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First published online June 1, 2004; 10.1104/pp.103.038109 Plant Physiology 135:927-937 (2004) © 2004 American Society of Plant Biologists Type-B Response Regulators Display Overlapping Expression Patterns in Arabidopsis1Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 (M.G.M., G.E.S); Department of Biochemistry and Molecular Biology (J.L.) and Department of Plant Biology (D.E.M.), University of New Hampshire, Durham, New Hampshire 03824; and Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599 (J.J.K.)
Two-component signaling systems, involving His kinases, His-containing phosphotransfer proteins, and response regulators, have been implicated in plant responses to hormones and environmental factors. Genomic analysis of Arabidopsis supports the existence of 22 response regulators (ARRs) that can be divided into at least two distinct groups designated type-A and type-B. Phylogenetic analysis indicates that the type-B family is composed of one major and two minor subfamilies. The expression of the type-B ARRs was examined by using both reverse transcription-PCR and  -glucuronidase fusion constructs. The major subfamily of type-B ARRs showed particularly high expression in regions where cytokinins play a significant role, including cells in the apical meristem region and in young leaves that would be undergoing cell division. Multiple members within this same subfamily of type-B ARRs were expressed near the root tip with highest expression in the root elongation zone. -Glucuronidase-fusions to full-length ARR2, ARR12, and ARR19 were nuclear localized, consistent with a role in transcriptional regulation. These data suggest that differing expression levels of the type-B ARRs may play a role in modulating the cellular responses to cytokinin.
Plant two-component signaling systems have been implicated in vital cellular processes such as the responses to cytokinins, ethylene, red light, and osmosensing (Schaller, 2000  ; Hutchison and Kieber, 2002; Hwang et al., 2002; Schaller et al., 2002). Two-component systems were originally identified in bacteria, and in their simplest form involve a receptor kinase that autophosphorylates itself on a conserved His residue in response to an environmental stimulus (Mizuno, 1997; Stock et al., 2000). This phosphate is then transferred to a conserved Asp residue within the receiver domain of a response regulator. Phosphorylation of the response regulator modulates its ability to mediate downstream signaling in the pathway. Of particular relevance to plants is a permutation on the two-component system known as the multi-step phosphorelay (Swanson et al., 1994; Schaller, 2000). The multi-step phosphorelay makes use of three components: a hybrid receptor kinase that contains both His-kinase and receiver domains in one protein, a His-containing phosphotransfer (HPt) protein, and a separate response regulator. In these multi-step phosphorelays the phosphate is transferred from amino acid to amino acid in sequence His to Asp to His to Asp.
In Arabidopsis, proteins with homology to all elements of the two-component system have been identified, including His kinases, response regulators, and HPt proteins (Schaller, 2000
Two-component signaling elements have been clearly implicated in cytokinin signal transduction (Hwang and Sheen, 2001
According to this model, type-B response regulators play a pivotal role in the early response of plants to cytokinin. None, however, were previously identified in screens for mutants with altered cytokinin sensitivity. Through use of reverse genetic approaches, a T-DNA insertion mutant in ARR1 was shown to shift but not eliminate the cytokinin sensitivity of the mutant plant (Sakai et al., 2001
The Type-B ARR Gene Family of Arabidopsis
Analysis of the Arabidopsis genome reveals the presence of 22 response regulators with all the residues required for activity (Schaller et al., 2002
An unrooted phylogenetic tree based on the receiver domain was constructed using bootstrap analysis (Fig. 1B). The 10 type-A response regulators all fall on one branch. The type-B response regulators form three distinct subfamilies. The largest subfamily, hereafter referred to as subfamily I, contains ARR1, ARR2, ARR10, ARR11, ARR12, ARR14, and ARR18. Notably, this subfamily contains ARR1, ARR2, and ARR11 that have been previously implicated in cytokinin responses based on loss-of-function and/or overexpression studies (Hwang and Sheen, 2001 ; Sakai et al., 2001; Imamura et al., 2003). A second subfamily (subfamily II) of the type-B response regulators is composed of ARR13 and ARR21. A third subfamily (subfamily III) of the type-B response regulators is composed of ARR19 and ARR20. The response regulator ARR22 does not group with members of the type-A or type-B families, and previous analysis indicates that it is more closely related to the receiver domains of the hybrid His kinases than to those of the other Arabidopsis response regulators (Schaller et al., 2002). Among the pseudo response regulators, APRR1, 3, 5, 7, and 9, which are implicated in the circadian clock mechanism (Matsushika et al., 2000; Strayer et al., 2000; Makino et al., 2001), all fall on one branch of the phylogenetic tree. In contrast, APRR4, which contains a GARP domain (Schaller et al., 2002), is as closely related to subfamily I of the type-B ARRs as it is to any of the pseudo response regulators. Analysis of intron positions (Fig. 1C) supports the phylogenetic analysis of the Arabidopsis response regulators. The type-A response regulators all contain four introns, similarly positioned, within their receiver domains. In contrast, the type-B response regulators contain only two introns, similarly positioned, within their receiver domains. Most of the type-B response regulators, including all members of subfamily I, contain an additional two introns of similar position in their C-terminal extensions. ARR13 and 21 of subfamily II share intron positions in their C-terminal extensions not found in the other type-B subfamilies. Members of the circadian subfamily of pseudo response regulators contain two shared intron positions within their receiver domains and a third conserved intron position (lacking in the type-A and type-B ARRs) just C-terminal to the receiver domain.
To obtain an overview of ARR expression throughout the plant, RNA was extracted from Arabidopsis, reverse transcribed, and the resultant cDNA analyzed for the relative levels of each type-B ARR by PCR (Fig. 2). Expression was examined in whole seedlings grown in the light or in the dark. This provided a means to assess whether there were any apparent effects of light upon expression of the ARR genes. In addition, one could potentially detect expression in whole seedlings that might be missed when only examining isolated tissues. This analysis supports expression for all members of subfamily I of the type-B response regulators. This analysis also suggests that the expression of ARR14 is light regulated, because ARR14 had a low level of expression in etiolated seedlings compared to light-grown seedlings of similar age (Fig. 2).
Expression of the ARR genes was also examined in various tissues isolated from plants grown in the light, including roots, mature leaves, stems, flowers (with buds and floral meristem), and green siliques (Fig. 2). Transcripts from the members of subfamily I were detected in all tissues tested, although at differing levels. ARR1, 2, 10, 11, and 12, in particular, had broad patterns of expression consistent with previous expression studies of ARR1, ARR2, and ARR10 (Sakai et al., 1998 ; Imamura et al., 1999). ARR14 and ARR18 demonstrated greater specificities of expression (Fig. 2) but could be detected in all tissues when examined by reverse transcription (RT)-PCR using increased numbers of cycles (results not shown). The presence of ARR14 transcript at low levels in roots compared to aerial tissues provides additional evidence for light regulation of ARR14 expression. Members of subfamilies II and III were more restricted than members of subfamily I in expression, being found predominantly in the flowers and/or siliques. A transcript for ARR13 was not detected even when different primer combinations were tested.
Expression of the type-B ARR proteins was also investigated by use of fusions with the
RT-PCR data shows that the members of subfamily I are broadly expressed throughout the plant (Fig. 2). In particular, transcripts for ARR1, ARR2, ARR10, ARR11, and ARR12 were readily detectable in most tissues tested. Consistent with this, GUS analysis also revealed overlapping expression of these ARRs, most notably within the shoot apical meristem region and in young rosette leaves (Fig. 4A). As leaf development progressed, GUS activity of the ARR fusions was predominantly observed at the leaf base adjacent to the petiole. Activity of ARR10::GUS was detected more readily than that of the other four ARR::GUS fusions in multiple transgenic lines, potentially indicating a higher level of expression for ARR10 under these growth conditions.
In contrast to what was observed in young leaves, expression of the GUS fusions for ARR1, ARR2, ARR10, and ARR12 was localized to specific cell types and regions within the mature leaf. Expression for ARR11::GUS dropped to below detectable limits in mature leaves. Expression of the ARR1, ARR2, ARR10, and ARR12 GUS-fusions was predominantly in the vascular tissue and the hydathodes (Fig. 4A). ARR10::GUS and ARR12::GUS showed consistent staining along the length of the vasculature. In contrast, ARR2::GUS staining appeared intermittently along the leaf vascular system (Fig. 4A, ARR2-b). A similar staining pattern was occasionally seen in ARR1p::GUS lines (data not shown). These patches of expression appear randomly along the vascular tissue and do not appear to be associated with vascular junctions. In addition to vascular staining, ARR2::GUS and ARR12::GUS were found in leaf and floral stem trichomes (Fig. 4, ARR2a; Fig. 6). ARR12::GUS was only found in the trichomes at the base of young rosette leaves, whereas ARR2::GUS was observed in trichomes on leaves of all ages.
We also observed overlapping patterns of expression for subfamily I members within the roots. GUS activity for the ARR1, ARR2, ARR10, and ARR12 fusions was observed in the zone of elongation near the root tip (Fig. 5). Within lines showing higher levels of GUS expression (Fig. 5, ARR2), it appears that a gradient of increasing ARR::GUS activity begins at the root meristem, reaches a peak in the zone of elongation, and then decreases to below detectable limits in mature roots. In addition to being found at the root tip, GUS fusions of ARR2, ARR10, and ARR12 were found associated with developing lateral roots. Expression was initially observed in the vascular tissue of the main root adjacent to the site of lateral root formation. As lateral roots developed, the ARR::GUS fusions took on the expression patterns observed with the primary root tip. Occasionally ARR11::GUS was detected in the root-shoot junction but was not observed near the root tip or lateral root junctions (data not shown).
Within the floral structures, GUS expression for the ARR1 construct was observed in young developing anthers (Fig. 4B), consistent with the ready detection of ARR1 in flowers by RT-PCR (Fig. 2). However, as the anthers matured, ARR1p::GUS activity decreased to below the limit of detection. RT-PCR reveals that ARR14 and ARR18 are unique members of subfamily I in that they display pronounced expression in a subset of tissues (Fig. 2). RT-PCR revealed a higher level of ARR14 expression in leaves than in other tissues examined. Likewise, GUS analysis revealed ARR14 expressed predominantly in young leaf tissue, although its expression decreased as the leaves matured (Fig. 4A). ARR18::GUS was observed in developing anthers (Fig. 4B), consistent with transcript being detected in flowers by RT-PCR (Fig. 2). Like other members of subfamily I, ARR18::GUS was also found in young leaf tissue, its expression decreasing to below detection levels in mature leaves (Fig. 4A).
Comparison of the intron-exon structure and sequence of ARR13 with its close relative, ARR21, suggested that the original ARR13 genomic annotation had incorrectly predicted the C terminus of ARR13. GUS constructs were made to ARR13 and ARR21 based on shared features that were consistent with the genomic annotation for the C terminus of ARR21. Although we were not able to observe any tissue staining using the full-length ARR13::GUS fusion, we were able to detect GUS activity using a promoter fusion construct (ARR13p::GUS). ARR13p::GUS showed relatively strong GUS expression only in the aerial portions of the plants, particularly in young leaves (Fig. 4A). Like many of the subfamily I genes, ARR13p::GUS expression became predominantly localized to the vascular tissue as the leaves matured. ARR13p::GUS was also seen in the vascular tissue of the sepals (Fig. 4B). For ARR21::GUS, we observed weak GUS activity in germinating seedlings (data not shown), but did not observe consistent GUS staining patterns in mature plants despite the detection of transcripts in siliques by RT-PCR.
ARR19::GUS expression was observed in the trichomes at the base of the youngest rosette leaves (Fig. 6) similar to that of subfamily I member, ARR12. However, unlike ARR12, ARR19 was not observed in the roots, shoot apical meristem, or mature leaves. Additionally, we did not detect the expression of the ARR19::GUS fusion in the silique, even though RT-PCR supports its expression in this tissue. GUS activity for the second member of subfamily III, ARR20, was observed in the mature pistil tip (Fig. 4B), consistent with expression in the flower as determined by RT-PCR. ARR20::GUS was also observed in the shoot apical meristem region as well as the vascular tissue and hydathodes of leaves (Fig. 4A).
Previous work has shown that ARR1, ARR2, and ARR10 under the control of the 35S promoter will localize to the nucleus of transiently transformed onion (Allium cepa) or parsley (Petroselinum crispum) cells (Sakai et al., 2000
The type-B response regulators function in the final step of Arabidopsis histidyl-aspartyl phosphorelays and are thought to be transcription factors based on several lines of evidence. First, all type-B ARRs contain a GARP domain shown capable of directly binding DNA in studies of ARR10 (Hosoda et al., 2002 ). Second, several members of subfamily I (ARR1, ARR2, ARR10, and ARR11) can bind specific DNA sequences and enhance transcription (Sakai et al., 2000, 2001; Hosoda et al., 2002; Imamura et al., 2003). Third, type-B ARRs contain putative nuclear localization signals and transiently expressed subfamily I members (ARR1, ARR2, and ARR10) are localized to the nucleus (Sakai et al., 2000; Imamura et al., 2001; Lohrmann et al., 2001; Hosoda et al., 2002). Consistent with a role in transcription, we have localized ARR2, ARR12, and ARR19 GUS-fusions under control of their native promoters to the nucleus. Notably, whereas previous analyses were confined to members of subfamily I, ARR19 is a member of subfamily III. Our results thus support a general role for the type-B ARRs in transcription that is not limited to specific subfamilies.
Both RT-PCR and GUS analysis reveals that type-B ARRs have overlapping expression patterns in Arabidopsis. These results are consistent with those recently reported by Tajima et al. (2004)
A subset of subfamily I members are also expressed in mature leaf tissue. The expression of the ARR1, ARR2, ARR10, and ARR12 GUS fusions appeared ubiquitous throughout the young leaves. However, as the leaves matured, these proteins became predominantly localized to the vascular tissue and the hydathodes (Fig. 4A). Two out of these four subfamily I members, ARR2 and ARR12, were also found to be expressed in trichomes (Fig. 6). This suggests that the type-B ARRs have different functions within leaves of different developmental stages and/or that their activity is mainly required by particular cell types as the leaves mature. ARR2::GUS fusions produced patchy leaf vascular staining in which GUS activity appears randomly along the vascular tissue (Fig. 4A, ARR2-b). A similar staining pattern was occasionally observed in ARR1p::GUS plants (data not shown). The expression pattern of type-B ARRs in mature leaves may relate to the regulation of leaf vascular differentiation, because cytokinin-deficient plants had reduced leaf vasculature (Werner et al., 2003 ). The expression pattern may also explain the seemingly random emergence of adventitious buds along the vascular tissue of plants overexpressing the ipt gene for cytokinin biosynthesis (Estruch et al., 1991). The results of this previous study had suggested that different cells in the leaf have different cytokinin sensitivities and thus different capacities to produce new meristemoids (Estruch et al., 1991), a capacity that could potentially be mediated by the varying cellular levels of type-B ARRs.
Overlapping expression of subfamily I members ARR1, ARR2, ARR10, and ARR12 was also observed in the lateral root junctions and root tips, with each ARR forming a gradient of increasing ARR::GUS activity beginning in the root meristem, reaching a peak in the zone of elongation and then decreasing below detectable limits in the mature root (Fig. 5). This localization is interesting in light of the role of cytokinins in inhibiting both root growth rate and the formation of lateral roots, a role that contrasts with the stimulatory effect of cytokinin upon shoot growth (Werner et al., 2001 RT-PCR and GUS analysis reveals that the members of subfamilies II and III have unique expression patterns but that these still overlap to some extent with those of subfamily I members. For example, ARR19 (subfamily III) is expressed in young trichomes, similar to ARR2 and ARR12 (Fig. 6). However, unlike these subfamily I ARRs, ARR19 was not detected in the shoot apical meristem, the vascular tissue of mature leaves, or the roots. ARR13::GUS expression (subfamily II) overlaps with several subfamily I members in aerial tissues but, unlike them, is not detected in root tissues. From the expression analysis, it is clear that there is overlapping expression among the type-B family members. ARR1, ARR2, ARR10, and ARR12 from subfamily I in particular are expressed in many of the same cell types. However, the overall pattern of expression for each ARR is distinct, the differences being most apparent when examined in mature differentiated cell types. For example, ARR::GUS fusions were expressed in three different structures of the flower: ARR1 and ARR18 were found in the anthers, ARR13 was found in the sepal vasculature, and ARR20 was found at the pistil tip (Fig. 4B). Although not a focus of this study, the potential light regulation of ARR14 expression suggests that the patterns of expression for each ARR may also differ based on environmental signaling factors.
Based on the finding that multiple type-B ARRs are expressed in regions of the shoot undergoing rapid cell division, it will be of interest to determine the extent of the correlation between type-B ARR expression and cell division in proliferating tissues. In preliminary experiments, we did not observe GUS activity in developing embryos, although several lines of ARR1p::GUS and ARR10::GUS did display GUS activity in the funiculus (data not shown). The inability to detect type-B ARR expression in embryos may indicate that the level of type-B ARR::GUS activity was below detectable limits and/or that this ARR-mediated signaling pathway has a more restricted role in embryogenesis. The wol1 mutation, for example, is within a gene encoding a cytokinin receptor, but its effect is not until the torpedo stage of embryogenesis and is restricted to cell division of the vascular initials (Mahonen et al., 2000
Analysis of ARR gene expression provides limited functional relevance by itself although, based on previous studies, potential functional roles of type-B ARRs can be inferred. Because a correlation has been made between type-B ARRs and cytokinin signal transduction (Hwang and Sheen, 2001
In conclusion, type-B response regulators display distinct, yet overlapping expression patterns in Arabidopsis, with subfamily I members showing the broadest expression throughout the plant. The more specific localization of subfamily II and III members suggests that these proteins may play more specialized roles in plant growth and development. Expression of type-B ARRs, in particular subfamily I members, overlaps with the expression of cytokinin primary response genes such as those encoding type-A ARRs (D'Agostino et al., 2000
Phylogenetic Analysis
The receiver domain for each response regulator was determined by analysis using the Simple Modular Architecture Research Tool search algorithms (http://smart.embl-heidelberg.de; Schultz et al., 1998
Wild-type Arabidopsis (ecotype Columbia) was used for all experiments. Tissues used for RT-PCR were obtained from plants grown on soil, liquid media, and agar plates. Growth on soil involved stratifying the sown seeds at 4°C for 3 d prior to their incubation at 22°C under a 16-h light (fluorescent illumination)/8-h dark cycle. Seeds germinated on plates for use in RT-PCR experiments were surface-sterilized and then sown on 0.8% (w/v) agar plates of one-half-strength Murashige and Skoog (MS) basal medium (pH 5.7) containing Gamborg's vitamins (MS media, Sigma-Aldrich, St.Louis). Seeds were stratified at 4°C for 3 d and then placed under constant light at 22°C for 8 d. Plants grown for GUS histochemical analysis were grown similarly to plants used for RT-PCR except the seeds were sown onto full-strength MS media containing 0.1% (w/v) Suc and grown for approximately 3 weeks under constant light. For growth of etiolated seedlings, sown seeds were exposed to light for 12 h and then grown in the dark for 3 d. For growth of plants in liquid media, seeds were surface sterilized and placed in 50-mL one-half-strength MS media containing 1% (w/v) Suc under a 16-h light/8-h dark cycle for 16 d.
Total RNA was isolated using the RNeasy plant mini kit (Qiagen, Valencia, CA) from 3.5-d-old dark grown seedlings, 8-d-old green seedlings, 16-d-old roots grown in liquid MS media, and rosette leaves, stems, flowers (including buds and floral meristem), and green siliques from 5-week-old plants. cDNA was synthesized from 1 µg total RNA using the Reverse Transcription System (Promega, Madison, WI) after pretreatment with RNase Free DNase I (Qiagen). PCR reactions were performed using HotMaster Taq (Eppendorf, Westbury, NY). Primers specific for the sequences of interest were designed so that for each primer set at least one primer spans a region that contains an intron in the genomic sequence. The following primers were used for the PCR reactions: EF1, 5'-TAGGGCTGGTATCTCTAAG-3' and 5'-CGAAGGGGCTTGTCTGATG-3'; ARR1, 5'-CTTTTCTTTTTTTGTTTCTTGGGTT-3' and 5'-CGGTATTTCTGGAGGTGACTTG-3'; ARR2, 5'-TTCGGGTACTGCTGCTGGTG-3' and 5'-CTACTGGCAACATCATTCCGCT-3'; ARR10, 5'-CGTTGCTCTGAAGAAGGTGT-3' and 5'-GATTGGCTCTGTTCCTGTGT-3'; ARR11, 5'-CCTGTAATAATGATGTCGGT-3' and 5'-CATAGGAACTTTGACTTGGC-3'; ARR12, 5'-CTGTCATAATGTTGTCTGCG-3' and 5'-TAGAATGCGGTAATGGAGAG-3'; ARR13, 5'-ATGGCTTTTGCTCAATCTGTCT-3' and 5'-TTGGGCACCACCTTATCATAAC-3', 5'-AAAGGACGCAAATGTTAGTGT-3' and 5'-CTATCCGAAGAAAGCATTATC-3', 5'-ATGTACGGATTCGGAATAGAA-3' and 5'-GCCATCATCACTAGGACCAC-3'; ARR14, 5'-ATTATGATGTCTGTTGATGG-3' and 5'-TGTCTGATTCTGTTGTTGTT-3'; ARR18, 5'-AGGCTGTTCCCAAAAAAATA-3' and 5'-TGGTTGTCATTCTCTGGCTT-3'; ARR19, 5'-TTTTACGGTGCTTGTGACTATG-3' and 5'-TGATACGGTGTTTCTGAAGATG-3'; ARR20, 5'-TGACACAGTATTCCTATCAAGTAACGA-3' and 5'-TTGACGGTACTTCTGGAGATGACTG-3'; ARR21, 5'-CCAAATACAGAGATCCATCAG-3' and 5'-ATACGGTGCGGCTCATAG-3'. EF1 was used as an RT-PCR control and the amount PCR template used for the different samples was normalized to the expression level of EF1. The number of PCR cycles used for each ARR was determined such that the level of product from each tissue was in the linear range of the reaction. The amplified fragments were separated by agarose gel electrophoresis, stained with ethidium bromide, digitally scanned under UV light, and the relative intensities of the bands quantified using the software GelExpert 3.5 (Nucleotech, San Carlos, CA).
PCR primers were designed to amplify the genomic clone of each type-B response regulator including approximately 2 kb of DNA upstream of the start of translation and the entire coding sequence up to but not including the translational stop codon. ARR1 was an exception to this, in that 2 kb of the ARR1 promoter and the coding sequence up to and including part its second exon was amplified by PCR. A similar PCR was performed to amplify the ARR13 promoter region in addition to a full-length clone. The PCR products were cloned into a pCAMBIA-3381 vector (Cambia, Canberra, Australia) modified to include the GATEWAY system (Invitrogen Life Technologies, Carlsbad, CA). Constructs were introduced into Agrobacterium tumefaciens strain GV3101 and used to transform Arabidopsis by the floral dipping method (Bent and Clough, 1998
Histochemical analysis of GUS activity in stably transformed lines of Arabidopsis was performed as described (Jefferson et al., 1987
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requestor. Received December 19, 2003; returned for revision January 29, 2004; accepted March 3, 2004.
1 This work was supported by the National Science Foundation (grant no. 0114965 to J.J.K. and G.E.S.) and by the USDA-NRICGP (grant no. 2001–35311–10988 to D.E.M.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.038109. * Corresponding author; e-mail george.e.schaller{at}dartmouth.edu; fax 603–646–1347.
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