TY - JOUR
AU - Mizuno, Takeshi
AB - Abstract In higher plants, there are wide ranges of biological processes that are controlled through the circadian clock. In this connection, we have been characterizing a small family of proteins, designated as ARABIDOPSIS PSEUDO-RESPONSE REGULATORS (APRR1, APRR3, APRR5, APRR7, and APRR9), among which APRR1 is identical to TOC1 (TIMING OF CAB EXPRESSION1) that is believed to be a component of the central oscillator. Through previous genetic studies, several lines of evidence have already been provided to support the view that, not only APRR1/TOC1, but also other APRR1/TOC1 quintet members are important for a better understanding of the molecular links between circadian rhythm, control of flowering time, and also photomorphogenesis. However, the least characterized one was APRR3 in that no genetic study has been conducted to see if APRR3 also plays an important role in the circadian-associated biological events. Here we show that APRR3-overexpressing transgenic plants (APRR3-ox) exhibited: (i) a phenotype of longer period (and/or delayed phase) of rhythms of certain circadian-controlled genes under continuous white light, (ii) a phenotype of late flowering under long-day photoperiod conditions, (iii) a phenotype of hypo-sensitiveness to red light during early photomorphogenesis of de-etiolated seedlings, supporting the current idea as to the APRR1/TOC1 quintet described above. (Received November 20, 2003; Accepted February 26, 2004) In higher plants, there are wide ranges of biological processes that are controlled through the circadian clock (for a review, see McClung 2000). One of the well-characterized circadian-regulated events in plants is the photoperiodic control of flowering time (for a review, see Simpson and Dean 2002). Furthermore, some (if not all) circadian-associated genes have also been implicated in the photomorphogenesis, such as the elongation of hypocotyls during de-etiolation (for a review, see Quail 2002). Recent intensive studies on Arabidopsis thaliana have begun to shed light on the molecular mechanisms underlying these circadian-controlled biological events (for reviews, see Eriksson and Millar 2003, Yanovsky and Kay 2003, and references therein). In the model higher plant, the best candidates of clock components (or central oscillators) are CCA1 (CIRCADIAN CLOCK-ASSOCIATED1) and LHY (LATE ELONGATED HYPOCOTYL) (Green and Tobin 1999, Mizoguchi et al. 2002, Schaffer et al. 1998). TOC1 (TIMING OF CAB EXPRESSION1) is also believed to be another component of the central oscillator (Somers et al. 1998, Strayer et al. 2000, Alabadi et al. 2001). According to a current consistent model (Alabadi et al. 2001), the CCA1 and LHY Myb-related transcription factors act redundantly in a manner that they repress the transcription of TOC1 through directly binding to the promoter region of TOC1, and conversely, the transcription of CCA1 and LHY is activated by TOC1, directly or indirectly. Consequently, such mutual interactions between CCA1/LHY and TOC1 result in a formation of a transcriptional negative/positive feedback loop. In this connection, we have been characterizing a small family of proteins, designated as ARABIDOPSIS PSEUDO-RESPONSE REGULATORS (APRR1, APRR3, APRR5, APRR7, and APRR9), based on the fact that APRR1 is identical to TOC1 (Ito et al. 2003, Makino et al. 2000, Makino et al. 2001, Makino et al. 2002, Matsushika et al. 2000, Matsushika et al. 2002a, Matsushika et al. 2002b, Murakami-Kojima et al. 2002, Murakami et al. 2003, Nakamichi et al. 2003, Nakamichi et al. 2004, Sato et al. 2002, Yamamoto et al. 2003, Yamashino et al. 2003). Several lines of evidence have already been provided to support the view that, not only APRR1/TOC1, but also other APRR1/TOC1 quintet members are crucial for a better understanding of the molecular links between circadian rhythm, control of flowering time, and photomorphogenesis. This view was further supported by the recent studies of several other laboratories (Eriksson et al. 2003, Kaczorowski and Quail 2003, Michael et al. 2003). Amongst the APRR1/TOC1 family members, nonetheless, the least characterized one was APRR3 in that no genetic study has been conducted to see if APRR3 also plays an important role in the circadian-associated events. Here we address this issue by characterizing transgenic lines aberrantly overexpressing the transcript of APRR3, with special reference to circadian rhythm, flowering time, and photomorphogenesis. First of all, we attempted to search for mutant lines that presumably carry a T-DNA insertion in the APRR3 gene. We obtained and characterized such putative mutants from The Kazusa DNA Research Institute (Chiba, Japan) and The Salk Institute Genomic Analysis Laboratory (California, U.S.A.), respectively. However, the former (labeled KG26826) contained a T-DNA insertion at the position downstream (114-bp) of the termination codon of APRR3, whereas the latter (labeled SALK_090261) contained a T-DNA insertion at the 3′-proximal end of the APRR3-coding sequence that results in a subtle truncation of C-terminal 11 amino acid residues. Therefore, they are not suitable for further characterization. We thus decided to construct transgenic lines that aberrantly express the transcript of APRR3 in a manner independent of circadian rhythm, by employing the entire APRR3 genomic DNA connected downstream to the cauliflower mosaic virus (CaMV) 35S promoter. Three independent transgenic lines, homozygous with regard to the 35S-promoter::APRR3 transgene, were established (named APRR3-ox, L1, L2, and L3). For these, it was confirmed that APRR3-ox plants expressed a high level of APRR3 in a manner independent of circadian rhythm (Fig. 1, for L1), while the APRR3 transcript showed a robust free-running rhythm in wild-type plants (Columbia, Col) under continuous white light. Others (L2 and L3) also showed essentially the same nature (data not shown), and these APRR3-ox transgenic plants were characterized simultaneously in the following examinations. To gain a first insight into the properties of APRR3-ox plants in terms of circadian rhythms, a hallmarked rhythmic expression of CCA1 was examined, after they had been grown under continuous light (LL) (Fig. 2A). The rhythmic profile of CCA1 in APRR3-ox was considerably different from that seen in wild-type plants. In particular, APRR3-ox showed a phenotype of longer period (and/or delayed phase) with regard to the CCA1 rhythm in LL. This phenomenon of APRR3-ox was further evidenced for another circadian-controlled gene, PIL6, (PHYTOCHROME INTERACTING FACTOR-LIKE6) (Fig. 2B). We previously showed that APRR1/TOC1 physically interacts with PIL6 (Yamashino et al. 2003), which is a member of the large family of basic helix-loop-helix (bHLH) transcription factors (the unified nomenclature of PIL6 is BHLH065, Bailey et al. 2003). Some other circadian-controlled genes (e.g., APRR1/TOC1, APRR7, and CAB2) were also characterized, and the results of these were also consistent with those described above (data not shown). However, it should be noted that, even when we analyzed the results from several independent experiments by using the FFT-NLLS method (Fast Fourier Transform-Nonlinear Least Squares) (Strume et al. 1991), our experimental procedures (i.e., Northern hybridization with RNA samples prepared at 3 h intervals) did not allow us to distinguish small period changes from small phase changes. In any case, the circadian-associated phenotype observed for APRR3-ox was less striking as compared with those observed previously for other APRR-overexpressing transgenic plants, such as APRR1-ox that showed an arrhythmicity in LL (Mas et al. 2003, Matsushika et al. 2002a). Another critical issue as to APRR3-ox plants is whether or not they show any phenotype with regard to the photoperiod-dependent control of flowering time. For example, we previously demonstrated that APRR5-ox plants show a characteristic phenotype of early flowering under both the long-day and short-day photoperiod conditions (Sato et al. 2002). Employing such APRR5-ox plants as appropriate references, APRR3-ox plants were grown under both the long-day (16 h light/8 h dark) and short-day (8 h light/16 h dark) conditions. APRR5-ox plants flowered earlier under the long-day conditions, as compared with wild-type plants, as scored by the number of rosette leaves (Fig. 3A), and the date of bolting (Fig. 3B). In contrast, APRR3-ox showed a phenotype of late flowering (Fig. 3A, B). These events were also demonstrated by showing the pictures of representative plants of APRR3-ox (32-day-old in long-day) (Fig. 3C). Note also that inflorescences appeared more or less at the same timing in both wild-type and APRR3-ox plants under the short-day conditions (Fig. 3D). These observations suggested that APRR3-ox plants showed a characteristic phenotype of late flowering under the long-day photoperiod conditions. It is well known that some circadian-associated genes are implicated not only in the control of flowering time, but also the photomorphogenesis (for a review, see Quail 2002). A well-established and visible hallmark of such photosensory signal transduction is the de-etiolation of seedlings under light with a certain spectrum (e.g., continuous red light) (Quail 2002). In this respect, we previously demonstrated that both APRR1-ox and APRR5-ox plants showed the similar phenotype (Fig. 4, upper panels), in that they are hyper-sensitive to red light in early photomorphogenesis, thereby giving rise to shorter hypocotyls when they were germinated under red light (1.0 µmol m–2 s–1), as compared with wild-type seedlings. Here we found that APRR3-ox seedlings displayed markedly longer hypocotyls than wild-type seedlings, suggesting that APRR3-ox seedlings are hypo-sensitive (or less sensitive) to red light with regard to the early photomorphogenesis under red light. These events were confirmed by examining fluence-rate response curves as to the length of hypocotyls (Fig. 4, lower panel). We also examined such photomorphogenesis of APRR3-ox under far-red light (from 0.2 to 1.0 µmol m–2 s–1) and blue light (from 0.001 to 8.6 µmol m–2 s–1). APRR3-ox seedlings were slightly less sensitive to far-red light, while no difference was observed in blue light (data not shown). It was thus revealed that APRR3-ox plants were hypo-sensitive to red light, as far as the early photomorphogenesis of young seedlings were concerned, regardless of whether it is specific to red light or not. In summary, in this study we conducted for the first time a genetic study, in order to see if APRR3 is also implicated in the circadian-associated events. We showed that APRR3-overexpressing transgenic plants (APRR3-ox) exhibited: (i) a phenotype of longer period (and/or delayed phase) of rhythms of certain circadian controlled genes under continuous white light (Fig. 2), (ii) a phenotype of late flowering under long-day photoperiod conditions (Fig. 3), and (iii) a phenotype of hypo-sensitiveness to red light during early photomorphogenesis of de-etiolated seedlings (Fig. 4). By incorporating these new results into a whole, we compiled all the available genetic data as to the APRR1/TOC1 quintet with special reference to the circadian-associated phenotypes, which have been rapidly accumulated within these few years (Table 1, and references therein). Although these genetic data are apparently quite complex, several implications could be pointed out, as follows. APRR1/TOC1 appears to be deeply implicated in the circadian rhythm and photosignal transduction, but its implication in the control of flowering time is less evident (Alabadi et al. 2001, Sato et al. 2002, Mas et al. 2003). APRR5 appears to be implicated in these circadian-associated events in each similar extent (Sato et al. 2002, Eriksson et al. 2003, Yamamoto et al. 2003). Certain aprr7 mutants show a clear phenotype with regard to the red light sensitiveness in the elongation of hypocotyls, but its phenotype of flowering time is less striking (Kaczorowski and Quail 2003, Yamamoto et al. 2003). Curiously, APRR9 is less relevant to the photomorphogenesis, albeit with the fact that the expression of APRR9 is induced by light in an acute and phytochrome-dependent manner (Eriksson et al. 2003, Ito et al. 2003). The results of this study further provided us with the intriguing idea that APRR3 also appears to be crucially implicated in a red light-mediated (or phytochrome-dependent) photosignal transduction pathway, in which APRR3 appears to serve as a negative regulator (Table 1). Interestingly, all others (APRR1/TOC1, APRR5, APRR7, and APRR9) are suggested to act in a positive manner in this signaling pathway. It is also apparent that APRR3 is implicated both in circadian rhythm and control of flowering time. These observations suggest that APRR3 plays a complementary role with other APRR1/TOC1 quintet members. In any event, it is clear that each single loss-of-function mutant of the APRR1/TOC1 family genes shows each characteristic phenotype with regard to the circadian-associated events. At least, these results are compatible with the generalized view that the functions of the APRR1/TOC1 family members are complimentary with each other, but not solely redundant. The genetic results of aberrant expression of each APRR1/TOC1 family gene also consistently supported this view (Table 1, and references therein). Nevertheless, it is premature to envisage a molecular basis of the genetic and/or functional interactions among the APRR1/TOC1 quintet members and also other clock-associated components including CCA1 and LHY. To this end, intensive epistatic analyses should be carried out. Acknowledgments This study was supported by Grants-in-Aid from the Ministry of Education, Science, Sports, and Culture of Japan, and also the Ministry of Agriculture, Forestry and Fisheries of Japan. For some Arabidopsis mutant seeds, we deeply thank The Salk Institute Genomic Analysis Laboratory (California, U.S.A.) and The Arabidopsis Biological Resource Center (Columbus, U.S.A.), as well as The Kazusa DNA Research Institute (Chiba, Japan). 1 Corresponding author: E-mail: tmizuno@agr.nagoya-u.ac.jp; Fax: +81-52-789-4091. View largeDownload slide Fig. 1 Isolation of APRR3-ox transgenic plants. Together with wild-type plants (Columbia, Col), APRR3-ox plants (with T3 homozygous seeds) were grown on MS agar-plates (12 h light/12 h dark) for 21 d, and then they were released into continuous white light (LL). RNA samples were prepared from leaves at the times indicated with appropriate intervals (3 h). Northern hybridization was carried out with a probe specific for the APRR3 coding sequence (Matsushika et al. 2000). The hybridized bands were detected with a phosphoimage analyzer (BAS-2500, FujiXerox, Japan) (lower panel), and also the intensities of bands were quantified (upper panel). In these experiments, the transcript of UBQ10 was also detected as an internal reference (data not shown). The measured intensities of each band were normalized (by dividing with the UBQ10 value). Based on these values, the relative amounts of mRNA (or transcript) were calculated and expressed as arbitrarily units, in which the maximum level of the transcript of APRR3 detected for wild-type (WT) plants was taken as 10 arbitrarily in order to clarify the profiles. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and other independent transgenic lines (L2 and L3) showed essentially the same aberrant expression profiles. View largeDownload slide Fig. 1 Isolation of APRR3-ox transgenic plants. Together with wild-type plants (Columbia, Col), APRR3-ox plants (with T3 homozygous seeds) were grown on MS agar-plates (12 h light/12 h dark) for 21 d, and then they were released into continuous white light (LL). RNA samples were prepared from leaves at the times indicated with appropriate intervals (3 h). Northern hybridization was carried out with a probe specific for the APRR3 coding sequence (Matsushika et al. 2000). The hybridized bands were detected with a phosphoimage analyzer (BAS-2500, FujiXerox, Japan) (lower panel), and also the intensities of bands were quantified (upper panel). In these experiments, the transcript of UBQ10 was also detected as an internal reference (data not shown). The measured intensities of each band were normalized (by dividing with the UBQ10 value). Based on these values, the relative amounts of mRNA (or transcript) were calculated and expressed as arbitrarily units, in which the maximum level of the transcript of APRR3 detected for wild-type (WT) plants was taken as 10 arbitrarily in order to clarify the profiles. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and other independent transgenic lines (L2 and L3) showed essentially the same aberrant expression profiles. View largeDownload slide Fig. 2 Free-running rhythms characterized by Northern blot hybridization analyses for certain circadian-controlled genes in APRR3-ox plants under continuous white light. Both wild-type (WT, Col) and APRR3-ox plants were grown under the conditions of 12 h light/12 h dark for 21 d, and then they were released into continuous white light (LL). RNA samples were prepared from leaves at the times indicated with appropriate intervals (3 h). (A) They were analyzed with a probe specific for the CCA1 coding sequence (Matsushika et al. 2002a). (B) Similarly, Northern hybridization was carried out with a probe specific for the PIL6 coding sequence (Yamashino et al. 2003). In these experiments, the transcript of UBQ10 was also detected as an internal reference (lower panels). The hybridized bands were detected with a phosphoimage analyzer (BAS-2500, FujiXerox, Japan), and also the intensities of each band were quantified (each upper panel). Other details are the same as those given in the legend to Fig. 1. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. View largeDownload slide Fig. 2 Free-running rhythms characterized by Northern blot hybridization analyses for certain circadian-controlled genes in APRR3-ox plants under continuous white light. Both wild-type (WT, Col) and APRR3-ox plants were grown under the conditions of 12 h light/12 h dark for 21 d, and then they were released into continuous white light (LL). RNA samples were prepared from leaves at the times indicated with appropriate intervals (3 h). (A) They were analyzed with a probe specific for the CCA1 coding sequence (Matsushika et al. 2002a). (B) Similarly, Northern hybridization was carried out with a probe specific for the PIL6 coding sequence (Yamashino et al. 2003). In these experiments, the transcript of UBQ10 was also detected as an internal reference (lower panels). The hybridized bands were detected with a phosphoimage analyzer (BAS-2500, FujiXerox, Japan), and also the intensities of each band were quantified (each upper panel). Other details are the same as those given in the legend to Fig. 1. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. View largeDownload slide Fig. 3 Phenotype of APRR3-ox with reference to the flowering time. The plants (wild-type (WT), APRR3-ox, and APRR5-ox) were grown as follows. APRR5-ox plants were constructed previously (Sato et al. 2002). Seeds were imbibed directly on soil (110 ml), supplemented with 50 ml of 5,000-times diluted HYPONEX (N : P : K = 5 : 10 : 5) (HYPONEX-JAPAN, Osaka, Japan). They were cold-treated at 4°C for 3 d in the dark. They were then transferred for germination under light (80–100 µmol m–2 s–1), and they were grown in chambers (22°C) under the photoperiod conditions of long-day (16 h light/8 dark) and short-day (8 h light/ 16 h dark). (A) For number of leaves at flowering, the leaf count was taken on the day the flower primordia were first observed on a given plant. (B and D) Days to visible inflorescence (about 1 cm) was defined as the time at which a given plant possessed the flower primordia. The numbers of plants examined were: wild-type (n = 8 for long-day. n = 6 for short-day), APRR3-ox (n = 23 for long-day, n = 8 for short-day), APRR5-ox (n = 7 for long-day). (C) Among these plants examined, the pictures of such representatives grown for 32 d in the long-day photoperiod were taken, as indicated. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. Other independent transgenic lines (L2 and L3) showed essentially the same phenotypic properties. View largeDownload slide Fig. 3 Phenotype of APRR3-ox with reference to the flowering time. The plants (wild-type (WT), APRR3-ox, and APRR5-ox) were grown as follows. APRR5-ox plants were constructed previously (Sato et al. 2002). Seeds were imbibed directly on soil (110 ml), supplemented with 50 ml of 5,000-times diluted HYPONEX (N : P : K = 5 : 10 : 5) (HYPONEX-JAPAN, Osaka, Japan). They were cold-treated at 4°C for 3 d in the dark. They were then transferred for germination under light (80–100 µmol m–2 s–1), and they were grown in chambers (22°C) under the photoperiod conditions of long-day (16 h light/8 dark) and short-day (8 h light/ 16 h dark). (A) For number of leaves at flowering, the leaf count was taken on the day the flower primordia were first observed on a given plant. (B and D) Days to visible inflorescence (about 1 cm) was defined as the time at which a given plant possessed the flower primordia. The numbers of plants examined were: wild-type (n = 8 for long-day. n = 6 for short-day), APRR3-ox (n = 23 for long-day, n = 8 for short-day), APRR5-ox (n = 7 for long-day). (C) Among these plants examined, the pictures of such representatives grown for 32 d in the long-day photoperiod were taken, as indicated. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. Other independent transgenic lines (L2 and L3) showed essentially the same phenotypic properties. View largeDownload slide Fig. 4 Red light response of APRR3-ox plants in the early photomorphogenesis during de-etiolation. (Upper panel) Photographs were taken for the seedlings that were grown under continuous red light with a given fluence rates (1.0 µmol m–2 s–1) and in the dark. Characterized plants were: APRR1-ox (1ox), APRR5-ox (5ox), wild-type (WT, Col), and APRR3-ox (3ox), as indicated. APRR1-ox and APRR5-ox plants were constructed previously (Makino et al. 2002, Sato et al. 2002). Seeds were sowed on agarose (0.8%)-plates containing MS salts without sucrose, and they were then kept at 4°C for 48 h in the dark. After seeds were exposed to white light for 3 h in order to enhance germination, and then they were kept at 22°C for 21 h again in the dark. Seedlings were grown for 72 h. (Lower panel) Fluence-rate response curves were examined. The experiments were carried out as described above; however, in these experiments seedlings were grown for 72 h under continuous red light with a varied range of fluence rates or in the dark, as indicated. The data are means with standard deviations from 15 seedlings of each transgenic line grown under each fluence-rate. For the lower panel, it should be noted that the symbols of APRR1-ox are completely obscured by those of APRR5-ox. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. Other independent transgenic lines (L2 and L3) showed essentially the same phenotypic properties. View largeDownload slide Fig. 4 Red light response of APRR3-ox plants in the early photomorphogenesis during de-etiolation. (Upper panel) Photographs were taken for the seedlings that were grown under continuous red light with a given fluence rates (1.0 µmol m–2 s–1) and in the dark. Characterized plants were: APRR1-ox (1ox), APRR5-ox (5ox), wild-type (WT, Col), and APRR3-ox (3ox), as indicated. APRR1-ox and APRR5-ox plants were constructed previously (Makino et al. 2002, Sato et al. 2002). Seeds were sowed on agarose (0.8%)-plates containing MS salts without sucrose, and they were then kept at 4°C for 48 h in the dark. After seeds were exposed to white light for 3 h in order to enhance germination, and then they were kept at 22°C for 21 h again in the dark. Seedlings were grown for 72 h. (Lower panel) Fluence-rate response curves were examined. The experiments were carried out as described above; however, in these experiments seedlings were grown for 72 h under continuous red light with a varied range of fluence rates or in the dark, as indicated. The data are means with standard deviations from 15 seedlings of each transgenic line grown under each fluence-rate. For the lower panel, it should be noted that the symbols of APRR1-ox are completely obscured by those of APRR5-ox. For these experiments, a certain APRR3-ox transgenic line (L1) was employed, and the presented data are representatives of several independent experimentations. Other independent transgenic lines (L2 and L3) showed essentially the same phenotypic properties. Table 1 A summarized view as to the results of genetic studies on the APRR1/TOC1 quintet members   Free-running rhythms under continuous white light  Flowering time under long-day photoperiod  Hypocotyl length in red light  References  Mutants a          aprr9  long period (or phase delay) c  no apparent change  long (slightly)  Eriksson et al. (2003), Ito et al. (2003), Michael et al. (2003)  aprr7  long period (or phase advance) b  late  long  Kaczorowski and Quail (2003), Michael et al. (2003), Yamamoto et al. (2003)  aprr5  short period c  late  long  Eriksson et al. (2003), Michael et al. (2003), Yamamoto et al. (2003)  aprr3a  short period  ND  ND  Michael et al. (2003)  toc1-2  short period c  ND d  long  Alabadi et al. (2001), Mas et al. (2003)  Aberrant expression          APRR9-ox  short period  early  short (slightly)  Matsushika et al. (2002b), Sato et al. (2002)  APRR7-ox  ND  ND  ND    APRR5-ox  lowered amplitude  early  short  Sato et al. (2002)  APRR3-ox  slightly long period (or phase delay)  late  long  This study  TOC1/APRR1-ox  arrhythmic (or long period) e  no apparent change  short  Mas et al. (2003), Matsushika et al. (2002a)Sato et al. (2002)    Free-running rhythms under continuous white light  Flowering time under long-day photoperiod  Hypocotyl length in red light  References  Mutants a          aprr9  long period (or phase delay) c  no apparent change  long (slightly)  Eriksson et al. (2003), Ito et al. (2003), Michael et al. (2003)  aprr7  long period (or phase advance) b  late  long  Kaczorowski and Quail (2003), Michael et al. (2003), Yamamoto et al. (2003)  aprr5  short period c  late  long  Eriksson et al. (2003), Michael et al. (2003), Yamamoto et al. (2003)  aprr3a  short period  ND  ND  Michael et al. (2003)  toc1-2  short period c  ND d  long  Alabadi et al. (2001), Mas et al. (2003)  Aberrant expression          APRR9-ox  short period  early  short (slightly)  Matsushika et al. (2002b), Sato et al. (2002)  APRR7-ox  ND  ND  ND    APRR5-ox  lowered amplitude  early  short  Sato et al. (2002)  APRR3-ox  slightly long period (or phase delay)  late  long  This study  TOC1/APRR1-ox  arrhythmic (or long period) e  no apparent change  short  Mas et al. (2003), Matsushika et al. (2002a)Sato et al. (2002)  a These are most likely loss-of-function mutants of the Columbia ecotype, except for the aprr3 mutant. This particular mutant (aprr3-1) has a T-DNA insertion at the very C-terminal end of the APRR3 coding sequence (Michael et al. 2003), as mentioned in the text. Note also that the prr7-1 mutant characterized by Kaczorowski and Quail (2003) is a derivative of the RLD ecotype. b There is seemingly a conflict in that two groups reported that a aprr7 mutant showed a phenotype of long period (Michael et al. 2003, Yamamoto et al. 2003), whereas another showed that the other aprr7 mutant showed a phenotype of phase advance (Kaczorowski and Quail 2003). This might be due to the difference of ecotypes used (see a). c The effect of this toc1 mutation on rhythms appears to be dependent on the light conditions in that it showed a phenotype of arrhythmic under red light or constant darkness. The period effects of the aprr9 and aprr5 mutants also appear to be light-dependent (Eriksson et al. 2003). d The phenotype of toc1-2 with regard to the flowering time was not reported, thereby denoted as ND (not determined). The original toc1-1 mutant is semi-dominant, thus this is not listed in this table. However, note that this toc1-1 mutant shows a phenotype of early flowering in the background of Landsberg erecta (Yanovsky and Kay 2002). e The phenotypes appear to be dependent on the levels of overexpression (Mas et al. 2003, Matsushika et al. 2002a). View Large References Alabadi, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Mas, P. and Kay, S.A. ( 2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. 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TI - Characterization of Circadian-Associated APRR3 Pseudo-Response Regulator Belonging to the APRR1/TOC1 Quintet in Arabidopsis thaliana
JF - Plant and Cell Physiology
DO - 10.1093/pcp/pch065
DA - 2004-05-01
UR - https://www.deepdyve.com/lp/oxford-university-press/characterization-of-circadian-associated-aprr3-pseudo-response-vkdbhYyDTl
SP - 645
EP - 650
VL - 45
IS - 5
DP - DeepDyve
ER -