Molecular characterization and differential expression of cytokinin-responsive type-A response regulators in rice (Oryza sativa)
© Jain et al; licensee BioMed Central Ltd. 2006
Received: 16 August 2005
Accepted: 13 February 2006
Published: 13 February 2006
The response regulators represent the elements of bacterial two-component system and have been characterized from dicot plants like Arabidopsis but little information is available on the monocots, including the cereal crops. The aim of this study was to characterize type-A response regulator genes from rice, and to investigate their expression in various organs as well as in response to different hormones, including cytokinin, and environmental stimuli.
By analysis of the whole genome sequence of rice, we have identified ten genes encoding type-A response regulators based upon their high sequence identity within the receiver domain. The exon-intron organization, intron-phasing as well as chromosomal location of all the RT-PCR amplified rice (Oryza sativa) response regulator (OsRR) genes have been analyzed. The transcripts of OsRR genes could be detected by real-time PCR in all organs of the light- and dark-grown rice seedlings/plants, although there were quantitative differences. The steady-state transcript levels of most of the OsRR genes increased rapidly (within 15 min) on exogenous cytokinin application even in the presence of cycloheximide. Moreover, the expression of the OsRR6 gene was enhanced in rice seedlings exposed to salinity, dehydration and low temperature stress.
Ten type-A response regulator genes identified in rice, the model monocot plant, show overlapping/differential expression patterns in various organs and in response to light. The induction of OsRR genes by cytokinin even in the absence of de novo protein synthesis qualifies them to be primary cytokinin response genes. The induction of OsRR6 in response to different environmental stimuli indicates its role in cross-talk between abiotic stress and cytokinin signaling. These results provide a foundation for further investigations on specific as well as overlapping cellular functions of type-A response regulators in rice.
Cytokinins regulate various plant growth and developmental processes, including cell division, apical dominance, chloroplast biogenesis, leaf senescence, vascular differentiation, photomorphogenic development, shoot differentiation in tissue cultures and anthocyanin production, primarily by altering the expression of diverse genes [1, 2]. The recent genetic and molecular studies in plants have suggested the involvement of two-component sensor-regulator system in cytokinin signal perception and transduction, comprising sensor histidine kinase (HK) proteins, histidine phosphotransfer (HPt) proteins, and effector response regulator (RR) proteins [3–9]. Such signal transduction systems, once thought to be restricted to prokaryotes, have also been found in many eukaryotes, including yeast, fungi, slime molds and higher plants . In Arabidopsis, proteins with homology to all the elements of two-component system have been identified .
The analysis of Arabidopsis genome revealed the existence of 32 putative response regulator genes . Based on the predicted protein domain architecture and amino acid composition, the response regulators have been broadly categorized into three distinct families: type-A, type-B and pseudo-response regulators. The type-A response regulators are relatively small, containing a receiver domain along with small N- and C-terminal extensions . The type-B response regulators comprise a receiver domain fused to the DNA-binding domain and are supposed to be transcriptional regulators [12–14]. The pseudo-response regulators share significant sequence similarity with the receiver domain of other response regulators but the invariant D-D-K motif is not present . The pseudo-response regulators are also considered to be the elements of the circadian clock in Arabidopsis and rice [15–18].
The type-A response regulator genes in Arabidopsis (type-A ARRs) are rapidly and specifically induced by exogenous cytokinin, although with varying kinetics, and have been characterized as primary cytokinin response genes [11, 19, 20]. The transcription of type-A ARR genes is regulated in part by type-B ARRs [21, 22]. Some of the type-A ARRs perform partially redundant functions, acting as negative regulators of cytokinin responses by a feedback mechanism [21, 23, 24]. In contrast, ARR4 was claimed to be a positive regulator of cytokinin signaling because its over-expression enhanced the cytokinin responsiveness of transgenic Arabidopsis plants . However, the loss-of-function mutant did not reveal a positive role for ARR4 in cytokinin signaling  and this discrepancy remains to be resolved. The tissue distribution of ARR4 overlaps to a large extent with that of phytochrome B (phyB) and it has been found to interact with N-terminus of phyB to stabilize its active form . The transgenic Arabidopsis plants overexpressing ARR4 are specifically hypersensitive to red light , indicating that ARR4 may be involved in integrating red light and cytokinin signaling.
The type-A response regulators have been isolated and characterized from maize [27, 28]. However, there is no report on the characterization of any type-A response regulator from other monocot species, although several EST/cDNA sequences are available in the databases. Here, we report the identification and analysis of type-A response regulator gene family in rice (Oryza sativa), the model monocot plant. The exon-intron organization, chromosomal distribution and sequence homology have been analyzed for all ten members. The OsRR genes express differentially in various organs examined, and also in response to light. The application of exogenous cytokinin induced OsRR genes in the absence of de novo protein synthesis. Evidence has also been provided for a probable role of OsRR6 in abiotic stress signaling.
Results and discussion
Identification of type-A response regulators in rice
Type-A response regulators in rice.
ORF Length (bp)c
Polypeptide length (aa)d
No. of intronse
Exon-intron organization and chromosomal distribution
The BAC (bacterial artificial chromosome) or PAC (phage artificial chromosome) clones carrying the genes for OsRR proteins were identified (Table 1). The chromosome map positions of BAC/PACs given in centiMorgans (cM) from top of the chromosome, and the nearest marker to each OsRR gene are indicated in Table 1. The ten OsRR genes were found to be distributed on 7 of the 12 rice chromosomes (Table 1). Three OsRR genes are present on chromosome 4, two on chromosome 2, and one each on chromosome 1, 7, 8, 11, and 12. The distribution of OsRR genes on rice chromosomes did not reveal evident clusters. However, OsRR9 and OsRR10 are present on the duplicated block between chromosome 11 and 12 [32, 33].
Percentage identities among the rice type-A response regulators.
Organ-specific expression of OsRRgenes
OsRRsrepresent primary cytokinin response genes
The expression of OsRR genes in response to other plant hormones, including auxin, brassinosteroid, gibberellin and ethylene, was also examined. However, no significant effect of these hormones could be detected on the steady-state transcript levels of OsRR genes (Fig. 5), indicating their role primarily in cytokinin signaling.
Expression of OsRRgenes under stress conditions
What are the probable functions of OsRR proteins?
The type-A RRs in Arabidopsis have been shown to act as the negative regulators of cytokinin signaling with partially redundant functions [11, 24]. In addition, some of these ARRs and other elements of the two-component sensor-regulator phosphorelay participate in cross-talk between cytokinin and light signaling (mediated by phytochromes) and also with the gaseous hormone ethylene [4, 45]. The role of one of the type-A RRs, i.e. ARR4, has also been ascribed in red light mediated photomorphogenesis [24, 26]. In fact, ARR4 physically associates with phytochrome B to prolong the stability of its active conformation, Pfr, and accentuates red light signaling. The role of type-B ARRs (and possibly of type-A ARRs) has also been envisaged in a cross-talk between ethylene and cytokinin signaling, although they may regulate these components differentially to control diverse plant processes . To have an inkling about the functions of OsRR genes, the rice Tos17 insertion mutant database  providing the phenotype of rice Tos17 retrotransposon insertion mutants  was accessed using the BLAST program. We could identify insertion mutants corresponding only to OsRR9/10 gene (NE6006_0_401_1A and ND8005_0_402_1A); it was difficult to demarcate whether the sequence flanking the Tos17 insertion represents OsRR9 or OsRR10 because of more than 99% similarity between them. Despite the fact that OsRR9 and OsRR10 genes are so similar and may function redundantly, the phenotype of the insertion mutants (representing only one of these two loci) showed dwarfism, sterility, lesion mimic and vivipary. It can thus be speculated that OsRR9/10 genes may quantitatively affect different cellular processes influenced by both light and cytokinin. A detailed analysis of the insertional mutants already available and RNAi strategy for the remaining OsRR genes will greatly help in elucidation of the precise role of these genes.
The results of structural analyses of rice type-A RR proteins and their phylogenetic relationship with ARRs will be helpful for their functional validation in rice. The organ-specific differential expression profile of OsRR genes suggests that their products most likely perform diverse and overlapping functions in different cell types of rice. This study also reflects the role of OsRR genes in both light and cytokinin signaling. The induction of OsRR6 by different abiotic stress stimuli provides a molecular link between stress and cytokinin signaling as well. These results provide a foundation for future work on the elucidation of cellular functions of type-A response regulators in rice.
The type-A response regulator genes in rice were identified by performing BLAST searches at the National Centre for Biotechnology Information  and TIGR genomic and annotated database  resources of rice using the response regulator protein sequences of Arabidopsis thaliana as query. The number and positions of exons and introns for individual OsRR genes were determined by comparison of the cDNAs with their corresponding genomic DNA sequences. The position of each gene on rice chromosomes was found by BLASTN search in genomic sequences of rice chromosome pseudomolecules available at TIGR (Release 3). Multiple sequence alignments were done using the ClustalX (version 1.83) program  and the phylogenetic analysis carried out by neighbor-joining method . The unrooted phylogenetic tree was displayed using the Treeview program. The DNA and protein sequence analyses were performed using Gene Runner program version 3.04. Pairwise comparisons were done with the DNASTAR MegAlign 4.03 package to determine the sequence identities.
Plant material and growth conditions
Rice (Oryza sativa L. ssp. indica var. Pusa Basmati 1) seeds were disinfected with 0.1% HgCl2 solution for 1 h and thoroughly washed with RO (reverse-osmosis) water before soaking overnight in RO water. Seedlings were grown on cotton saturated with RO water, at 28 ± 1°C, either in complete darkness or in a culture room with a daily photoperiodic cycle of 14 h light and 10 h dark. Flowers and mature leaves were collected from rice plants grown in the greenhouse.
Hormone and stress treatments
For cytokinin treatment, 6-day-old light-grown rice seedlings were transferred to a solution of 50 μM benzyl aminopurine (BAP) and harvested at the indicated times. For treatment with other hormones/compounds, 6-day-old light-grown rice seedlings were transferred to beakers containing solutions of indole-3-acetic acid (IAA, 50 μM), epibrassinolide (Ebr, 10 μM), gibberellic acid (GA3, 50 μM), 1-aminocyclopropane-1-carboxylic acid (ACC, 50 μM), abscisic acid (ABA, 50 μM) and cycloheximide (CHX, 50 μM) and incubated for for 3 h. The mock-treated seedlings for the respective time intervals served as the control.
For salt and drought stress treatments, 6-day-old light-grown rice seedlings were transferred to 250 mM NaCl or 300 mM mannitol for 6 h. For low temperature treatment, the seedlings were kept at 8 ± 1°C for 6 h. The seedlings kept in water for the same duration, and at 28 ± 1°C, served as control.
Total RNA was extracted using the RNeasy Plant mini kit (Qiagen, Germany). To remove any genomic DNA contamination, the RNA samples were treated with RNase-free DNase I (Qiagen) according to the manufacturer's instructions. For each RNA sample, absorption at 260 nm was measured and RNA concentration calculated as A260 × 40 (μg/mL) × dilution factor. The integrity of RNA samples was monitored by agarose gel elecrophoresis.
cDNA isolation, cloning and sequencing
The coding region of OsRR genes were amplified by RT-PCR, using gene-specific primers, from total RNA isolated from light-grown seedlings using Titan One Tube RT-PCR kit (Roche, USA) according to the manufacturer's instructions. After 30 or 35 cycles, the PCR products were examined by gel electrophoresis and EtBr staining. RT-PCR products were cloned into pGEM-T Easy vector (Promega, Madison, WI) as per manufacturer's instructions. Sequencing was carried out using ABI Prism 377 Sequencer (PE Applied Biosystems, USA), with the Thermosequenase Dye Terminator Cycle Sequencing Kit (Amersham, UK).
Quantitative real-time PCR expression analysis
Primer sequences used for real time PCR expression analysis.
MJ acknowledges the award of Senior Research Fellowship from the Council of Scientific and Industrial Research, New Delhi. We gratefully acknowledge the financial support of Department of Biotechnology, Government of India, and the University Grants Commission, New Delhi.
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