Journal of Experimental Botany, Vol. 54, No. 393, pp. 2701-2708,
December 1, 2003
© 2003 Oxford University Press
Interaction between two auxin-resistant mutants and their effects on lateral root formation in rice (Oryza sativa L.)
Received 7 July 2003; Accepted 4 September 2003
1 Faculty of Agriculture, Kagawa University, Miki, Kagawa 761-0795, Japan
2 Radioisotope Research Center, Kobe University, Rokkodai, Nada-ku, Kobe 657-8501, Japan
* To whom correspondence should be addressed: Fax: +81 87 891 3127. E-mail: s01x604{at}stmail.ag.kagawa-u.ac.jp
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Abstract |
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Since root elongation is very sensitive to auxin, screening for reduced inhibition in root elongation has been an important method for the detection of auxin-resistant mutants. Two recessive auxin-resistant lines of rice (Oryza sativa L. ssp. indica cv. IR8), arm1 and arm2, have been isolated by screening for resistance to 2,4-dichlorophenoxyacetic acid (2,4-D). arm1 displays a variety of morphological defects including reduced lateral root formation, increased seminal root elongation, reduced root diameter, and impaired xylem development in roots, while the arm2 phenotype is almost similar to wild-type IR8 except for a slightly reduced lateral root formation, impaired xylem development in roots and an enhanced plant height. Although the growth of arm2 roots exhibited a resistance to 2,4-D, it was sensitive to 1-naphthaleneacetic acid (NAA) as the wild type. At the same time, the arm2 roots showed a reduced [14C]2,4-D uptake while uptake of [3H]NAA was normal, suggesting that the resistance to 2,4-D of arm2 roots is due to a defect in 2,4-D uptake. To investigate the possible interaction between arm1 and arm2 genes, a double mutant has been constructed. The roots of arm1 arm2 double mutant were more resistant to 2,4-D and formed fewer lateral roots than those of either single mutant, suggesting that the two genes show synergistic effects with respect to both auxin response and lateral root formation. By contrast, all these mutants displayed the normal gravitropic response in roots, as did the wild-type plants. Taken together, Arm1 and Arm2 genes seem to function in different processes in the auxin-response pathways leading to lateral root formation.
Key words: Auxin influx, auxin-resistant mutant, 2,4-dichlorophenoxyacetic acid, gravitropic response, lateral root formation, rice root, root elongation, xylem development.
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Introduction |
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Auxins are plant hormones that regulate almost every aspect of plant growth and development including cell enlargement and division, lateral branching of shoots and roots, vascular differentiation, gravitropism, and early embryonic development (Davies, 1995; Hobbie, 1998). Roots are important and attractive systems to study auxin action because of their morphological simplicity and well-characterized auxin responses (Hobbie and Estelle, 1995). Since root elongation is sensitive to auxin, screening for reduced auxin sensitivity has been an important approach for the detection of auxin-response mutants (Evans et al., 1994; Lincoln et al., 1990; Pickett et al., 1990; Wilson et al., 1990). In Arabidopsis, several auxin-resistant mutants have been isolated and these mutants have proved to be attractive materials in the determination of the mechanism of auxin actions (Gray et al., 1999).
Recently, Hao and Ichii (1999) isolated a dominant auxin-resistant mutant in rice (Oryza sativa L. ssp. japonica cv. Oochikara) in a screen for 2,4-dichlorophenoxyacetic acid (2,4-D) resistance and named it Lrt1 (lateral rootless). Lrt1 also exhibited resistance to synthetic auxin 1-naphthaleneacetic acid (NAA) and natural auxins indole-3-acetic acid (IAA) and indole-3-butyric acid (IBA) (Chhun et al., 2003). In addition to auxin resistance, Lrt1 is a lateral rootless mutant showing delayed root gravitropic response and reduced root hairs, suggesting that auxin is required for normal root growth in this process.
In the present study, two non-allelic recessive mutations of a different rice cultivar (Oryza sativa L. ssp. indica cv. IR8), arm1 and arm2, derived from a screen for 2,4-D resistance have been analysed. By crossing the two mutants a double mutant has been constructed that exhibits a greater resistance to 2,4-D in root elongation with fewer lateral roots compared with either single mutant. The uptake of labelled [14C]2,4-D has been investigated in roots of arm1, arm2, the double mutant, and wild-type IR8. The results show that Arm1 and Arm2 genes are involved in different processes of the auxin response pathway required for lateral root formation.
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Materials and methods |
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Plant materials
Rice mutant MT16, MT37 and the double mutant derived from a cross between the two mutants were used in this study. MT16 and MT37 were isolated from indica type rice cv. IR8 in a screen for 2,4-D resistance. MT16 and MT37 were then characterized and designated as arm1 and arm2 (auxin-resistant mutant), respectively.
Chemicals
Labelled 2,4-dichlorophenoxyacetic acid [2,4-D, ring-14(U)] (specific activity 55mCi mmol–1) and 1-naphthaleneacetic acid [NAA, 4-3H] (specific activity 25Ci mmol–1) were purchased from American Radiolabeled Chemicals, Inc. (USA). Scintisol EX-H was from Dojindo Laboratories (Kumamoto, Japan). 2,4-D and NAA were from Nacalai Tesque Inc. (Kyoto, Japan) and Sigma Chemical Co. (St Louis), respectively.
Mutagenesis and screening
Rice seeds of wild-type IR8 were treated with 1 mM sodium azide for 6 h. Around 62 000 M2 seeds derived from selfing of M1 plants were sterilized with 0.2% Benomyl (Dupont Company, Tokyo, Japan) and germinated in deionized water for 48 h at 25 °C in a glass-covered growth chamber placed in a greenhouse. Germinating seeds were sown on net floats (10x20 cm) in water supplemented with 1 µM 2,4-D and grown for 7 d. Putative resistant mutants were transferred to Kimura’s B solution (pH 5.0) containing 182 µM (NH4)SO4, 274 µM MgSO4.7H2O, 91 µM KNO3, 90 µM KH2SO4, 45 µM K2SO4, 176 µM Ca(NO3)2.4H2O, and 7 µM FeC6H5O7.xH2O for 7 d to allow recovery and then transplanted to pots in a glasshouse to produce M3 seeds. M3 progeny of the selected M2 plants were retested for 2,4-D resistance. At least five mutants were shown to be stably resistant to 2,4-D. From these lines, arm1 and arm2 were selected and used in the present study.
Genetic analysis
To investigate genetic segregation in auxin-resistant mutants, arm1 and arm2 were crossed with wild-type IR8. All F1 progeny was tested in Kimura’s B supplemented with 1 µM 2,4-D for 7 d. The recovered F1 seedlings were transferred to Kimura’s B and transplanted to pots. F1 plants were allowed to self-fertilize and F2 segregation was observed by sowing the seeds on 1 µM 2,4-D medium. A complementation test was also done by crossing arm1 with arm2 to investigate their allelism, and to examine possible genetic interactions between arm1 and arm2.
Auxin resistance analysis
To evaluate auxin resistance, seedlings were grown in glass cups containing 400 ml water supplemented with or without various concentrations of 2,4-D or NAA. The seedlings were allowed to grow under continuous white fluorescent light (FL20S.W, Toshiba, Japan) at an irradiance of approximately 67 µmol m–2 s–1 at 25 °C for 7 d. Data were presented as the percentage of root length on water culture supplemented with auxin relative to root length on auxin-free medium.
Histological analysis
Rice seedlings were grown in water under continuous white fluorescent light at 25 °C for 3 d. About 1 cm of root tips was taken from the seminal root and then fixed with acetic acid:ethanol (1:3 v:v) for 24 h. Serial ethanol dehydration was then performed (70, 80, 90, 95, and 100% [twice]) at room temperature for 1 h at each step. Samples were embedded in Technovit 7100 resin. Sections were cut at a thickness of 6 µm, placed on glass slides, dried and observed using a microscope (Olympus BX50-3, Olympus Optical Co., Ltd. Japan).
Auxin uptake analysis
Rice seedlings were grown for 3 d in water without auxin under continuous white light at 25 °C. Root tips of 1 cm in length were excised from them. Twenty excised root tips were transferred to a 2.6 cm Petri dish containing 1 µM [14C] 2,4-D (2.06 KBq ml–1) or 1 µM [3H] NAA (4.7 KBq ml–1) in 10 mM 2-(N-morpholino)ethanesulphonic acid (MES) buffer (pH.5.7) and incubated for 30 min with a gentle shaking. After incubation, the root tips were carefully washed twice for 60 s with fresh MES buffer and 20 roots were divided into four groups. The surface water of roots was carefully removed by filter paper and fresh weight of five roots was measured, and then they were soaked overnight in 5 ml liquid scintillation fluid (Scintisol EX-H). Fresh weight of roots did not significantly change during the 30 min incubation. Radioactivity was counted with a scintillation counter (model LS6500, Beckman Instruments, Fullerton, CA). Although 1 cm root tip segments were used in all these auxin uptake experiments, the diameter of mutant root was slightly different from wild-type roots. To find a reasonable method to evaluate auxin uptake in mutant and wild-type roots, the auxin accumulation in roots was expressed in three ways: radioactivity accumulation per 1 cm root segment, per mg fresh weight of root segment and per mm2 surface area of root segment (as shown in Table 4 of the Results).
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Estimation of the surface area of a 1 cm root tip
The surface area of 1 cm root tip was estimated as follows. When the shape of 1 cm root is assumed as a cylinder, the surface area is approximately expressed as:
Y=
r2+10x2r(1)
where Y (mm2) is the surface area of a 1 cm root and r (mm) is the radius of root. Since the root has a tip, the base area of cylinder is omitted in the equation 1. When the density of root is assumed as 1, the weight of 1 cm root is expressed as:
Z=10xr2(2)
where Z (mg) is the weight of 1 cm root. From equation 2, equation 1 can be rewritten as:
Y=Z/10+2(10Z)1/2(3)
Analysis for gravity response in roots
Rice seedlings were grown vertically in plastic cases (10x14x 1.5 cm) containing 1% agar under continuous white light at 25 °C for 3 d and then they were rotated by 90°. The gravitropic bending of root tips was measured every 2 h after the reorientation.
Statistical analysis
The experiments were repeated three to four times and the Student’s t-test was used for statistical analysis on the difference between mutant and wild-type plants. For analysing genetic segregation, the chi-square test was performed.
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Results |
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Isolation of 2,4-D resistant mutants
To investigate molecular mechanism for auxin action, mutants which derived from wild-type IR8 (WT) treated with 1 mM sodium azide were screened. Five 2,4-D resistant lines were isolated. Among them, arm1 and arm2 were used in this study. The arm1 and arm2 seedlings were able to elongate their roots in Kimura’s B medium even in the presence of 1 µM 2,4-D, where the growth of wild-type roots was almost completely inhibited.
Genetic analysis
To determine the genetic basis for auxin resistance in arm1 and arm2 mutants, the two lines were crossed to wild-type IR8. The resulting F1 plants were all auxin-sensitive, and either F2 segregation was 3:1 (3 sensitive, 1 resistant) (Table 1). Therefore, the resistance to 2,4-D in arm1 and arm2 is due to a respective single recessive mutation. To test their allelism, they were crossed with each other. All F1 progeny from this cross was sensitive to auxin (Table 1), indicating that the two mutant genes are not allelic. Segregation of F2 progeny fitted to a 9:3:3:1 ratio (9 wild type, 3 arm1, 3 arm2, 1 double mutant). The genotype of the double mutant was confirmed by analysing F3 progeny.
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Morphological analysis
To compare the morphology of mutants, seedlings were grown in water for 7 d. As shown in Table 2, arm1 seedlings exhibited a greater level of seminal root elongation, fewer lateral roots per plant, less lateral root density, and slightly shorter crown roots compared with wild-type IR8, while no significant difference was observed in root number and plant height. By contrast, arm2 showed a greater plant height and slightly fewer laterals on both seminal roots (Table 2; Fig. 1) and crown roots (data not shown) compared with the wild type.
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In the arm1 arm2 double mutant, lateral root formation was dramatically reduced compared with parental single mutant plants (Table 2; Fig. 1), suggesting that the two mutant genes provided synergistic effects in inhibiting lateral root formation. By contrast, many other phenotypes of the double mutant plants are similar to parental arm1 plants in root number, crown root length and plant height. Although the length of the seminal roots of the double mutant is slightly shorter than that of arm1 and longer than arm2, the length of double mutant roots is closer to arm1 roots compared with arm2 roots.
Root structure was also compared by analysing their cross-sections at about 9 mm from the root tips (Table 3; Fig. 2). The diameters of arm1 and double mutant roots were narrower compared with the wild type. In arm1 roots, both the stele diameter and cortical cell diameter were reduced while the number of cortical cell layers was normal. By contrast, in the double mutant, one cell layer was missing from the cortex. The diameters of protoxylem and metaxylem were narrower in arm1, arm2 and double mutant roots compared with the wild type, suggesting that the two genes may be involved in xylem development in roots.
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Auxin resistance
In order to evaluate quantitatively the level of resistance to auxin, the dose–response of root elongation was measured for 2,4-D. Seedlings of arm1, arm2, the double mutant arm1 arm2, and wild-type IR8 were grown with various concentrations of 2,4-D for 7 d. The result of the assay is presented in Fig. 3. The roots of arm2 are more resistant than those of wild-type IR8 in the range from 0.1–1 µM, while the response to 2,4-D of arm1 roots is complex. At 0.01 µM 2,4-D, arm1 roots unexpectedly exhibited a slightly higher sensitivity (0.01<P<0.05) to auxin compared with the wild type. However, in higher concentrations (0.1–1 µM), arm1 roots were resistant to 2,4-D and showed a greater resistance to 1 µM 2,4-D than arm2 roots. As a result, the dose–response curve for arm1 roots is crossed with those for wild-type and arm2 roots. The double mutant roots were more resistant to 2,4-D than parental single mutants and the greater resistance of the double mutant was striking at 1 µM 2,4-D (P <0.01) (Figs 3, 4).
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In order to compare quantitatively the resistance to auxin, the concentration of 2,4-D which induced a 50% inhibition in root elongation (IC50) was calculated. IC50 for arm1, arm2, and wild-type IR8 was 0.3 µM, 0.3 µM, and 0.05 µM, respectively. The 2,4-D-induced inhibition in the growth of double mutant roots did not reach 50% even at the highest concentration (1 µM 2,4-D) (Fig. 3). Although, the IC50 value for arm1 is the same as arm2, the slopes of the dose–response curves for these mutants are different. The slope for arm2 is similar to that of the wild type, while the slope for arm1 is gentler than that of arm2 as described above.
Reduced auxin accumulation in arm2 roots
In order to determine whether or not the resistance phenotype of mutant roots is due to a change in auxin uptake, the accumulation of radioactivity was examined in 1 cm root tips incubated with 1 µM [14C]2,4-D for 30 min using mutants and the wild type. Since the accumulation of radioactivity in root tip segments increased linearly up to 1 h (data not shown), the accumulation for the initial 30 min was measured.
To find the best way to compare auxin uptake between thick roots, as for the wild type, and thin roots as for arm1, auxin uptake was expressed in three ways as shown in Table 4; radioactivity accumulation per 1 cm root, per mg fresh weight and per mm2 surface area. The surface area of root segments was estimated from equation 3. From Table 4, it was concluded that auxin accumulation per mm2 surface area is the best method of comparing auxin uptake because of the following two reasons. First, since labelled 2,4-D is taken up through the surface of roots, the surface area is the most important factor in short-term experiments. Second, the data expressed per surface area are well correlated to genotypes, suggesting that the arm2 mutant shows a reduced 2,4-D uptake while the arm1 mutant shows normal uptake. The reduced auxin accumulation in arm2 roots and in the double mutant arm1 arm2 roots was significant for all three methods, suggesting that arm2 and double mutant roots are defective in 2,4-D uptake.
Normal uptake of NAA in arm2 roots
Delbarre et al. (1996) reported that an influx auxin carrier facilitates the uptake of 2,4-D, but not NAA which enters the cells through diffusion. This concept has been supported using Arabidopsis roots (Yamamoto and Yamamoto, 1998; Marchant et al., 1999; Rahman et al., 2001). To differentiate carrier uptake from diffusion, the uptake of 1 µM [3H] NAA was examined. As shown in Table 5, the accumulation of labelled NAA in arm2 and double mutant roots was similar to the wild type, suggesting that 2,4-D uptake is mediated by an auxin carrier.
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Furthermore, the effect of NAA was examined on the growth of roots in arm2 and wild-type IR8. As shown in Fig. 5, arm2 roots did not show any resistance to NAA, although the resistance to NAA was observed in arm1 and double mutant roots. These results are consistent with the idea that arm2 has a defect in auxin uptake.
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Normal gravitropic response in the roots of auxin-resistant mutants
Many auxin-resistant mutants have been reported as defective in gravitropic response as well as in lateral root development (Hobbie, 1998). This information prompted an examination of the gravitropic response of the mutants used in this work. Unexpectedly, arm1, arm2 and the double mutant roots bent towards the gravity to the same extent as the wild-type roots after reorientating the seedlings by 90° (Fig. 6).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Two non-allelic rice mutants, arm1 and arm2, showing a reduced sensitivity to 2,4-D in a root elongation assay have been isolated. Both arm1 and arm2 mutants are controlled by a respective single recessive gene (Table 1) and display reduced lateral root formation (Table 2) and impaired xylem development in roots (Table 3; Fig. 2).
In order to investigate whether or not the resistance phenotype of arm1 and arm2 mutant roots is due to a change in auxin uptake, the accumulation of radioactivity in 1 cm root tips incubated with 1 µM [14C]2,4-D for 30 min was also examined. Since arm1 roots are more slender compared with wild-type roots, the radioactivity accumulation data were analysed using the three methods shown in Table 4. It was concluded that auxin accumulation per mm2 surface area of roots was the best method for comparing auxin uptake, because auxin is taken up through the root surface and the data correlate well with root genotype. The results show that the 2,4-D uptake in arm2 roots is reduced compared with wild-type IR8, while uptake in arm1 roots is normal (Table 4). By contrast, the uptake of [3H] NAA in arm2 roots was similar to the wild type (Table 5) and arm2 roots responded to NAA in the same way as the wild type (Fig. 5). These results suggest that an auxin influx carrier is required for 2,4-D uptake in rice roots and that the arm2 mutant has a defect in auxin uptake.
In addition, the genetic relationships between arm1 and arm2 mutants have been analysed by establishing double mutant plants. The phenotypes of the double mutant were somewhat complex compared with either parental single mutant (Tables 2, 3; Figs 2, 3). The arm1 arm2 double mutant was more resistant to 2,4-D and formed fewer lateral roots than either parental single mutant, suggesting that the two mutant genes interact synergistically with respect to both auxin resistance and lateral root formation. Loss of one cortical cell layer in the double mutant roots is possibly due to another synergistic interaction of two genes. Such synergistic interaction was not observed in other phenotypes of the mutants. The diameters of protoxylem and metaxylem were reduced in arm1 and arm2 roots compared with the wild type. However, no additive effect was observed in the double mutant. To explain these interactions between arm1 and arm2 genes, the hypothesis is presented that both resistance to 2,4-D and reduced lateral root formation in arm1 are enhanced in the double mutant by reduced auxin uptake in roots, whereas other phenotypes of the double mutant are not much influenced by reduced auxin uptake. This idea suggests that the Arm2 gene is involved in lateral root formation in vivo.
Many auxin-resistant mutants of Arabidopsis, aux1, axr1, axr4, and axr6, show a defect in gravitropic response as well as in lateral root development (Hobbie and Estelle, 1995; Hobbie et al., 2000; Rahman et al. 2001; Marchant et al., 2002). An auxin-resistant mutant of rice, Lrt1, also fails to form lateral roots and shows reduced root gravitropic response (Chhun et al., 2003). The tomato mutant diageotropica (dgt), isolated for a horizontal growth pattern, does not produce lateral roots and exhibits a reduction in auxin sensitivity in the root (Muday et al., 1995). However, rice arm1, arm2 and their double mutant, which have been isolated as auxin-resistant lines, exhibited a normal gravitropic response in roots (Fig. 6). These unexpected results are consistent with the suggestion that the Arm1 and Arm2 genes are involved in lateral root formation in vivo. An alternative explanation could be that the arm2 mutant is leaky and unable to inhibit the gravitropic response.
Although auxins are effective in inhibiting root growth and lateral root formation, a higher concentration of auxin is usually required for inducing lateral roots than for root growth inhibition (Zolman et al., 2001; Chhun et al., 2003). Considering this difference, the roles of Arm1 and Arm2 genes are hypothesized as follows. If these genes or their products require relatively high concentration of auxin, they could be effective for lateral root formation only in vivo. However, when high concentrations of auxin were applied, they could be effective in inhibiting root growth as well. This may explain the results that arm1 and arm2 mutations were isolated as resistant mutants to toxic levels of auxin in the root elongation assay and that these mutations inhibit lateral root formation, but not the gravitropic response, in the absence of exogenous auxin.
In rice, no information has so far been reported on the mechanism for reduced sensitivity to inhibitory levels of auxin. In the present study, it has been demonstrated that two genes arm1 and arm2 are involved in both reduced 2,4-D sensitivity and poor lateral root formation in rice. It is also suggested that arm2 has a defect in auxin uptake and that Arm1 and Arm2 genes are involved in different processes of the auxin response pathways required for lateral root formation.
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