in jasmonic acid (JA) biosynthesis were analysed for a common TFBS module, since some genes responsible for JA biosynthesis are induced by NO, and an interaction between NO and JA signalling has already been described.
Key words: Arabidopsis, gene expression, microarray, nitric oxide, signal transduction
|
Introduction |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Nitric oxide (NO) is a small, highly reactive, membrane-permeable molecule, which has turned out to be an important biological messenger in animals and plants (Stamler et al., 1992; Schmidt and Walter, 1994; Wendehenne et al., 2001). In the last few years, many studies have described NO as both a cytotoxic and a cytoprotecting regulator involved in different physiological processes in plants. It has been implicated in disease resistance, stomata closure, seed germination, iron homeostasis, different development processes, and the response of plants to abiotic stresses such as drought, UV-B, salinity, and high temperature (Delledonne et al., 1998; Durner et al., 1998; Garcia-Mata and Lamattina, 2002; Zhao et al., 2004).
Many of the biological functions of NO arise as a direct consequence of chemical reactions between proteins and NO or NO oxides generated as NO/O2 or NO/superoxide reaction products. The reactions of NO with metal ions of haem groups or the formation of dinitrosyl complexes are demonstrated to play important roles in NO signalling. In mammalian cells, NO regulates the production of the important second messenger cGMP by interacting with the iron ion of the haem moiety of guanylate cyclase (Russwurm and Koesling, 2004). An increase in the endogenous cGMP in tobacco leaves and suspension cells after NO treatment was demonstrated by Durner et al. (1998), suggesting the existence of an NO-dependent cGMP pathway in plants, too.
However, NO is also an important redox-active signalling molecule and after the cGMP signalling mechanism, S-nitrosylation of cysteine residues of redox-sensitive proteins is the second most important principle of NO signalling. Recently, >100 proteins were identified in Arabidopsis representing candidates for protein S-nitrosylation (Lindermayr et al., 2005). However, until now there is experimental evidence for only a few plant proteins being regulated by S-nitrosylation, including haemoglobin 1, glyceraldehyde 3-phosphate dehydrogenase, S-adenosylmethionine synthetase, and metacaspase, and the K+ channels in guard cells of Arabidopsis thaliana are regulated by NO via S-nitrosylation (Perazzolli et al., 2004; Sokolovski and Blatt, 2004; Lindermayr et al., 2005, 2006).
Besides the regulation of signalling pathways, NO can control physiological processes directly by encroaching upon gene transcription. Transcriptional changes in A. thaliana in response to NO have been analysed using different techniques such as cDNA-amplified fragment length polymorphism (Polverari et al., 2003), microarray, and real-time PCR (Huang et al., 2002; Parani et al., 2004). Identified NO-modulated genes are involved in different functional processes such as signal transduction, defence and cell death, transport, basic metabolism, and reactive oxygen species (ROS) production and degradation. An important number of these modulated genes correspond to proteins with a regulatory role as components of the signal transduction cascade or transcription factors.
How can NO regulate gene expression? The transcription of genes is regulated by transcription factors. These proteins bind to defined promoter sequences to enhance or repress gene expression by assisting or blocking RNA polymerase binding, respectively. As well as direct DNA binding, transcription factors often interact with other proteins and bind to promoter regions as multiprotein complexes. The DNA binding affinity of transcription factors can be altered, for example, by phosphorylation or redox-dependent modifications of transcription factors, such as protein S-nitrosylation. For example, the activity of the thiol-containing transcriptional activator OxyR, whose oxidation controls the expression of genes involved in H2O2 detoxification, is modulated by S-nitrosylation (Hausladen et al., 1996).
The use of whole genome transcript analyses to identify co-regulated genes has been rapidly becoming a widespread approach to understanding the regulation of physiological processes. Similar expression profiles might be caused by the co-ordinated action of transcription factors. Thus, a systematic and logical approach to study genes with similar expression patterns is to analyse their promoter sequences in order to identify transcription factors that might be responsible for the co-expression.
Here the screening of promoter regions of NO-regulated genes for common transcription factor-binding site (TFBS) patterns is described. Using Agilent microarrays, the transcriptional changes in Arabidopsis plants in response to gaseous NO and in cell suspension cultures after treatment with an NO donor were investigated. A total of 28 genes which were up-regulated in both plant and cell culture experiments were identified. Furthermore, 121 and 79 genes were induced exclusively in plant and cell culture experiments, respectively. Twenty-six genes were found to be down-regulated. Using the Genomatix Gene2Promotor program, the promoter regions of the NO-regulated genes were identified, which were then screened for common TFBSs with Genomatix MatInspector.
|
Material and methods |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Cell culture and plant treatment
Plants (A. thaliana, ecotype Columbia) were grown for 4–5 weeks in a growth chamber (at 69% relative humidity, 10 h dark) at 23 °C during the day and 18 °C at night. The experimental set-ups to study the effect of NO on plants consisted of controlled environment cabinets as well as complete instrumentation to adjust and control gaseous NO concentrations of 1250 ppm for 10 min. At this concentration, the plants did not show symptoms. After the treatment, plants were put back into the growth chambers until they were harvested.
Cell suspension cultures of A. thaliana (ecotype Columbia) were grown in liquid PS-medium as described in Huang et al. (2002). A 7-d-old cell suspension culture was treated with 0.5 mM of the NO donor NOR3 {(E)-ethyl-2-[(E)-hydrxyimino]-5-nitro-3-hexene-amide}. After the treatment, cells were harvested by filtration at different time points. Harvested plants and cell cultures were immediately frozen in liquid nitrogen and stored at –80 °C.
Microarray
Microarray analyses were performed as described in Huang et al. (2002) with some modifications. For microarray analyses, Agilent whole genome Arabidopsis arrays were used (Agilent, Santa Clara, CA, USA). Probes were made by using an indirect aminoallyl labelling method with Cy3-dUTP or Cy5-dUTP (Amersham Pharmacia, Freiburg, Germany) and purified according to standard protocols. The arrays were scanned by using an Axon GenePix 4000 scanner (Axon Instruments, Union City, CA, USA) and the GENEPIX PRO 4.1 and ACUITY (Axon Instruments) software packages.
Fluorescent probes
Target RNA from NOR-3-treated Arabidopsis cells was extracted using the TRIzol reagent according to the supplier's instructions (Invitrogen, Karlsruhe, Germany). Poly(A) RNA was purified from total RNA with the Fast Track mRNA isolation kit (Invitrogen) according to the manufacturer's instructions. Probes were made using the indirect aminoallyl labelling method (see http://www.tigr.org/tdb/microarray/protocols.shtml). Each mRNA sample (one control and one treated sample) was reverse-transcribed in the presence of Cy3-dUTP or Cy5-dUTP (Amersham Pharmacia Biotech), and purified according to standard protocols.
Hybridization and scanning
Hybridization was done as previously described (Huang et al., 2002). GenePix Pro3.0 software was used to identify differentially expressed genes. Background fluorescence was calculated as the median fluorescence signal of non-target pixels around each gene spot. The induction or repression of a gene is defined as a minimum 2.5-fold change in its transcript level. Presented data show the mean of four experiments.
Screening for putative TFBSs (Genomatix analyses)
Identification of the potential promoter regions and TFBSs was conducted using the Genomatix suite of programs (http://www.genomatix.de, Genomatix Software GmbH, Munich, Germany) (Quandt et al., 1995). The Gene2promotor program from the Genomatix software package was used to locate the correlated genes within the genome and define 601 bp of the promoter regions (500 bp upstream of and 100 bp into the transcription start site) for each gene. The 601 bp sequences obtained from the Gene2promotor program were then used as the target sequences for putative transcription factor recognition site identification using the MatInspector Version 4.3 program (Cartharius et al., 2005). The parameters used were the standard (0.75) core similarity and the optimized matrix similarity. To identify common TFBS modules in the promoter regions of the jasmonic acid (JA) biosynthetic pathway genes, the Genomatix Frameworker program was used. The parameters used were: (i) minimum number of sequences with framework, 27%; (ii) maximum distance variance between two elements, 25 bp.
|
Results and discussion |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
NO is an important signalling molecule, which fulfils many different physiological functions in plants. Gene expression in response to NO was analysed in several laboratories, where an induction of several pathogenesis-related proteins and an array of antioxidant genes encoding peroxidases, glutathione S-transferases (GST), protein kinases, and transcription factors could be demonstrated.
Microarray analyses
Whole genome microarray (Agilent 1/2) was used to explore transcriptional changes in Arabidopsis cell suspension cultures and plants in response to the NO donor NOR-3 and gaseous NO. Array hybridizations were based on four replicates. Rigorous criteria were applied in the selection procedure so that those genes with <2.5-fold signal compared with the background were ignored (see Materials and methods). To obtain specific gene expression, the NO treatment was adjusted to yield only moderate changes in transcriptional activity. Under the conditions applied (0.5 mM NOR-3) the cells did not show any symptoms such as cell death. Modifying the treatment (i.e. lower NO concentrations for a prolonged time) resulted in a slightly different expression array (data not shown).
In summary, 28 genes which were up-regulated in almost all experiment were observed (Fig. 1; Supplementary data 1 available at JXB online). Furthermore, 79 and 121 genes were exclusively induced in cell culture and plant experiments, respectively. Additionally, 26 genes were found to be down-regulated in cell culture experiments. The difference in the set of regulated genes is probably due to the difference between the biological system used (plant/cell culture) but also to the different mechanism of action of the NO applications (NO donor, NOR-3/gaseous NO).
|
Common TFBSs in NO-regulated genes
Based on the results of the microarray analyses, the possibility of identifying common TFBSs in the promoter regions of the co-expressed genes was explored. The Gene2promotor program from the Genomatix software package was used to locate the correlated genes within the genome and define 601 bp of the promoter regions (500 bp upstream of and 100 bp into the transcription start site) for each gene (Genomatix Software GmbH, Munich, Germany). The 601 bp sequences obtained from the Gene2promotor program then were used as the target sequences for putative transcription factor recognition site identification using the Genomatix MatInspector Version 4.3 program. The parameters used were the standard (0.75) core similarity and the optimized matrix similarity (Quandt et al., 1995). As a control, the occurrence of the TFBSs within a set of 28 447 Arabidopsis genes as a percentage was used (Genomatix database, http://www.genomatix.de).
The MatInspector analyses showed a large number of putative TFBSs in the promoter of the NO-regulated genes. In Table 1 all TFBSs which are common to at least 25% of the analysed promoters are listed. The given values represent the percentage of promoters in which a match to the matrix family is found with optimized matrix similarity. The detailed results are given as Supplementary data at JXB online (Supplementary data 2–5). Most of the TFBSs were found to occur with the same frequency as the 28 447 Arabidopsis genes, e.g. MADS, AHBP, and IBOX elements (Table 1). However, eight families of TFBSs occurred at least 15% more often in the promoter regions of the analysed groups of genes in comparison with the promoter regions of the control genes (Table 1). GBOX, OCSE, and L1BX elements are enriched in genes up-regulated in both cell culture and plant experiments. Moreover, GBOX and OCSE elements, together with MYCL and OPAQ, are highly present in promoters of up-regulated cell culture genes. In genes induced in plants only, WRKY-binding sites are enriched in their promoters. In the down-regulated genes of cell cultures an increased occurrence of TBPF and MIIG elements was observed.
|
In plants, basic region/leucine zipper motif (bZIP) transcription factors are involved in the regulation of many different physiological processes such as biotic and abiotic stress signalling, seed maturation, flowering, and light signalling (Lebel et al., 1998; Hobo et al., 1999; Ratcliffe and Riechmann, 2002). The bZIP transcription factors contain a DNA-binding motif and a leucine zipper domain, which is responsible for dimerization (Ellenberger et al., 1992; Izawa et al., 1993; Metallo and Schepartz, 1997; Choi et al., 2000). The core motif for DNA binding is ACGT. However, using recombinant bZIP proteins, it has been demonstrated that neighbouring nucleotides affect binding affinity. Dependent on the nucleotide flanking the 3' site of the motif, three different types of ACGT elements have been defined: a G-box (CACGTG), C-box (GACGTG), and A-box (TACGTA). bZIP transcription factors seem to play a pivotal role in regulation of plant physiology, since Arabidopsis has
4 times as many bZIP-encoding genes as yeast, worm, and human (Riechmann et al., 2000). The memebers of the bZIP family of G-box-binding factors have been implicated in the expression of a number of genes during pathogen attack (Kim et al., 1992). Interestingly, in almost all promoters of the genes up-regulated in plants and cell cultures treated with NO, GBOX elements were located within the first 250 bp upstream of the putative transcription start (Fig. 2A).
|
Another class of bZIP-binding elements implicated in the plant defence response is formed by octopine synthase (ocs). In Arabidopsis, ocs element-like sequences (OCSEs) are important for the expression of specific GST- and pathogenesis-related genes such as the GST6 and the PR1 genes (Lebel et al., 1998; Chen and Singh, 1999). This relationship between ocs elements and plant defence responses was supported by the discovery that Arabidopsis TGA/ocs element-binding factors (OBFs) interact with NPR1, a key component in the salicylic acid defence signalling pathway (Zhou et al., 2000). Moreover, there are several members of the TGA/OBF family which plays a role in xenobiotic stress responses and development (Johnson et al., 2001).
Opaque-2-like transcriptional activators (OPAQs) are also a well-characterized family of plant bZIPs with an extended leucine zipper with up to nine heptad repeats. One of the main processes modulating OPAQ activity is the heterodimerization with other bZIP transcription factors. Opaque-2 regulates the expression of 
and β prolamines, the main storage proteins in seeds of cereals such as maize and Coix (Takatsuji, 1998). Other members of the OPAQ family, such as CPFR2 and G/HBF-1, might be involved in responses to environmental or pathogen challenge (Droge-Laser et al., 1997; Lara et al., 2003). The stimulation of G/HBF-1 kinase activity and G/HBF-1 phosphorylation after treatment with glutathione or avirulent Pseudomonas syringae pv. glycinea are terminal events in a signal pathway for activation of early transcription-dependent plant defence responses (Droge-Laser et al., 1997).
Similar to bZIP proteins, WRKY family members are involved in the regulation of various physiological processes, including pathogen defence, senescence, and trichome development (Robatzek and Somssich, 2001; Johnson et al., 2002; Dong et al., 2003). Their DNA-binding domain (WRKY domain) comprises 60 amino acids, but the overall structures of WRKY proteins are highly divergent and can be categorized into distinct groups, which might reflect their different functions (Eulgem et al., 2000). Additional domains of WRKYs are restricted to subgroups of this family and include, for example, conserved regions of nuclear localization signals, calmodulin-binding sites, or putative leucine zippers (Cormack et al., 2002; Sun et al., 2003; Park et al., 2005). Multiple studies have demonstrated the ability of WRKYs to bind the W box element (TTGACC/T) (Rushton et al., 2002; Yamasaki et al., 2005), which is found in the promoters of many plant defence genes (Maleck et al., 2000; Chen et al., 2002). W box or W box-like sequences often occur in clusters within promoters, suggesting a possible synergistic action with other WRKY proteins and/or other classes of transcription factors (Maleck et al., 2000). The transcription of WRKY genes is strongly and rapidly up-regulated in numerous plant species in response to wounding, pathogen infection, or abiotic stresses, such as drought, cold adaptation, or heat-induced chilling tolerance (Eulgem et al., 2000; Robatzek and Somssich, 2001; Rizhsky et al., 2002). A total of 74 Arabidopsis WRKY genes respond to bacterial infection or salicylic acid (SA) treatment (Dong et al., 2003), and Arabidopsis WRKY70 was identified as a common regulatory component of SA- and JA-dependent defence signalling, mediating cross-talk between these antagonistic pathways. Overexpression and antisense lines indicated that WRKY70 plays a positive role in SA signalling and functions as a negative regulator of JA-inducible genes (Li et al., 2004). In contrast, WRKY18, WRKY40, and WRKY60 may function redundantly as negative regulators in SA-dependent pathways but play a positive role in JA-mediated pathways (Xu et al., 2006). Moreover, NPR1 is functionally linked to WRKYs during plant immune responses. Intriguingly, WRKYs control NPR1 expression on the one hand, while on the other hand they seem to operate downstream from NPR1 (Yu et al., 2001; Wang et al., 2006). Additionally, WRKY transcription factors are involved in co-ordination of plant development and/or ageing, since the expression of several Arabidopsis WRKY genes is strongly up-regulated during plant senescence (Robatzek and Somssich, 2001).
Many of the genes induced in Arabidopsis plants after NO treatment have more than one WRKY-binding site in their promoter region (Fig. 2B). Typically, WRKY promoters are enriched for W boxes, and multiple studies have revealed interactions of WRKYs with either their own promoters or those of other family members, suggesting that these transcription factors engage extensively in auto- and cross-regulation (Eulgem et al., 1999; Turck et al., 2004).
The L1 box (L1BX) was identified as an essential promoter sequence for the expression of the A. thaliana PROTODERMAL FACTOR1 (PDF1). The PDF1 gene encodes a putative extracellular proline-rich protein that is exclusively expressed in the L1 layer of shoot apices and the protoderm of organ primordia. Electrophoretic mobility shift assays demonstrated that the L1-specific homeodomain protein ATML1 can bind to the L1 box sequence in vitro (Abe et al., 2001). This protein belongs to the HD-ZIP IV class homeodomain (HD) proteins that are expressed exclusively in the L1 layer of the shoot apical meristem (SAM) (Lu et al., 1996). The homeodomain consists of 60 amino acids starting with the N-terminal arm followed by three helical regions. Helix 3 of the HD binds in the major groove of DNA, with helices 1 and 2 lying outside the double helix. The N-terminal arm is located in the major groove and makes additional contacts. Different genes coding for the HD-ZIP IV class have been shown in the Arabidopsis genome. Intriguingly, a similar target sequences of the L1 box has been identified in the upstream region of a parsley PR2 gene (Korfhage et al., 1994). Interaction of this element with PRHP, an HD protein isolated as a binding factor to it, has been suggested to play a role in the elicitor-inducible expression of PR2 (Korfhage et al., 1994).
The TATA box is a cis-regulatory element found in the promoter region of many eukaryotic genes. This binding site can interact with transcription factors or histones (Godde et al., 1995; Smale and Kadonaga, 2003). It is normally bound by the TATA-binding protein (TBP) in the process of transcription. The segment coding for the evolutionarily conserved C-terminal DNA-binding domain is unique. Binding of TBP is the first step in the assembly of a transcription complex and is essentially the only step where the particular base sequence of the DNA is read and recognized during this process (Smale and Kadonaga, 2003).
The characteristic feature of the MYCL transcription factors is their basic helix–loop–helix (bHLH) structure, a stretch of 40–50 amino acids containing two amphipathic -helices separated by a linker region (the loop) of varying length. bHLH proteins have a region with conserved positive charges immediately adjacent to the first helix (Murre et al., 1994). Proteins in this group form both homodimers and heterodimers by means of interactions between the hydrophobic residues on the corresponding faces of the two helices. A dimer in which both subunits have the basic region can bind to DNA. While the bHLH domain is evolutionarily conserved, there is little sequence similarity between clades beyond the domain (Morgenstern and Atchley, 1999). The bHLHs that have been characterized function in the transcriptional regulation of genes associated with anthocyanin biosynthesis, phytochrome signalling, globulin expression, fruit dehiscence, carpel and epidermal development, and the circadian clock (Heisler et al., 2001; Rajani and Sundaresan, 2001; Makino et al., 2002). AtMYC2, a bHLH transcription factor, has been shown to function in abscisic acid (ABA)-inducible gene expression under drought stress in plants. Moreover, as a positive regulator of ABA signalling, it plays a role in negative regulation of JA/ethylene-responsive defence genes in Arabidopsis (Abe et al., 2003; Anderson et al., 2004; Boter et al., 2004; Lorenzo et al., 2004).
The myb domain of vertebrates consists of three imperfect tandem repeats (R1, R2, and R3), each forming a helix–turn–helix (HTH) structure of 53 amino acids. Three regularly spaced tryptophan residues, which form a tryptophan cluster in the three-dimensional HTH structure, are characteristic of a MYB repeat. Myb proteins usually have only one (R1) or two imperfect tandem repeats (R2, R3). MYB genes containing two repeats constitute the largest MYB gene family in plants and is subdivided into three groups (MI, MII, MIIG) depending on the sequence of the binding site. An important function for R2R3-type MYB factors is the control of development and determination of cell fate and identity (Oppenheimer et al., 1991; Lee and Schiefelbein, 1999); some are activated in plants in response to environmental factors and hormones (Iturriaga et al., 1996; Hoeren et al., 1998). Most members of the family seem to be involved in control of secondary metabolism or response to secondary metabolites such as flavonoid and phenylpropanoid metabolism and the anthocyanin pathway (Logemann et al., 1995; Moyano et al., 1996; Grotewold et al., 1998). Moreover, MYB factors play a role in the plant defence reactions. NtMYB2 is involved in the stress response of retrotransposon- and defence-related genes. Overexpression of NtMYB2 cDNA in transgenic tobacco plants induced expression of Tto1 and a phenylalanine ammonia lyase (PAL), a gene involved in the defence response to plant development and in response to light, pathogen ingress, mechanical damage, and other stresses (Sugimoto et al., 2000).
Common TFBS modules
Interestingly, several genes of the JA biosynthetic pathway are up-regulated after NO treatment: all three 12-oxophytodienoate reductases (OPR1, OPR2, and OPR3) and two lipoxygenases (LOX3 and a putative lipoxygenase protein). The Genomatix program Frameworker was used to search for common TFBS modules in the promoter regions of the JA biosynthetic pathway genes. Two modules common to three genes each and consisting of four TFBS elements were identified (Fig. 3). One is present in the promoter region of LOX3, OPR1, and a putative OPR, and is formed by OPAQ, OCSE, GBOX, and MYBL elements (Fig. 3A). The second module is present in LOX3, OPR3, and a putative LOX gene, and is composed of MADS, GBOX, and MYBL (Fig. 3B). These modules inside the promoters represent a possible explanation of the co-expression of some genes of the JA biosynthetic pathway after NO treatment. As already shown, a particular physiological process can induce a distinct set of genes responsible for the elevation of JA levels in plants (He et al., 2002). For example, LOX2 is required for the wound-induced synthesis of JA in leaves (Bell et al., 1995). Furthermore, OPR1, OPR3, and LOX3 are reported to be overexpressed during leaf senescence, while OPR2 appears to be constitutively expressed throughout the different stages of leaf development, and LOX2 is down-regulated in senescent leaves (He et al., 2002).
|
In several reports, the correlation between NO and JA is discussed controversially. Huang et al. (2004) showed JA- and wounding-dependent NO production by diamino-fluoresceins (DAFs). Using a cDNA microarray made up of
330 defence-related genes, they observed the induction of three genes involved in wounding-induced JA biosynthesis (allene oxide synthase, LOX2, and OPR3). Although NO activates genes involved in JA biosynthesis, it did not affect JA levels in Arabidopsis and showed an extremely weak or almost no accumulation of JA-dependent late defence genes (Huang et al., 2004). In Taxus cell cultures, exogenously supplied methyl jasmonate (MeJA) induced rapid production of NO, and the MeJA-induced intracellular malondialdehyde (MDA), LOX, and PAL were all enhanced by an NO donor, but suppressed by NO inhibitors, underlining the connection between NO and JA signalling (Wang and Wu, 2005). In leaf senescence, the role of NO and JA is still controversial. Although it was demonstrated that exogenous application of JA or MeJA induces leaf senescence (Ueda and Kato, 1980) and that the endogenous JA level in senescing leaves increased to nearly 500% of that in non-senescent leaves (He et al., 2002), the role of JA in this process remains unclear. NO also seems to affect this phase of the plant life cycle. It is hypothesized that a stoichiometric relationship between the two gases NO and ethylene probably determined whether senescence took place or not (Leshem and Haramaty, 1996; Leshem and Pinchasov, 2000). |
Conclusion |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Taken together, such a bioinformatics approach is a useful tool to identify common TFBSs and promoter modules in co-regulated genes, which might be involved in establishing specific expression profiles. Since co-expression can be due to a variety of co-regulatory mechanisms, such analyses may be a first step to provide the basis to understanding the regulatory networks involved in gene expression profiles. Next, the involvement of the identified motifs in the NO response should be experimentally validated.
|
Supplementary data |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Supplementary data containing the microarray and the MatInspector analyses results are available at JXB online.
|
Acknowledgements |
|---|
Our work was supported by the Deutsche Forschungsgemeinschaft (DFG).
|
Footnotes |
|---|
* Present address: Institute of Biological Science and Technology, Hainan University, Haikou, PR China.
|
References |
|---|
|
TopAbstractIntroductionMaterial and methodsResults and discussionConclusionSupplementary dataReferences |
|---|
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell (2003) 15:63–78.
Abe M, Takahashi T, Komeda Y. Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. The Plant Journal (2001) 26:487–494.[CrossRef][Web of Science][Medline]
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K. Antagonistic interaction between abscisic acid and jasmonate–ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell (2004) 16:3460–3479.
Bell E, Creelman R, Mullet J. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences, USA (1995) 92:8675–8679.
Boter M, Ruiz-Rivero O, Abdeen A, Prat S. Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes and Development (2004) 18:1577–1591.
Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics (2005) 21:2933–2942.
Chen W, Provart NJ, Glazebrook J, et al. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell (2002) 14:559–574.
Chen WQ, Singh KB. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. The Plant Journal (1999) 19:667–677.[CrossRef][Web of Science][Medline]
Choi H, Hong J, Ha J, Kang J, Kim SY. ABFs, a family of ABA-responsive element binding factors. Journal of Biological Chemistry (2000) 275:1723–1730.
Cormack RS, Eulgem T, Rushton PJ, Kochner P, Hahlbrock K, Somssich IE. Leucine zipper-containing WRKY proteins widen the spectrum of immediate early elicitor-induced WRKY transcription factors in parsley. Biochimica et Biophysica Acta (2002) 1576:92–100.[Medline]
Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature (1998) 394:585–588.[CrossRef][Medline]
Dong J, Chen C, Chen Z. Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Molecular Biology (2003) 51:21–37.[CrossRef][Web of Science][Medline]
Droge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C. Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO Journal (1997) 16:726–738.[CrossRef][Web of Science][Medline]
Durner J, Wendehenne D, Klessig DF. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences, USA (1998) 95:10328–10333.
Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein–DNA complex. Cell (1992) 71:1223–1237.[CrossRef][Web of Science][Medline]
Eulgem T, Rushton PJ, Robatzek S, Somssich IE. The WRKY superfamily of plant transcription factors. Trends in Plant Science (2000) 5:199–206.[CrossRef][Web of Science][Medline]
Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO Journal (1999) 18:4689–4699.[CrossRef][Web of Science][Medline]
Garcia-Mata C, Lamattina L. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiology (2002) 128:790–792.
Godde JS, Nakatani Y, Wolffe AP. The amino-terminal tails of the core histones and the translational position of the TATA box determine TBP/TFIIA association with nucleosomal DNA. Nucleic Acids Research (1995) 23:4557–4564.
Grotewold E, Chamberlin M, Snook M, Siame B, Butler L, Swenson J, Maddock S, Clair G, Bowen B. Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. The Plant Cell (1998) 10:721–740.
Hausladen A, Privalle CT, Keng T, DeAngelo J, Stamler JS. Nitrosative stress: activation of the transcription factor OxyR. Cell (1996) 86:719–729.[CrossRef][Web of Science][Medline]
He Y, Fukushige H, Hildebrand DF, Gan S. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiology (2002) 128:876–884.
Heisler MG, Atkinson A, Bylstra YH, Walsh R, Smyth DR. SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development (2001) 128:1089–1098.[Abstract]
Hobo T, Kowyama Y, Hattori T. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proceedings of the National Academy of Sciences, USA (1999) 96:15348–15353.
Hoeren FU, Dolferus R, Wu Y, Peacock WJ, Dennis ES. Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. Genetics (1998) 149:479–490.
Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta (2004) 218:938–946.[CrossRef][Web of Science][Medline]
Huang X, von Rad U, Durner J. Nitric oxide induces the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta (2002) 215:914–923.[CrossRef][Web of Science][Medline]
Iturriaga G, Leyns L, Villegas A, Gharaibeh R, Salamini F, Bartels D. A family of novel myb-related genes from the resurrection plant Craterostigma plantagineum are specifically expressed in callus and roots in response to ABA or desiccation. Plant Molecular Biology (1996) 32:707–716.[CrossRef][Web of Science][Medline]
Izawa T, Foster R, Chua NH. Plant bZIP protein DNA binding specificity. Journal of Molecular Biology (1993) 230:1131–1144.[CrossRef][Web of Science][Medline]
Johnson CS, Kolevski B, Smyth DR. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. The Plant Cell (2002) 14:1359–1375.
Kim SR, Choi JL, Costa MA, An G. Identification of G-box sequence as an essential element for methyl jasmonate response of potato proteinase inhibitor II promoter. Plant Physiology (1992) 99:627–631.
Korfhage U, Trezzini GF, Meier I, Hahlbrock K, Somssich IE. Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. The Plant Cell (1994) 6:695–708.
Lara P, Onate-Sanchez L, Abraham Z, Ferrandiz C, Diaz I, Carbonero P, Vicente-Carbajosa J. Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. Journal of Biological Chemistry (2003) 278:21003–21011.
Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. The Plant Journal (1998) 16:223–233.[CrossRef][Web of Science][Medline]
Lee MM, Schiefelbein J. WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell (1999) 99:473–483.[CrossRef][Web of Science][Medline]
Leshem Y, Haramaty E. The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. Journal of Plant Physiology (1996) 148:258–263.[Web of Science]
Leshem YY, Pinchasov Y. Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch.) and avocados Persea americana (Mill.). Journal of Experimental Botany (2000) 51:1471–1473.
Li J, Brader G, Palva ET. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell (2004) 16:319–331.
Lindermayr C, Saalbach G, Bahnweg G, Durner J. Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. Journal of Biological Chemistry (2006) 281:4285–4291.
Lindermayr C, Saalbach G, Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiology (2005) 137:921–930.
Logemann E, Parniske M, Hahlbrock K. Modes of expression and common structural features of the complete phenylalanine ammonia-lyase gene family in parsley. Proceedings of the National Academy of Sciences, USA (1995) 92:5905–5909.
Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. The Plant Cell (2004) 16:1938–1950.
Lu P, Porat R, Nadeau JA, O'Neill SD. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. The Plant Cell (1996) 8:2155–2168.[Abstract]
Makino S, Matsushika A, Kojima M, Yamashino T, Mizuno T. The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana. I. Characterization with APRR1-overexpressing plants. Plant and Cell Physiology (2002) 43:58–69.
Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics (2000) 26:403–410.[CrossRef][Web of Science][Medline]
Metallo SJ, Schepartz A. Certain bZIP peptides bind DNA sequentially as monomers and dimerize on the DNA. Nature Structural Biology (1997) 4:115–117.[CrossRef][Web of Science][Medline]
Morgenstern B, Atchley WR. Evolution of bHLH transcription factors: modular evolution by domain shuffling? Molecular Biology and Evolution (1999) 16:1654–1663.[Abstract]
Moyano E, Martinez-Garcia JF, Martin C. Apparent redundancy in myb gene function provides gearing for the control of flavonoid biosynthesis in antirrhinum flowers. The Plant Cell (1996) 8:1519–1532.[Abstract]
Murre C, Bain G, van Dijk MA, Engel I, Furnari BA, Massari ME, Matthews JR, Quong MW, Rivera RR, Stuiver MH. Structure and function of helix–loop–helix proteins. Biochimica et Biophysica Acta (1994) 1218:129–135.[Medline]
Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell (1991) 67:483–493.[CrossRef][Web of Science][Medline]
Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL. Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnology Journal (2004) 2:359–366.[CrossRef][Web of Science][Medline]
Park CY, Lee JH, Yoo JH, et al. WRKY group IId transcription factors interact with calmodulin. FEBS Letters (2005) 579:1545–1550.[CrossRef][Web of Science][Medline]
Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M. Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. The Plant Cell (2004) 16:2785–2794.
Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M. Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Molecular Plant–Microbe Interactions (2003) 16:1094–1105.[CrossRef]
Quandt K, Frech K, Karas H, Wingender E, Werner T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Research (1995) 23:4878–4884.
Rajani S, Sundaresan V. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Current Biology (2001) 11:1914–1922.[CrossRef][Web of Science][Medline]
Ratcliffe OJ, Riechmann JL. Arabidopsis transcription factors and the regulation of flowering time: a genomic perspective. Current Issues in Molecular Biology (2002) 4:77–91.[Medline]
Riechmann JL, Heard J, Martin G, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science (2000) 290:2105–2110.
Rizhsky L, Liang H, Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology (2002) 130:1143–1151.
Robatzek S, Somssich IE. A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. The Plant Journal (2001) 28:123–133.[CrossRef][Web of Science][Medline]
Rushton PJ, Reinstadler A, Lipka V, Lippok B, Somssich IE. Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. The Plant Cell (2002) 14:749–762.
Russwurm M, Koesling D. NO activation of guanylyl cyclase. EMBO Journal (2004) 23:4443–4450.[CrossRef][Web of Science][Medline]
Schmidt HH, Walter U. NO at work. Cell (1994) 78:919–925.[CrossRef][Web of Science][Medline]
Smale ST, Kadonaga JT. The RNA polymerase II core promoter. Annual Review of Biochemistry (2003) 72:449–479.[CrossRef][Web of Science][Medline]
Sokolovski S, Blatt MR. Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiology (2004) 136:4275–4284.
Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel D, Valeri CR, Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proceedings of the National Academy of Sciences, USA (1992) 89:7674–7677.
Sugimoto K, Takeda S, Hirochika H. MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. The Plant Cell (2000) 12:2511–2528.
Sun C, Palmqvist S, Olsson H, Boren M, Ahlandsberg S, Jansson C. A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. The Plant Cell (2003) 15:2076–2092.
Takatsuji H. Zinc-finger transcription factors in plants. Cellular and Molecular Life Sciences (1998) 54:582–596.[CrossRef][Web of Science][Medline]
Turck F, Zhou A, Somssich IE. Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to its native promoter and the defense-related gene PcPR1-1 in parsley. The Plant Cell (2004) 16:2573–2585.
Ueda J, Kato J. Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiology (1980) 66:246–249.
Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogens (2006) 2, e123.
Wang JW, Wu JY. Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant and Cell Physiology (2005) 46:923–930.
Wendehenne D, Pugin A, Klessig DF, Durner J. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends in Plant Science (2001) 6:177–183.[CrossRef][Web of Science][Medline]
Xu X, Chen C, Fan B, Chen Z. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant Cell (2006) 18:1310–1326.
Yamasaki K, Kigawa T, Inoue M, et al. Solution structure of an Arabidopsis WRKY DNA binding domain. The Plant Cell (2005) 17:944–956.
Yu D, Chen C, Chen Z. Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. The Plant Cell (2001) 13:1527–1540.
Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology (2004) 134:849–857.
Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Molecular Plant–Microbe Interactions (2000) 13:191–202.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||