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First published online July 16, 2008; 10.1104/pp.108.119164 Plant Physiology 148:337-347 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
A Novel ARID DNA-Binding Protein Interacts with SymRK and Is Expressed during Early Nodule Development in Lotus japonicus1,[C],[W],[OA]State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, China (H.Z., T.C., M.Z., Q.F., H.K., Z.Z.); and Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, Idaho 83844–3052 (Z.H.)
During the establishment of symbiosis in legume roots, the rhizobial Nod factor signal is perceived by the host cells via receptor-like kinases, including SymRK. The NODULE INCEPTION (NIN) gene in Lotus japonicus is required for rhizobial entry into root cells and for nodule organogenesis. We describe here a novel DNA-binding protein from L. japonicus, referred to as SIP1, because it was identified as a SymRK-interacting protein. SIP1 contains a conserved AT-rich interaction domain (ARID) and represents a unique member of the ARID-containing proteins in plants. The C terminus of SIP1 was found to be responsible for its interaction with the kinase domain of SymRK and for homodimerization in the absence of DNA. SIP1 specifically binds to the promoter of LjNIN but not to that of LjCBP1 (a calcium-binding protein gene), both of which are known to be inducible by Nod factors. SIP1 recognizes two of the three AT-rich domains present in the NIN gene promoter. Deletion of one of the AT-rich domains at the NIN promoter diminishes the binding of SIP1 to the NIN promoter. The protein is localized to the nuclei when expressed as a red fluorescence fusion protein in the onion (Allium cepa) epidermal cells. The SIP1 gene is expressed constitutively in the uninfected roots, and its expression levels are elevated after infection by Mesorhizobium loti. It is proposed that SIP1 may be required for the expression of NIN and involved in the initial communications between the rhizobia and the host root cells.
Legume plants are capable of acquiring nitrogen from rhizobacteria maintained symbiotically in specialized root organ nodules that form through a complex developmental process involving an exchange of signals between the host root cells and the bacteria. At the beginning of nodule organogenesis, specific flavonoid metabolites released by the legume roots notify soil rhizobia that a suitable host is nearby. Inside the bacteria, the flavonoids are recognized by a receptor protein known as NodD. The binding of NodD to these flavonoids activates the protein and promotes the transcription of other nod genes involved in the synthesis and secretion of Nod factors, the rhizobial signaling molecules (Peck et al., 2006  ). The common feature of all Nod factors is the presence of a chitin backbone and a fatty acyl tail (Denarie et al., 1996). Rhizobial Nod factors, in turn, are capable of inducing a series of specific responses in the host root cells, including root hair deformation, alkalinization of the cytosol, depolarization of the plasma membrane, and calcium influx and spiking (Ehrhardt et al., 1992, 1996; Kurkdjian, 1995; Felle et al., 1995, 1996; Limpens and Bisseling, 2003; Gleason et al., 2006). Root hair deformation and curling are the early morphological changes induced by rhizobia. Purified Nod factors can cause root hair deformation at concentrations as low as 10–12 M (Lerouge et al., 1990; Spaink et al., 1991; Sanjuan et al., 1992; Margaert et al., 1993), although in most cases curling is only observed when the bacteria are present (Relic et al., 1993).
The perception and signal transduction of Nod factors in the host cells have been subject to intense molecular and genetic studies in recent years. Rhizobial Nod factors have been shown to be recognized by lysin motif (LysM)-containing receptor-like kinases (RLKs), such as NFR1/NFR5 from Lotus japonicus and LYK3 and NFP from Medicago truncatula (Madsen et al., 2003
SymRK from L. japonicus encodes a protein with three Leu-rich repeat (LRR) domains in the predicted extracellular region. Mutations in the SymRK gene abolish the host interaction with rhizobia (Stracke et al., 2002 In this study, we demonstrate that a novel protein, designated as SIP1 for SymRK-interacting protein 1, interacts with the kinase domain of SymRK. SIP1 is a transcription factor containing an AT-rich interaction domain (ARID) and may participate in Nod factor-induced transcriptional activation of genes required for nodule initiation.
Characterization of a SymRK-Associated Protein
The SymRK peptide contains three LRRs, a transmembrane domain, and an intracellular kinase domain. The structure features suggest potential roles of SymRK in the perception of extracellular signals and transduction of the signals through the intracellular kinase domain (Stracke et al., 2002
The full-length SIP1 cDNA (GenBank accession no. EU559710) contained an open reading frame of 1,224 nucleotides encoding a peptide of 408 amino acid residues with a predicted molecular mass of 45.7 kD. Analysis of the peptide sequence revealed the presence of a conserved ARID (Fig. 1B) that has been implicated in sequence-specific DNA binding (Gregory et al., 1996 ). ARID-containing proteins appear to play important roles in diverse biological functions, including cell proliferation and differentiation, and organ development (Herrscher et al., 1995; Gregory et al., 1996; Kortschak et al., 2000). The mouse BRIGHT (B-cell regulator of immunoglobulin H transcription) protein and the fruit fly DRI (Drosophila dead ringer) are two well-characterized ARID-containing transcription factors (Herrscher et al., 1995; Gregory et al., 1996; Valentine et al., 1998; Iwahara et al., 2002; Wilsker et al., 2005). The predicted three-dimensional model of the ARID domain of SIP1 consists of eight  -helices, two β-strands, and four structure-undefined loops (Fig. 1B). The structural features of this 91-residue motif were identical to those found in animal ARID-containing proteins such as DRI (Fig. 1B; Iwahara and Clubb, 1999) and indicated that SIP1 might bind to the AT-rich region of plant promoters.
ARID-containing proteins are widely present in plant genomes. Ten such proteins have been found in Arabidopsis (Fig. 1C) and can be grouped into four subfamilies, designated high-mobility group (HMG), EGL-27 and MTA1 homology 2 (ELM2), plant homeodomain (PHD), and heat stress protein 20-like (Hsp20)-related proteins (Fig. 1D). Animal proteins containing HMG and ELM2 motifs have been implicated in DNA binding and transcription regulation (Ding et al., 2003
To determine which domain of SIP1 is responsible for its interaction with SymRK-PK, we constructed a series of SIP1 deletions in pGADT7 (Fig. 2A ). The N-terminal half of SIP1 (SIP1N) containing the N terminus and the ARID domain was not found to interact with SymRK-PK. The ARID domain alone, SIP1A, also did not interact with SymRK-PK. However, yeast colonies expressing the C terminus of SIP1, SIP1C, were able to grow on the selection medium lacking His (SD/-Leu-Trp-His) and exhibited significant β-galactosidase activities (Fig. 2C), suggesting that the C-terminal 184 amino acid residues of SIP1 are critical for its interaction with SymRK. This interaction was further confirmed using an in vitro protein-protein interaction assay (Fig. 2D). For this assay, SIP1 and its deletion fragments were expressed as His- or chitin-binding domain (CBD)-tagged recombinant proteins and immobilized to nickel beads or chitin beads. After incubation of the beads with purified SymRK-PK, followed by washing with buffer, proteins retained to the beads were eluted in SDS sample buffer and resolved on SDS-PAGE. The presence of SymRK on the beads was detected by immunoblotting with the anti-SymRK antibody. As shown in Figure 2D, only the full-length SIP1 and SIP1C could pull down SymRK-PK, confirming that the C terminus of SIP1 was responsible for its interaction with SymRK.
SIP1 Binds AT-Rich Double-Stranded DNA
The ARID motif of SIP1 contains a noncanonical helix-turn-helix motif (helices H5 and H6) for potential DNA binding. To test this DNA-binding activity, we purified His-tagged SIP1 and performed electrophoretic mobility shift assays (EMSA) with a 32P-end-labeled double-stranded DNA trimer of NP3 or TTA9, the consensus binding sites of the Drosophila homeodomain protein Engrailed (Gregory et al., 1996
We further examined whether SIP1 contains a transcription activation domain (AD). We constructed plasmids that would express the GAL4 DNA-binding domain fused with SIP1 or its deletion fragments. The plasmids were transferred into the yeast strain AH109 that expressed ADE2, HIS3, lacZ, and MEL1 reporter constructs under GAL4-responsive promoters (CLONTECH). If SIP1 contained an AD, the SIP1 fusion protein should bind to the GAL4-responsive promoters and drive the expression of the ADE2, HIS3, lacZ, and MEL1 reporters. A known transcription activator, NSP1 (Smit et al., 2005 ; Heckmann et al., 2006), was used as a positive control and proved able to allow yeast colonies to grow on SD/-Trp-His and SD/-Trp-Ade media (Fig. 3B). However, as shown in Figure 3B, colonies expressing SIP1 and its deletion fragments could not grow on these media, indicating that SIP1 did not contain a transcription AD (Fig. 3B). It would be interesting to test if SIP1 forms hetero-oligomers with other proteins that contain an activator or repressor domain.
The expression of the NIN (nodule inception) and CBP1 (calcium-binding protein 1) genes is induced by Nod factors (Schauser et al., 1999
A search of the promoter region (about 4 kb upstream of the first ATG) of the NIN gene identified three potential AT-rich motifs, located in the regions from –2,299 to –2,287, from –393 to –367, and from –69 to –59 bp, respectively (Borisov et al., 2003 ; Fig. 4A). To determine whether SIP1 binds to these sequences in vitro, we synthesized three oligonucleotides corresponding to Oligo1 to Oligo3 (Fig. 4A) and performed EMSA assays using purified SIP1. As shown in Figure 4B, SIP1 specifically recognized and bound to Oligo1 and Oligo3 but not Oligo2.
Because the 500-bp NIN promoter fragment used in the yeast one-hybrid assay (Fig. 4A) did not contain Oligo1 (Fig. 4C), we hypothesized that Oligo3 should be the AT-rich site for SIP1 binding. We further reasoned that deletion of the Oligo3 site from the NIN promoter should diminish the ability of the yeast cells to grow on SD-His+3-AT medium. We removed a 70-bp fragment (–1 to –69 bp) from the NIN promoter and showed that the
The mouse BRIGHT protein forms a tetramer that binds to DNA (Herrscher et al., 1995
To further confirm this interaction, we immobilized glutathione S-transferase (GST)-SIP1, CBD-SIP1N, and CBD-SIP1C fusion proteins on GST beads or chitin beads and incubated the beads with His-tagged SIP1, SIP1N, and SIP1C, respectively. After washing, the proteins retained on the beads were subjected to immunoblotting with the anti-His-tag antibody. As shown in Figure 5B, GST-SIP1 and CBD-SIP1C could pull down SIP1 (lanes 1 and 3), whereas CBD-SIP1N could not (lane 2). Moreover, CBD-SIP1C was able to pull down SIP1C (lane 6), suggesting the C termini are sufficient to form dimers.
SymRK is expressed constitutively in the roots of Lotus, and its mRNA level does not change upon the treatment with Nod factors for 24 and 48 h or after the inoculation with Mesorhizobium loti (Stracke et al., 2002
We then focused on the expression levels of SIP1 and NIN in roots after infection with M. loti. When inoculated with M. loti, an induction of SIP1 mRNA was observed as early as 5 h post inoculation (hpi). In 24 hpi, the expression levels dropped down to a steady level, which was slightly higher than that observed in the control roots. This expression pattern was distinct from that of NIN (Fig. 6B), which exhibited significant induction 5 h after rhizobial inoculation and maintained a high expression level in inoculated roots. It is important to note that the timing of the SIP1 induction (5 hpi) correlates well with that of NIN. After the initial induction, NIN continued to be expressed at relatively high levels. In conclusion, the SIP1 gene is expressed constitutively in roots and leaves, and its expression levels are elevated in roots transiently (5 hpi–1 d postinoculation [dpi]) after rhizobial infection. It may play a role in the induction of the NIN gene during the process of rhizobial entry and nodule organogenesis.
To determine the subcellular localization of SIP1, we expressed SIP1 as a fusion protein with the Discosoma red fluorescent protein (DsRed) under the control of the cauliflower mosaic virus 35S promoter. The fusion protein was transiently expressed in the onion (Allium cepa) epidermal cells via particle bombardment, and its expression was monitored using a confocal laser-scanning microscope. As expected in the control cells expressing DsRed alone, the red fluorescence was detected only in the cytoplasm (Fig. 7, D–F ). In the onion epidermal cells expressing the SIP1-DsRed fusion protein, the red fluorescence was concentrated to the nuclei (Fig. 7, A–C). This result is consistent with its potential function in DNA binding and transcription regulation. However, it remains to be determined how SIP1 interacts with SymRK in Lotus roots after rhizobial infection.
SymRK is a member of a large family of LRR RLKs in plants and is required for the legume root cells to perceive the Nod factor signals released by the infecting rhizobia (Yoshida and Parniske, 2005 ). NIN is a key transcription factor required for rhizobial entry into the root cells and for nodule organogenesis (Schauser et al., 1999; Radutoiu et al., 2003). In this report, we describe a novel DNA-binding protein, SIP1, which may provide a link between SymRK and NIN. We demonstrate that SIP1 interacts with the intracellular kinase domain of SymRK (Fig. 2) and specifically binds to the Oligo3 AT-rich site of the NIN promoter (Fig. 4). Because SIP1 does not contain a transcription AD (Fig. 3), it may form hetero-oligomers with other unidentified proteins that contain an activator or repressor domain. Plu-1, a human ARID-containing protein, also lacks an AD but contains transcriptional repressor properties and forms hetero-oligomers with other transcription factors (Tan et al., 2003). The initial signal communications between the rhizobia and roots involve a number of different molecular exchanges culminating in calcium spiking in the host cells. SIP1, by linking the SymRK receptor kinase to the NIN transcription factor, may play a pivotal role for the successful establishment of rhizobia-legume symbiosis.
SIP1 represents a new member of the conserved ARID family of proteins in plants. The ARID domain was initially identified in the mouse BRIGHT protein (Herrscher et al., 1995 The ARID domains, especially their 3-D structures, are conserved between animals and plants (Fig. 1B). However, other parts of the molecules can be very different among ARID-containing proteins in an organism. In Arabidopsis, the 10 ARID-containing proteins vary in length from 319 residues in At3g13350 to 786 residues in At2g17410. They can be grouped into four subfamilies on the basis of their phylogenetic relationship and the presence of functional motifs (Fig. 1D). L. japonicus SIP1 is closely related to the Hsp20 subfamily in Arabidopsis, although it does not contain an Hsp20-like domain. The Hsp20 motif is found in the C termini of the Arabidopsis ARID proteins (Fig. 1C). In L. japonicus SIP1, the C terminus has evolved into a different domain that is responsible for interacting with SymRK (Fig. 2) and for the homodimerization (Fig. 5). SIP1 represents a new ARID-containing transcription factor in plants and is potentially involved in linking the Nod signal perception to the transcriptional regulation during nodule development in L. japonicus.
The ARID domain has not been found in Archea and eubacteria, but is widespread in protozoa, metazoans, green algae, fungi, plants, and animals. There are 15 ARID proteins in the human genome and two in S. cerevisiae (Wilsker et al., 2002
ARID proteins in higher eukaryotes are involved in differentiation and transcriptional regulation of gene expression (Wang et al., 2007 There are three AT-rich motifs in the promoter of the NIN gene, two of which showed affinity with SIP1 in in vitro assays (Fig. 4). In the yeast one-hybrid system, the 500-bp promoter region of the NIN gene was found to contain cis-DNA elements for SIP1 binding. The binding of SIP1 to the NIN promoter was apparently brought about via the Oligo3 AT-rich motif, which is localized to the promoter region between –59 to –69 bp. Because SIP1 does not have a transcription AD (Fig. 3B), it is likely that SIP1 may function as a DNA sequence-specific binding protein and may form an oligomer with another transcription activator or repressor. We are currently in the process of searching for these potential SIP1-interacting partners and examining the biological functions of SIP1 and its associated proteins in nodule organogenesis in L. japonicus. Further analyses of the signaling pathway involving SIP1 may eventually lead to the identification of new molecular events required for the later steps in the symbiotic establishment in legume roots.
Plant Materials
Seeds of Lotus japonicus MG-20 were surface-sterilized in 2% sodium hypochlorite for 8 min and washed seven times with sterile water. The seeds were left to germinate for 48 h at 22°C on sterile water-soaked filter paper in petri dishes in a dark room. Seedlings were subsequently planted in pots on sterile sands supplemented with nitrogen-free Fahraeus medium (Fahraeus, 1957
Total RNA was isolated from the equally mixed roots collected 2, 4, 6, 8, and 12 d after rhizobial inoculation using the TRIzol reagent (Invitrogen). Total RNA (2 µg) was reverse transcribed into single-stranded cDNA using oligo(dT) as the primer. The cDNA was size-fractionated using BD Matchmaker library construction and screening kits (BD Biosciences CLONTECH). The cDNA fragments longer than 500 bp were cotransformed with linearized pGADT7-Rec into yeast (Saccharomyces cerevisiae) AH109 cells. The transformants were selected on SD/-Leu medium according to the manufacturer's instruction. The transformation efficiency was approximately 2 x 106 CFU/3 µg pGADT7-Rec.
The SymRK-PK cDNA (GenBank accession no. AF492655) was amplified by reverse transcription-PCR with the following gene-specific primers: 5'-GGGCATATGATGGAGAGGTACAAAACCTTG-3' and 5'-AAAGAATTCTCTCGGCTGTGGGTGAG-3'. PCR was carried out using ExTaq DNA polymerase (TaKaRa) with an initial denaturation step of 95°C for 5 min, followed by 30 cycles of 95°C for 15 s, 55°C for 30 s, and 72°C for 1 min. After the last cycle, an extension step for 10 min at 72°C was carried out. Purified PCR products were inserted into the Nde1-EcoR1 site of pGBKT7 vector. Screening of interaction clones was carried out according to the manufacturer's instructions (CLONTECH). A total of 1 x 107 transformants from the cDNA library were screened for growth on the SD/-Leu-Trp-His-Ade media. Positive clones were verified by retransformation of the rescued plasmid into the AH109 containing the bait plasmid (pGBKT7-SymRK-PK). Plasmid pGBKT7-Lam (CLONTECH) was used as a negative control. Colonies growing on the SD/-Leu-Trp-His-Ade media were transferred to selective media-containing X-Gal (80 µg/mL) or were left on filters as described (Ma et al., 2007
Yeast cells grown in liquid selection media were pelleted and washed twice with Z-buffer (60 mM Na2HPO4, 40 mM NaH2PO2, 10 mM KCl, 1.0 mM MgSO2, pH 7.0). The cells were resuspended in 300 µL of Z-buffer and permeabilized by two freeze-thaw cycles in liquid nitrogen and 37°C. Cell extracts were added 0.7 mL of Z-buffer containing 50 mM β-mercaptoethanol and 160 µL of O-nitrophenyl β-D-galactopyranoside (4 mg/mL) in Z-buffer. After incubation at 30°C for 30 min or until the yellow color appeared, the reaction was terminated by the addition of 0.4 mL of 1.0 M Na2CO3. The reaction mixture was centrifuged for 10 min at 14,000 rpm to remove cell debris. β-Galactosidase activity in the supernatant was measured at OD420 and expressed in Miller units (Miller, 1972
The full-length cDNA of SIP1 was inserted at the Nde1-Sal1 site of pET28 vector (Novagen), generating pET-SIP1. The 3' region of SIP1 was amplified by PCR using primers 5'-CTTTCTAGACCATATGAAGTCCAGAGAAAGGA-3' and 5'-TTTTGTCGACAAGCTTCACGGCTCCCTG-3'. The fragment was cloned into the Nde1-Sal1 site of pET28a vector, generating pET-SIP1C. The 5' region of SIP1 was amplified using primers 5'-CCGGTACCCATATGGAAATTGTTGAT-3' and 5'-GGGAAGCTTGTCGACTTAGAGCTGTAACTC-3'. The fragment was cloned into the Nde1-Sal1 site of pTYB12 (New England Biolabs), yielding pTYB-SIP1N. For protein expression, Escherichia coli BL21 (Novagen) or ER2566 cells (New England Biolabs) harboring the plasmid were induced with 0.5 mM isopropyl 1-thio-β-D-galactopyranoside in Luria-Bertani broth for 8 h at 16°C. His-tagged proteins were purified using nickel-agarose beads (Qiagen) according to the manufacturer's instruction. CBD-tagged proteins were purified using chitin beads (New England Biolabs) as described previously (Zhang et al., 2003
To assay the interaction between SymRK-PK and SIP1, His-tagged SIP1 and SIP1C were bound to nickel-agarose beads, while CBD-SIP1N was absorbed on the chitin beads. The beads were incubated with 5 µg of purified SymRK-PK protein in the interaction buffer (20 mM Tris-HCl, 100 mM KCl, 2 mM MgCl2, 5% glycerol, pH 8.0) for 1 h on ice with gentle shaking. The nickel beads were washed three times with a buffer solution (137 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 2 mM KH2PO4, 100 mM imidazole, 5% glycerol, pH 8.0), whereas the chitin beads were washed three times with 1.0 mL of TEG buffer (20 mM Tris-HCl, 1 mM EDTA, 5% glycerol, pH 8.0). The retained proteins were eluted by boiling for 3 min in 1x SDS sample buffer (2% SDS, 29.1 mmol/L Tris, pH 6.8, 10% glycerol, and 0.01% bromphenol blue; Zhang et al., 2003
To assay SIP1 dimerization, GST-tagged SIP1 was expressed and purified on glutathione-Sepharose 4B (Sigma) as described elsewhere (Zhang et al., 2000
EMSA of SIP1 was performed on 5% nondenaturing polyacrylamide gels as described previously (Gregory et al., 1996
The SIP1 cDNA amplified using primers 5'-TATACTAGTATGGAAATTGTTGAT-3', and 5'-AAGGTCACCTTACACGGCTCCCTG-3' was cloned into the Spe1/BstEII site of pCAMBIA1302 vector (CAMBIA). We amplified DsRed coding sequence using primer 5'-CAACTAGTATGAGGTCTTCCAAGAATGT-3', and 5'-TTACTAGTAAGGAACAGATGGTGGCGTC-3' from the pDsRed (CLONTECH), and it was inserted into the Spe1 site of the pCAMBIA1302-SIP1 construct, resulting in p35S-DsRed-SIP1. The plasmid was used for transient expression in the onion (Allium cepa) epidermal cells by particles bombardment using a Biolistic PDS-1000/He particle delivery system (Bio-Rad). After incubation for 24 to 48 h at 25°C in dark, the epidermal cell layers were examined using a confocal laser-scanning microscope (Leica).
The SIP1 cDNA was fused to the GAL4 AD in pGADT7-Rec2 (CLONTECH), generating pGADT7-SIP1. The promoter (–1 bp to –500 bp) of the NIN gene (Schauser et al., 1999 The plasmid was transformed into yeast Y187 cells harboring pGADT7-SIP1, which expresses SIP1 fused with the GAL4 transcription AD. The DNA-binding activity of SIP1 was determined by the expression of the HIS3 reporter.
Total RNA was isolated from stems, leaves, control roots, and roots inoculated with M. loti, using a TRIZOL reagent (Invitrogen). RNA samples were treated with DNase I to remove potential contaminating genomic DNA, followed by extraction with phenol:chloroform. The DNA-free RNA samples were confirmed by lack of a PCR product using primers specific to the untranscribed NIN gene promoter (5'-GTTTTCAAGAATGGGAGGGG-3', 5'-CTCCTCTGGTTTCATTGGTG-3'). First-strand cDNA was prepared using Oligo(dT) primer, and quantitative PCR was performed on a Mini Opticon real-time PCR system (Bio-Rad) using One-Step SYBR PrimeScript RT-PCR kit II (Takara). The same cDNA pool was used for amplification of all tested transcripts. The relative quantification software (Bio-Rad) was used to determine the efficiency-corrected relative transcript concentration, normalized to a calibrator sample (Radutoiu et al., 2003 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number EU559710.
The following materials are available in the online version of this article.
We thank Drs. Yongjun Lin, Chunli Chen, and Ms. Huazhi Song for advice on transient expression and confocal laser-scanning microscope. We also thank Dr. Allan Caplan for critical comments on the manuscript. Received March 17, 2008; accepted June 13, 2008; published July 16, 2008.
1 This work was supported by the National Natural Science Foundation of China (grant no. 30570056 to Z.Z.), by the National Basic Research Program of China (grant no. 01CB108901 to Z.Z.), and by the National Science Foundation (grant nos. NSF–MCB 0548525 and NSF–IOB 0543923 to Z.H.).  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: Zhongming Zhang (zmzhang{at}mail.hzau.edu.cn).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[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.108.119164 * Corresponding author; e-mail zmzhang{at}mail.hzau.edu.cn.
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NINpro::HIS3, or CBP1pro::HIS3, which expresses the HIS3 reporter gene under the promoter of the NIN or CBP1 gene. The NIN promoter is a 500-bp fragment (–1 to –500 bp), whereas the 
-32P-end-labeled double-stranded oligonucleotide trimer of the consensus Engrailed binding site NP3 [(TCAATTAAATGA)X3] or trimer of TTA9 [(TTATTATTA)X3; Gregory et al., 1996
