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First published online May 27, 2005; 10.1104/pp.104.059055 Plant Physiology 138:1106-1116 (2005) © 2005 American Society of Plant Biologists The Involvement of Gibberellin 20-Oxidase Genes in Phytochrome-Regulated Petiole Elongation of ArabidopsisNational Institute of Floricultural Science, Tsukuba 305–8519, Japan (T.H., M.K.); and Commonwealth Scientific and Industrial Research Organization, Plant Industry, Canberra 2601, Australian Capital Territory, Australia (T.H., R.W.K., C.A.H.)
Long day (LD) exposure of rosette plants causes rapid stem/petiole elongation, a more vertical growth habit, and flowering; all changes are suggestive of a role for the gibberellin (GA) plant growth regulators. For Arabidopsis (Arabidopsis thaliana) L. (Heynh), we show that enhancement of petiole elongation by a far-red (FR)-rich LD is mimicked by a brief (10 min) end-of-day (EOD) FR exposure in short day (SD). The EOD response shows red (R)/FR photoreversibility and is not affected in a phytochrome (PHY) A mutant so it is mediated by PHYB and related PHYs. FR photoconversion of PHYB to an inactive form activates a signaling pathway, leading to increased GA biosynthesis. Of 10 GA biosynthetic genes, expression of the 20-oxidase, AtGA20ox2, responded most to FR (up to a 40-fold increase within 3 h). AtGA20ox1 also responded but to a lesser extent. Stimulation of petiole elongation by EOD FR is reduced in a transgenic AtGA20ox2 hairpin gene silencing line. By contrast, it was only in SD that a T-DNA insertional mutant of AtGA20ox1 (ga5-3) showed reduced response. Circadian entrainment to a daytime pattern provides an explanation for the SD expression of AtGA20ox1. Conversely, the strong EOD/LD FR responses of AtGA20ox2 may reflect its independence of circadian regulation. While FR acting via PHYB increases expression of AtGA20ox2, other GA biosynthetic genes are known to respond to R rather than FR light and/or to other PHYs. Thus, there must be different signal transduction pathways, one at least showing a positive response to active PHYB and another showing a negative response.
The light environment of plants, particularly its quality and daily duration, regulates many aspects of plant development including seed germination, shoot elongation, shoot architecture, and flowering. Of the plant photoreceptors involved in such light responses, the phytochromes (PHYs), cryptochromes, and phototropins are most important (see Quail, 2002  ).
Typically, PHY acts by regulating the synthesis of the GA class of plant growth regulators. For example, a brief (5–10 min) exposure to PHY-active far-red (FR) light at the end-of-day (EOD) increases bioactive GA content in isolated, elongating epicotyls of cowpea (Vigna unguiculata; Martínez-García et al., 2000
In contrast to the FR stimulation of 20-oxidase expression in shoots, in germinating seed (Toyomasu et al., 1993
Genetic studies have provided clear evidence that the PHY family of photoreceptors are responsible for responses to brief R or FR exposures. In Arabidopsis, PHYB, D, E, and possibly PHYC, act redundantly in such regulation of shoot elongation, leaf growth, and flowering (Franklin et al., 2003
In our earlier studies with Arabidopsis, we showed that FR-rich light during an LD caused rapid increases (within 2 d) in both petiole elongation and their content of bioactive GAs (Gocal et al., 2001
Enhanced Expression of GA Biosynthetic Genes with FR Exposure Following exposure to a single low-irradiance FR-rich LD from incandescent lamps, Arabidopsis plants double their petiole elongation compared with plants kept in short day (SD; Fig. 1). Furthermore, since a 10-min EOD FR exposure in SD gave a comparable stimulation to that from a LD (Fig. 1), we can conclude that the enrichment for FR wavelengths in incandescent lamps accounts for their effectiveness. We return to this matter later but first examine the effect of LD/FR exposure on the expression of GA biosynthesis genes.
Using quantitative real time PCR (Q-PCR) and specific primers for 13 of the known GA biosynthetic genes, the effect of daylength on their mRNA expression level was examined in young elongating petioles of Arabidopsis (Fig. 2). We could detect little or no transcript of AtGA3ox2 and AtGA2ox1, while AtGA20ox3 was barely detectable and we could not detect expression of AtGA20ox4 or AtGA20ox5. The ACTIN standard was effectively detected in all samples, which excludes the possibility of failed assays. The lack of detection of AtGA3ox2 may reflect differences in tissue specificity as it has only been detected previously in germinating seeds (Yamaguchi et al., 2001 ).
The major effect of LD is to increase expression of AtGA20ox2 in elongating petioles, especially after the second LD exposure (Fig. 2). These findings fit with earlier evidence that GA 20-oxidases are important for the LD-regulated increases in GA biosynthesis that are required for increases in petiole and stem elongation (Gilmour et al., 1986 ; Xu et al., 1997; Lee and Zeevaart, 2002). However, it appears that not all 20-oxidases show such a large LD response. For AtGA20ox1, there was only a limited effect of LD on its expression (Fig. 2).
Despite the fact that the AtGA3ox genes are important for increased GA biosynthesis during R-light-regulated seed germination in Arabidopsis (Yamaguchi et al., 1998
Does Expression of GA Biosynthetic Genes Oscillate in a Circadian Manner?
Given the clear diurnal oscillations we observed in expression of at least one 20-oxidase gene and possibly some of the genes for early biosynthetic steps (Fig. 2), control by a circadian oscillator is likely. Therefore, some 7-week-old plants held in 8-h SD from high intensity light were transferred to continuous high intensity light (LL) and at the same constant temperature. Young petioles were harvested every 4 h and, as shown in Figure 3, in constant conditions, expression of AtGA20ox1 clearly oscillates with a circadian periodicity (approximately 24 h). The phase over the first 2 d was the same as for plants harvested at the same time but kept in SD (Figs. 2 and 3). There was little or no diurnal oscillation in expression of the second 20-oxidase, AtGA20ox2 (Figs. 2 and 3), and it did not show any circadian rhythmicity in constant conditions (Fig. 3). Rather, in SD, there was a noncircadian cycling in expression of AtGA20ox2 and this was reproduced in both the experiments shown (Figs. 2 and 3). Expression of some 20-oxidases is down-regulated by feedback by bioactive GA products (see Phillips et al., 1995
Based on our spectrophotometric measurements, input RNA amounts were equal and the constancy of the ACTIN assays supports this claim. For the three replicates of all 23 samples in Figure 3, the average ACTIN expression was 0.90 ± 0.06, after normalization across assays to the value of the first SD sample taken as 1.0. Thus, there is little variation in the loading control and the circadian oscillation must be in the expression of AtGA20ox1. Furthermore, the absence of any cycling in AtGA20ox2 expression in the same RNA samples supports this argument. Previously, Blazquez et al. (2002) To restate the above findings, AtGA20ox1 is entrained by the circadian clock and expresses more during the 8-h main SD-light period (Figs. 2 and 3). By contrast, expression of AtGA20ox2 is not entrained by the circadian clock, it expresses at low levels in darkness or during any R-rich fluorescent exposure (Figs. 2 and 3), and it expresses most during the FR-rich LD, increasing up to 7-fold, whereas expression of AtGA20ox1 barely doubled in LD (Fig. 2). To emphasize these differences between AtGA20ox1 and AtGA20ox2 in their response to daylength and light quality, a petiole sample was taken just before the start of the main 8-h-SD light period (predawn) when AtGA20ox2 expression should be elevated. A second sample was taken at the end of the main 8-h-light period (predusk) when AtGA20ox1 expression should be elevated. The results in Figure 4 confirm these expectations and, most importantly, show that only an FR-rich incandescent LD exposure activated AtGA20ox2 expression; a comparable low irradiance LD exposure (10 µmol m–2 s–1) from R-rich fluorescent lamps gave no LD increase. Furthermore, in the same experiment, the R-rich fluorescent light gave no enhancement of petiole elongation (Fig. 4). Thus, not only are these LD photoresponses linked closely to FR wavelengths and not to the R of fluorescent lamps, but these differences indicate that the blue wavebands of the fluorescent lamps may also be unimportant. Later, we return to the identity of photoreceptors. A further implication of these findings is that blocking AtGA20ox2 expression should impact on the LD enhancement of petiole elongation, while mutation of AtGA20ox1 should only impact on petiole growth in SD and we consider these predictions below.
Does Decreasing the Expression of GA Biosynthetic Genes Affect Petiole Elongation?
A Salk line (Alonso et al., 2003
We were unable to obtain a T-DNA insertional mutant of AtGA20ox2, although we examined two candidate lines available in the Salk Collection. Therefore, we used an RNA silencing approach and obtained 13 stably transformed second generation transgenic hairpin lines. As shown in Figure 5B, relative to wild type, AtGA20ox2 expression was reduced by 90% in line 3, to about 50% in line 2 and by about 10% in line 12 that was included as a transformed control. There was no effect of reduction in expression of AtGA20ox2 on expression of AtGA20ox1 (Fig. 5B). For these lines with their reduced 20-oxidase expression, petiole growth in SD or following an EOD FR exposure is shown in Figure 5, C and D. For ga5-3, its elongation in SD was reduced by approximately 25% compared to the wild type (Fig. 5C). However, ga5-3 showed a normal increase in response to an EOD FR exposure (Fig. 5D) and to an FR-rich LD (data not shown), this claim being based on first removing the SD effect that we have done here by calculating the LD increment over that of the same line in SD. With the AtGA20ox2 transgenic hairpin lines, the converse response was evident. They responded as well as the control in SD (Fig. 5C) but showed reduced FR (Fig. 5D) or LD response (data not shown). Importantly, the extent of gene silencing for the three AtGA20ox2 lines (Fig. 5B) matches the reduction in their petiole elongation on exposure to EOD FR (Fig. 5D). This finding further supports our claim that AtGA20ox2 expression induced by FR-light is important for the synthesis of GAs required for the LD stimulation of petiole elongation. No other "growth" phenotypes were obvious in these gene silencing lines.
In a further, preliminary study with GA20ox antisense lines provided to us by A. Phillips and P. Hedden (Biotechnology and Biological Science Research Council, Rothamsted, UK), we have found a similar daylength differential in the regulation of petiole elongation. The AtGA20ox1 antisense line showed a 22% reduction in its petiole elongation in SD and no reduction for the AtGA20ox2 antisense line (data not shown). Conversely, LD response was reduced somewhat in the AtGA20ox2 antisense line but there was no reduction in LD response for the AtGA20ox1 antisense line (data not shown). That petiole elongation is reduced in these antisense lines was noted by Coles et al. (1999) Overall, circadian changes regulate AtGA20ox1 so that it expresses most in the "daytime" of SD. By contrast, AtGA20ox2 lacks this circadian pattern of response and shows a FR-rich light, LD response over the "nighttime" hours of each daily cycle. Thus, there could be significant differences between these genes in their circadian regulation and in their response to different light treatments. We examine the photoregulation of these genes in more detail in the following section.
Of the various photoreceptors, we have examined only PHY action since petiole elongation and 20-oxidase expression increased in FR-rich LD or EOD FR conditions and not in R-rich conditions (Figs. 1 and 4). In an initial experiment, after exposure to a single 10-min EOD FR, AtGA20ox2 expression increased rapidly (within 3 h) and dramatically (up to 40-fold), and this increase was duplicated when the FR exposure was repeated the next day (Fig. 6). Importantly, the results in Table I show that the EOD FR promotion of AtGA20ox2 expression and of petiole elongation was fully reversed by a subsequent exposure to 10 min of R light. Both AtGA20ox genes showed increased expression after FR in the experiment shown in (Fig. 6), but AtGA20ox1 showed a weaker response and sometimes no change after FR whereas AtGA20ox2 always responded strongly (Fig. 6; Table I; a third experiment not shown here). In a further study, but with AtGA3ox1 that regulates a different GA biosynthetic step, there was no effect of R/FR on its expression in the petiole (Fig. 7), which confirms the evidence in Figure 2 for plants exposed to a FR-rich LD.
The R/FR photoreversibile control of gene expression as shown in Table I is diagnostic for PHY action (Borthwick et al., 1952 ) and, specifically, for the light stable PHY of the PHYB class (PHYB, C, D, and E; see Quail, 2002). To reinforce this claim, the wild type and a phyA mutant showed identical EOD FR effects on 20-oxidase expression and petiole elongation (Figs. 7 and 8). Thus, PHYA is not part of the response to either EOD FR or to FR-rich LD exposures. In a phyB null mutant, we expected the converse response, greater petiole elongation, and higher levels of gene expression in R light, particularly since hypocotyl elongation in young seedlings of this mutant is almost as great as for etiolated (dark) controls (Reed et al., 1993). The fact that light grown plants of the same mutant showed little or no increases in elongation or of gene expression when PHYB input was reduced in the mutant or when, in addition, the mutant was exposed to FR (Figs. 7 and 8), indicates that in adult plants, secondary, pleiotropic effects of the mutant make it unsuitable for testing for PHYB input. Nevertheless, our physiological demonstration of photoreversibility in the wild type stands as unequivocal evidence for the action of PHYB or of related PHYs.
The complex pattern of diurnal changes in expression of AtGA20ox1, particularly at the end of the SD (Figs. 2 and 6), could make it difficult to identify responses to FR exposure. Therefore, in further studies, the time of giving FR was either delayed by 3 h after the start of darkness or was given early when the main 8-h-SD light period was terminated after 4 h. The times to peak expression after such changes in the time of FR exposure were the same as before in Figures 6 and 7 (2 h in dark after FR for AtGA20ox1 and after 3 h for AtGA20ox2) and, again, the more substantial increases were for AtGA20ox2 (data not shown). Thus, the diurnal and circadian patterns of gene expression do not appear to influence the response to EOD FR.
Here, based both on gene expression analysis and on responses in a mutant or in gene silencing lines, we show that GA 20-oxidase biosynthetic genes are involved in the petiole elongation in Arabidopsis associated with exposure to EOD FR light or to LD from FR-rich incandescent lamps. The light input involves PHYB and related PHYs and not PHYA since responses were the same in the wild type and a phyA mutant. Furthermore, it is unlikely that there was an additional blue light action because petiole elongation and 20-oxidase expression could be accounted for as an R/FR response, an LD exposure from fluorescent tubes having the same effect as an R EOD treatment.
The rapid increase in elongation on exposure to FR fits with the scenario that increased expression of GA 20-oxidases caused increased GA synthesis and, in turn, greater elongation; gene expression increased within 3 h of a 10-min EOD FR exposure (Figs. 6 and 7) or within 4 h of the start of the first of two FR-rich LD exposures (Fig. 2). The first sign of increased petiole elongation is at 2 d (Fig. 1) by which time the GA1 and GA4 contents of the young petioles have increased up to 3-fold (Gocal et al., 2001
Expression profiling of elongation-related genes associated with exposure of Arabidopsis to FR-rich light (Devlin et al., 2003 A unique aspect of our study is the contrast apparent between two of the Arabidopsis 20-oxidase genes. AtGA20ox1 responds weakly to FR and is regulated by a circadian clock such that its maximum expression and physiological effectiveness is seen in SD. By contrast, AtGA20ox2, which shows no circadian control, is mostly expressed when exposed to FR-rich EOD or LD conditions (Figs. 2 and 3). These distinctions explain the daylength-specific effects of the mutant and silencing lines in that rhythmic gating of gene expression and a weak FR response confer the SD phenotype of ga5-3 (Fig. 5). Conversely, there is an LD phenotype in the AtGA20ox2 hairpin silencing lines (Fig. 5) because of the greater FR response of AtGA2ox2 coupled with its lack of rhythmic gating. The daylength-specific effects of these two 20-oxidases genes also have implications for studies of flowering of Arabidopsis. For example, in an FR-rich LD, AtGA20ox2 should regulate a GA-dependent pathway and we will present such an analysis of flowering responses in a future publication.
A model summarizing the interrelationships between LD or EOD FR light, GA metabolism, and elongation is presented in Figure 9. In relation to light regulation of GA biosynthesis, it is known that, in R light, PHY Pfr activates seed germination in association with increased expression of the 3-oxidase GA metabolism genes of Arabidopsis (Yamaguchi et al., 1998
The 20-oxidase, AtGA20ox2, is central to the LD/FR regulated PHY response associated with elongation, a claim also supported by our evidence of little or no change for the nine other GA metabolism genes studied here and including two 2-oxidases that regulate GA catabolism. As discussed above, the interaction between LD and circadian regulation of 20-oxidases can be significant but has received too little attention previously. The more significant LD-regulated changes occur rapidly, overnight (Fig. 2), and apparently independently of circadian regulation (Fig. 3). However, in earlier studies of Lee and Zeevaart (2002) , 20-oxidase expression in LD was examined only at dawn and dusk, while the analysis of 20-oxidase rhythms by Carrera et al. (1999), although involving frequent sampling, did not focus on changes occurring during the switch between daylengths.
The complex ways PHY regulates different GA biosynthetic genes, different signal transduction pathways, and different physiological responses is further heightened by studies of deetiolation. In pea, R light acting via Pfr inhibits growth of etiolated plants and blocks GA synthesis (Reid et al., 2002
An explanation for the clear evidence of R/FR photoreversible control of petiole elongation but the complete loss of response in the phyB mutant (Figs. 7 and 8) is not obvious. Were GA content to increase, as it appears to do in a sorghum phyB mutant (Lee et al., 1998
In conclusion, for Arabidopsis, we have shown that FR-rich LD or EOD FR conditions stimulate petiole elongation by regulating expression of GA20-oxidase biosynthetic genes, as was also implied in earlier studies of elongation of petioles or stems (for review, see García-Martínez and Gil, 2002
Plant Material, Growing Conditions, and Light Treatments
Plants of Arabidopsis (Arabidopsis thaliana) L. Heynh. ecotype Columbia and various mutant and transgenic lines of Columbia were grown for 5 to 7 weeks in 8-h SD at an irradiance of 100 µmol photons m–2 s–1 at 22°C. There was no flowering for plants held for up to 10 weeks in these SD conditions in light from red/blue-rich fluorescent tubes; however, flowering occurred within 3 weeks on transfer of 5-week-old plants to a 24-h LD from incandescent lamps (data not shown; Bagnall and King, 2001
For studies of petiole growth, plants were either kept in the standard 8-h SD from fluorescent lamps or exposed to a LD given as an additional 16 h of light either from incandescent bulbs (FR-enriched light) or from fluorescent lamps (R-rich light) and both at an irradiance of 10 µmol m–2 s–1. For 10-min R or FR light EOD exposures terminating the 8-h SD, FR light was obtained using a plastic cutoff filter and R was from red fluorescent lamps, as we described previously (Bagnall and King, 2001 Although we found no evidence of a touch effect, to minimize any touching we used calipers for daily measurements of petiole elongation. Single young petioles from 16 or more plants were measured in studies of elongation and, for studies of gene expression, young elongating petioles were harvested from 16 or more plants. The studies of gene expression required the use of a green safe light when young petioles were harvested during a dark period. All our findings were confirmed in duplicate experiments some of which are presented here.
Total RNA was extracted from young elongating petioles using an RNeasy Plant Mini kit (Qiagen, Clifton Hills, Australia) and treated with RNase-free DNase (Qiagen) according to the manufacturer's instruction. One or two micrograms of total RNA were reverse-transcribed using Super Script II (Invitrogen, Mt. Waverley, Australia) according to the manufacturer's instruction. The cDNA was diluted 5- or 25-fold and 4 µL used in a 20-µL Q-PCR with QuantiTect SYBR Green PCR Master Mix (Qiagen) or in a 10-µL Q-PCR with SYBR Green JumpStart Taq ReadyMix (Sigma Aldrich, Castle Hill, Australia). Q-PCR was performed on a Rotor-Gene 2000 Real-Time Cycler (Corbett Research, Sydney). Cycling and reaction conditions were as described in Klok et al. (2002)
Mutant Selection and Production of Gene Silencing Lines
The phyA-211 and phyB-9 mutants in Columbia were described previously (Reed et al., 1993
We thank Cheryl Blundell for her help with maintaining plants and Drs. Tony Miller, Masumi Robertson, and Peter Waterhouse for guidance with molecular techniques. Drs. Peter Hedden and Andy Phillips (BBSRC, UK) are thanked for supplying the Columbia 20-oxidase antisense lines that were used previously in the study of Coles et al. (1999) . For helpful comments on the manuscript, we thank Drs. Lloyd Evans, Neil Olszewski, and Masumi Robertson. During his stay in Canberra, T.H. was supported by a NARO Research Abroad Grant for Young Scientists. Received January 12, 2005; returned for revision February 10, 2005; accepted February 15, 2005.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.059055. * Corresponding author; e-mail rod.king{at}csiro.au; fax 62–262465275.
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) or exposed to two LD cycles (
).The shaded areas on each graph indicate the 16-h period of either darkness in SD or low intensity (10 µmol m–2 s–1) light from incandescent lamps for LD treatments. Changes in gene expression are shown as fold increases relative to the time zero value, which, generally, was the lowest value. The dashed line on the second day is the SD samples from the day before, although a repeat of this SD sampling to cover 2 SD (
). Other conditions as in 
-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10: 2115–2126
