JXB Advance Access originally published online on March 14, 2005
Journal of Experimental Botany 2005 56(415):1327-1334; doi:10.1093/jxb/eri133
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RESEARCH PAPER |
Gibberellin-regulated XET is differentially induced by auxin in rice leaf sheath bases during gravitropic bending
1Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China
2Centre for Research in Plant Science, Faculty of Applied Sciences, University of the West of England, Bristol, Frenchay, Bristol BS16 1QY, UK
* To whom correspondence should be addressed: Fax: +86 21 54924015. E-mail: wmcai{at}iris.sipp.ac.cn
Received 24 August 2004; Accepted 4 February 2005
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Abstract |
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The asymmetric distribution of auxin plays a fundamental role in plant gravitropism, yet little is understood about how its lateral distribution stimulates growth. In the present work, the asymmetric distribution not only of auxin, but also that of gibberellins (GAs), was observed in rice leaf sheath bases following gravistimulation. Gravistimulation induced the transient accumulation of greater amounts of both IAA and GA in the lower halves of the leaf sheath bases of rice seedlings. OsGA3ox1, a gene of active GA synthesis, was differentially induced by gravistimulation. Furthermore, 2,3,5-tri-iodobenzoic acid (TIBA), an inhibitor of auxin transport, substantially decreased the asymmetric distribution of IAA and the gradient of OsGA3ox1 expression. Externally applied GA3 restored the gravitropic curvature of rice leaf sheaths inhibited by either TIBA or by ancymidol, a GA synthesis inhibitor. The expression of XET (encoding xyloglucan endotransglycosylase) was differentially induced in the lower halves of gravistimulated leaf sheath bases and was also up-regulated by exogenous IAA and GA3. Both ancymidol and TIBA decreased the gradient of XET expression. These data suggest that the asymmetric distribution of auxin effected by gravistimulation induced a gradient of GAs via asymmetric expression of OsGA3ox1 in rice leaf sheath bases, and hence caused the asymmetric expression of XET. Cell wall loosening in the curvature site of the leaf sheath triggered by the expression of XET would contribute to gravitropic growth.
Key words: Auxin, gibberellin, gravitropism, OsGA3ox1, XET
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary dataReferences |
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Plant organs possess the ability to guide their growth in relation to humidity, chemicals, light, touch, and gravity, and the ability of plants to use gravity for growth has been recognized for two centuries (Knight, 1806
). Gravitropism, one of the most important phenomena in plant growth and development, is the asymmetric growth or curvature of plant organs in response to gravistimulation. Differential growth of plants in response to changes in the gravity vector requires a complex signal transduction cascade. The involvement of endogenous growth substances in the gravitropic growth response in higher plants has been postulated and there is much supporting experimental evidence. With regard to auxins, altered gravitropic responses have been observed in mutants with modified auxin metabolism and transport; differential auxin accumulation has been demonstrated through the use of radiolabelled auxin; auxin-inducible gene reporter systems have been described; and gravitropic responses can be blocked by inhibitors of auxin transport (reviewed by Gloria, 2001; Blancaflor and Masson, 2003). Tropic processes appear to be under the control of more than one hormone and other plant hormones have been investigated for their involvement in gravitropic curvature. Recent studies have shown that gravi-incompetent coleoptile-less seedlings of rye exhibit gravi-competence following the exogenous application of ethylene. Furthermore, continuous perception of ethylene was found to be necessary for the reinstatement of the gravitropic growth response in seedlings and for the transduction of the gravitropic signal (Edelmann, 2002; Edelmann et al., 2002; Kramer et al., 2003). Gibberellins are a class of plant hormones that exert profound and diverse effects on plant growth and development (Yamaguchi and Kamiya, 2000; Masashi et al., 2002) and that have been implicated in tropic growth responses since the 1970s. The redistribution of gibberellins during the gravitropic responses of roots and coleoptiles has been described (Janet and Malcolm, 1974). The application of GA3 or GA4/7 accelerated shoot curving in grasses (Hedden et al., 1982; Kaufman and Dayanandan, 1984; Kaufman et al., 1985; Brock and Kaufman, 1988) and of lateral branches of decapitated or intact conifers (Pickard, 1985). The differential localization of GA-like substances occurs between the lower and upper halves of gravistimulated shoots of oats, sunflowers and maize (Phillips, 1972a; Pharis et al., 1981; Rood et al., 1987).
Recent studies have highlighted the importance of hormone interactions or ‘crosstalk’, and how these interactions can affect both hormone biosynthesis and signal transduction (Kende et al., 1998; Grossmann, 2000; Ross and O'Neill, 2001; Peeters et al., 2002; Swarup et al., 2002). Some hormone interactions may be involved in gravitropic curvature in plants. Golan et al. (1996) reported that cytokinin, acting through ethylene, restored gravitropism to Arabidopsis seedlings grown under red light and other data indicate that brassinosteroids (BRs) might be involved in auxin-mediated processes for the gravitropic response (Kim et al., 2000). A new link between the ‘classical’ plant hormones auxin and GA has been demonstrated by Ross and colleagues (Ross et al., 2000; O'Neill and Ross, 2002). These data indicate that auxin, indole-3-acetic acid (IAA), can promote the biosynthesis of the active GA1 in pea shoots. Since IAA and GAs are both involved in gravitropism, the possibility of crosstalk between these two hormones was explored during the gravitropic curvature of rice leaf sheaths.
During morphogenesis at any developmental stage, all plant cells require modifications of the cell wall structure. The cell wall is the main factor that determines cell shape and cell wall reconstruction makes possible its modification during cell elongation. According to a cell wall model (McQueen-Mason, 1996; Cosgrove, 1997b), the primary cell wall consists of three co-extensive polymer networks: the cellulose–xyloglucan framework, pectin, and structural protein. It is considered that structural changes in these networks are regulated by enzymatic modification, and therefore wall-modifying enzymes would be expected to play an important role in regulating the plasticity of the cell wall. Xyloglucan endotransglycosylase (XET) catalyses the transglycosylation of xyloglucan, the major hemicellulose polymer that is thought to mediate the cross-linking of cellulose microfibrils in the cell wall and has been proposed to be involved in the control of cell wall relaxation (Nishitani and Tominaga, 1991; Fry et al., 1992). In various species, including both dicot and monocot plants, XET is encoded by a multigene family, and it may be that expression of the individual XET genes is differentially regulated at various developmental stages and by diverse environmental stimuli (Xu et al., 1996; Schünmann et al., 1997; Uozu et al., 2000). Some of these XET genes have been shown to be specifically up-regulated by various growth-promoting hormones, such as auxin and GAs (Potter and Fry, 1994; Xu et al., 1995; Smith et al., 1996; Catalá et al., 1997; Uozu et al., 2000). In addition, there have been several cases where significant correlations between high levels of XET activity and tissue elongation have been described (Nishitani and Tominaga, 1991; Schünmann et al., 1997; Burstin, 2000; Uozu et al., 2000). The data presented in this paper suggest that XET, regulated by the gradient of auxin and GAs, is involved in the hormone-mediated differential growth of the upper and lower halves of horizontally-orientated leaf sheaths during gravitropic bending in rice seedlings.
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Materials and methods |
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Plant material
Rice plants (Oryza sativa L. No. 4 Shengxiangjing) were germinated and then grown in nutrient solution (Ni, 1985
) at a photon flux density of 350–400 µmol m–2 s–1, 60–80% relative humidity, 12/12 h day/night cycle at 25 °C in a phytotron. All experiments were performed with 3–4-week-old seedlings.
Gravitropic stimulation
Before being gravistimulated, the seedlings were kept in darkness for 12 h. At time zero, the seedlings were gravistimulated by rotating their pots through 90° (the pots were covered in parafilm to prevent spillage of the growth medium). Control plants were kept vertical. The whole process was carried out in the dark. At the appropriate times, the curvature of the leaf sheath was determined (Rüdiger and Weiler, 1983). The bending leaf sheath bases (1 cm length above root) were cut (Fig. 1A) and the upper and lower halves prepared by bisection with a razor blade. After treatments or manipulations, seedlings or excised tissues to be used for hormone or RNA extraction were immediately frozen in liquid nitrogen (within 7–10 s) and stored at –70 °C.
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Hormone isolation and ELISA (Enzyme-Linked Immunosorbent Assay) analysis
Frozen tissue was ground with a mortar and pestle and hormones extracted in 80% methanol. Samples were centrifugated at 10 000 g for 15 min at 4 °C. The supernatant was collected and immediately applied to a pre-equilibrated C18 Sep-Pak cartridge [Millipore (Waters), Watford, UK], which was washed with 80% methanol solution and eluted with methanol:acetic acid (4:1, v/v). IAA and GA1/3 concentrations were then determined by ELISA (Nanjing Agricultural University, China). Ninety-six-well immunoassay plates were coated with 0.2 ml of a solution of rabbit anti-mouse IgG (1:20 000) in 50 mM NaHCO3, pH 9.6 and incubated at 4 °C for 16 h. The supernatant was discarded and the plates washed with water. Anti-IAA or anti-GA monoclonal antibody (mAb; 0.2 ml, 1:10 000) in 50 mM NaHCO3, pH 9.6) was added to the immunoassay plate wells and incubated at 4 °C for 24 h. The conjugates were then removed by washing three times with water. Experimental samples or standard hormone solutions were dispensed into each well and incubated at 4 °C for 1 h. Alkaline phosphatase solution (100 µl) diluted 1:500 in TBS (50 mM TRIS, 150 mM NaCl, 1 mM MgCl2, pH 7.8) was added into each well and incubated at 4 °C for 3 h. The conjugates were removed by washing three times with water and the plates incubated at room temperature for 1 h. The conjugate was removed by washing as before. p-Nitrophenyl-palmitate (150 µl at 1 mg ml–1 in 50 mM NaHCO3, pH 9.6) was then dispensed into each well and the colour reaction stopped by the addition of 50 µl 5 M KOH. Optical densities were measured at 410 nm (Yang et al., 2001
; Nakayama et al., 2002).
Inhibition of IAA transport and GA synthesis in rice leaf sheath bases during gravistimulation
To assess the effects of IAA and GA, plants were placed so that their roots were submerged in nutrient solution (control) or nutrient solution containing IAA (1 and 10 µM) or GA3 (1 and 10 µM). To determine the effect of the auxin transport inhibitor TIBA (2,3,5-tri-iodobenzoic acid) and the GA synthesis inhibitor ancymidol, the rice seedlings were placed in control nutrient solutions or solution containing TIBA (30 µM) or ANC (50 µM) and gravity stimulated for the indicated time. To test the redistribution of GAs after 12 h ANC incubation, the seedlings were cultured in solution containing 1 µM GA3, and gravistimulated for the indicated times. After 12 h TIBA incubation, the seedlings were cultured in the solution containing 1 µM GA3, and gravistimulated for the indicated times in order to explore the relationship between GAs and IAA.
Reverse transcription-PCR (RT-PCR)
Semi-quantitative RT-PCR was performed to analyse the expression of OsGA3ox1 (Genbank accession number AB054084) and XET (Genbank accession number AP003340). Total RNA was isolated from rice tissues as described in Maniatis et al. (1982). The cDNA was synthesized using AMV reverse transcriptase (Takara, Japan) and 2 µl of cDNA was used for PCR amplification. The OsGA3ox1 fragment (319 bp) was amplified with the primers: 5'-GCACACGGACTCGGGCTT-3' and 5'-CTCCGGCCACGTGACAGC-3' at 94 °C for 3 min; followed by 26–28 cycles at 94 °C for 40 s, 53 °C for 50 s, 72 °C for 45 s, and finished by an extension at 72 °C for 10 min. The XET fragment (217 bp AK071574
[GenBank]
) was amplified with the primers: 5'-GGCGATGGTGGTGGCAATG-3' and 5'-TGAAGTGGCCGAAGAGGTAGG-3' at 94 °C for 3 min; followed by 22–24 cycles at 94 °C for 40 s, 62 °C for 50 s, 72 °C for 45 s, and finished by an extension at 72 °C for 10 min. The ubiquitin (UBI) gene fragment (396 bp; Nishi et al., 1993, Genbank accession number D12776), amplified with the primers: 5'-GACGGACGCACCCTGGCTGACTAC-3' and 5'-TGCTGCCAATTACCATATACCACGAC-3', was used as the internal control. Agarose gel electrophoresis was used to display the PCR products. The optical densities (imaged using a digital camera and quantified with LABWORKS software) of the OsGA3ox1, XET, and UBI amplification products were used for the relative quantification of OsGA3ox1 and XET by expression as the ratio of OsGA3ox1 or XET over UBI.
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Results |
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Hormone content during gravitropic responses of rice leaf sheath bases
Rice leaf sheaths began to bend upwards in response to gravistimulation within 12 h and gravitropic bending continued up to 96 h (Fig. 1B). The ratio of hormones in the lower halves relative to that in the upper halves of gravistimulated leaf sheath bases also began to alter shortly after gravistimulation (Fig. 2; absolute values of IAA and GA1/3 can be seen in the supplementary material at JXB online). ELISA analysis revealed that an asymmetric distribution of IAA and GA1/3 occurred during gravitropic bending with kinetics consistent with those of gravibending. A greater than 2-fold difference in IAA content was determined in the lower versus the upper halves of the leaf sheath bases after 6 h of gravistimulation. With increasing time after stimulation the relative amount of IAA in the lower halves began to decrease. The relative amount of GA1/3 in the lower halves of gravistimulated leaf sheath bases also increased, but with slower kinetics than the changes in IAA content. Thus, these data show that a gravity stimulus not only increased the content of IAA, but also that of GA1/3 in the lower halves of bending rice leaf sheath bases. The auxin transport inhibitor TIBA effectively abolished the asymmetric distribution of GA1/3.
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Effect of gravistimulation and TIBA on OsGA3ox1 expression
Expression of the GA biosynthesis gene OsGA3ox1 (Itoh et al., 2001
) in gravistimulated rice leaf sheath bases was analysed by RT-PCR. After 6 h gravistimulation, an asymmetric expression of OsGA3ox1 was observed. At this time, the level of expression of OsGA3ox1 in the lower side was about 1.6-fold higher than in the upper side (Fig. 3A). After 12 h of gravistimulation the expression level of OsGA3ox1 was more than 8-fold higher in the lower halves of the leaf sheath bases. With increasing time, OsGA3ox1 expression on the lower side began to decline, whereas that on the upper side increased, such that after 24 h, the reverse gradient of expression was evident. Treatment with TIBA greatly reduced decrease the gradient of OsGA3ox1 expression (Fig. 3B).
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The effects of gravistimulation and IAA and GA3 on XET expression
Gravistimulation resulted in increased expression of XET in both the upper and lower halves of the leaf sheath bases within 6 h, and after 12 h the level of expression was clearly higher in the lower halves (Fig. 4). At this time, there was nine times the level of XET expression in the lower compared with the upper halves. With increasing time, XET expression on the lower side began to decline in a similar way as did expression of OsGA3ox1, but with slower kinetics, such that XET expression was still higher in the lower halves after 24 h, but was reduced relative to expression in the upper halves after 48 h (Fig. 4). XET expression in vertically-orientated rice seedlings was increased by the external application of IAA and GA3 for 12 h. Treatment with 1 µM IAA induced a small increase in XET expression and treatment with 10 µM IAA significantly increased the expression of XET, to over four times that in control leaf sheath bases. Treatment with 1 µM GA3 induced a 1.8-fold increase in XET expression, but at the higher concentration of 10 µM, XET expression was actually reduced (Fig. 5).
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Inhibition of differential XET expression and gravicurvature by inhibition of auxin transport and GA biosynthesis
To investigate the potential requirement for auxin transport and GA synthesis for XET expression, seedlings were gravistimulated in the absence or presence of the auxin transport inhibitor TIBA or the GA synthesis inhibitor ancymidol. In leaf sheath bases from control seedlings, the expression of XET was 9.4-fold higher in the lower versus the upper leaf sheath (Fig. 6). This increase was reduced substantially by incubation in TIBA, down to 2.3-fold, and incubation in ancymidol abolished completely the differential expression of XET (Fig. 6). Treatment with TBA or ancymidol also reduced leaf sheath bending in response to gravistimulation. TIBA reduced gravicurvature by 35% and ancymidol by 17%. However, gravicurvature could be restored to, or even increased above, control values by the simultaneous application of GA with TIBA or ancymidol (Fig. 7).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary dataReferences |
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Since the ability of plant organs to use gravity as a guide for growth was first recognized by Knight in 1806 (Knight, 1806
), a large number of biochemical and molecular studies have indicated that an asymmetric redistribution of hormones is involved in the gravitropic response (Rood et al., 1987; Gloria, 2001; Blancaflor and Masson, 2003; Kramer et al., 2003). Moreover, it has also been shown that hormone interactions are important (Golan et al., 1996; Kim et al., 2000). In the present work, the asymmetric distribution of IAA and GA1/3 in rice leaf sheath bases was observed after the rice seedlings were rotated 90° from the vertical position (Fig. 2; supplementary data can be seen at JXB online). After 6 h of gravistimulation, the content of IAA on the lower side of the rice leaf sheath bases was 2-fold that of the upper side. With prolonged stimulation, the lower/upper IAA ratio decreased. The lower/upper GA ratio, on the other hand, peaked later, at 12 h, before declining, kinetics that would be consistent with a requirement for IAA redistribution before activation of GA biosynthesis. A series of studies has revealed that IAA can indeed promote the biosynthesis of bioactive GA1 in pea shoots via the increased expression of the GA biosynthesis gene PsGA3ox1, encoding a key enzyme regulating the synthesis of active GAs (Ross et al., 2000; O'Neill and Ross, 2002). Other interactions between IAA and GAs have been reported recently (Fu and Harberd, 2003). The RT-PCR data described here demonstrate that expression of the rice gene OsGA3ox1 was induced by gravistimulation. After 12 h gravistimulation there was significant asymmetric expression of OsGA3ox1 in rice leaf sheath bases, such that expression of OsGA3ox1 on the lower side was about 8-fold higher than that on the upper side (Fig. 3A). The kinetics of asymmetric OsGA3ox1 expression and IAA and GA accumulation would be consistent with gravity inducing a redistribution of IAA that induced differential expression of OsGA3ox1 and the subsequent asymmetric distribution of GA. Furthermore, the inhibitor of auxin transport TIBA substantially reduced the asymmetric distribution of IAA and the gradient of OsGA3ox1 expression (Figs 2, 3B). Phillips and co-workers showed that GA asymmetry in gravitropically and phototropically stimulated stems and coleoptiles is not necessarily a result of lateral GA transport (Phillips, 1972b; Railton and Phillips, 1973; Phillips and Hartung, 1976). The data from this study indicate that gravity-induced redistribution of auxin results in the differential expression of OsGA3ox1, and thus activates differential biosynthesis of GAs in the lower relative to the upper halves of rice leaf sheath bases. The expression of the other two genes potentially important in GA biosynthesis, OsGA20ox2 and OsGA3ox2, was also analysed and no induction of differential expression by gravistimulation was observed (see the figure in the supplementary data available at JXB online).
Current studies are focused on understanding the mechanisms by which hormone transport and distribution are regulated, and on how the lateral distribution of hormones can stimulate differential growth. Some processes, such as epinastic leaf movement, photonastic responses, and gravitropic curvature are all based on differential growth of the upper and lower plant organ surface. In biophysical terms, the plant cell is a pressurized, fluid-filled sac confined and given shape by the relatively tough wall. To enlarge, the cell must extend its wall and at the same time take up water and solutes to fill the sac and maintain turgor pressure. Growing cells take up water because of wall stress relaxation, which causes a minor reduction in the water potential and turgor of the cell (Cosgrove, 1993). A number of enzymes that act in loosening the cell wall have been identified. The strengths and weaknesses of the wall ‘loosening enzymes’ concept and the possibility of their involvement in the bending response of stems have been reviewed recently (Cosgrove, 1997a). It was pointed out that a range of proteins and enzymes including expansins and xyloglucan endotransglycosylase are likely to be involved in the gravitropic curvature of plant stems.
The data presented here suggest that XET, a wall-loosening enzyme, may be involved in the gravitropic curvature of the rice leaf sheath. The RT-PCR results show that expression of XET on the lower side was stronger than that on the upper side of the leaf sheath bases after the rice seedlings were exposed to the gravistimulation (Fig. 4). In agreement with a proposed role in plant growth, XET activity levels were found to be high in rapidly growing tissues (Nishitani and Tominaga, 1991; Schünmann et al., 1997; Burstin, 2000; Uozu et al., 2000), and GA treatment, which induces the elongation of leaves and leaf sheath bases in several plant species, increases XET activity (Potter and Fry, 1994; Smith et al., 1996). Furthermore, specific XET genes have been shown to be up-regulated by auxin and GA (Xu et al., 1996; Catalá et al., 1997; Schünmann et al., 1997; Jan et al., 2004). Here, the expression of XET was also increased by exogenous 10 µM IAA and 1 µM GA3 (Fig. 5). Furthermore, either inhibition of IAA transport (by TIBA) or inhibition of GA biosynthesis (by ancymidol) both decreased the expression of XET and its expression gradient between the lower side and upper side of gravistimulated leaf sheath bases (Fig. 6). Thus, these data suggest that gravity-induced IAA and GA gradients trigger the differential expression of XET in the rice leaf sheath bases. The data also show that after inhibition of auxin transport by TIBA or inhibition of GA synthesis by ANC, gravitropic curvature was depressed, but that exogenous GA3 could restore gravitropic curvature, suggesting that GA synthesis is induced by auxin. The effects of TIBA and ANC were different with respect to XET expression and gravibending, ANC having a greater effect on the reduction in asymmetric XET expression, but TIBA having more effects on gravibending. One possible explanation for them would be that TIBA reduces the expression of other wall-loosening proteins such as expansins (Cosgrove, 1997a). The preliminary data indicate the expansin expression is indeed altered during gravibending (data not shown).
In conclusion, these data suggest that the gravity-induced redistribution of auxin results in the differential expression of OsGA3ox1, and thus activates differential biosynthesis of GAs in the lower relative to the upper halves of rice leaf sheath bases. This asymmetric distribution of GAs then activates differential expression of XET in rice leaf sheath bases which would trigger cell wall loosening in cells in the lower side of the leaf sheath bases and result in upwards growth.
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Supplementary data |
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Supplementary information (a table and a figure) is available at JXB online.
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Acknowledgements |
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This work was supported by the Chinese Academy of Sciences (Grant No. KSCX2-SW-322), Shanghai Institute of Plant Physiology and Ecology, National Natural Science Foundation of China (No. 39770199), UK–China collaboration was supported by The Royal Society and a Biotechnology and Biological Sciences Research Council (UK) China Partnering Award.
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Footnotes |
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Abbreviations: ANC, ancymidol; GAs, gibberellins; IAA, indole-3-acetic acid; TIBA, 2,3,5-tri-iodobenzoic acid; XET, xyloglucan endotransglycosylase gene; UBI, ubiquitin gene.
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References |
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