Annals of Botany 89: 77-82, 2002
© 2002 Annals of Botany Company
Expression Pattern of Aux/IAA Genes in the iaa3/shy2-1D Mutant of Arabidopsis thaliana (L.)
1Advanced Science Research Center, Japan Atomic Energy Research Institute (JAERI), Takasaki, Gunma 370-1292, Japan and 2Institute of Molecular and Cellular Biosciences, University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan
* For correspondence. Fax +81-273-346-9696, e-mail yoono{at}taka.jaeri.go.jp
Received: 18 June 2001; Returned for revision: 1 August 2001; Accepted: 17 September 2001.
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ABSTRACT |
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A semi-dominant mutant suppressor of hy2 (shy2-1D) of Arabidopsis thaliana, originally isolated as a photomorphogenesis mutant, shows altered auxin responses. Recent molecular cloning revealed that the SHY2 gene is identical to the IAA3 gene, a member of the primary auxin-response genes designated the Aux/IAA gene family. Because Aux/IAA proteins are reported to interact with auxin response factors, we investigated the pattern of expression of early auxin genes in the iaa3/shy2-1D mutant. RNA hybridization analysis showed that levels of mRNA accumulation of the early genes were reduced dramatically in the iaa3/shy2-1D mutants, although auxin still enhanced gene expression in the iaa3/shy2-1D mutant. Histochemical analysis using a fusion gene of the auxin responsive domain (AuxRD) and the GUS gene showed no IAA-inducible GUS expression in the root elongation zone of the iaa3/shy2-1D mutant. On the other hand, ectopic GUS expression occurred in the hypocotyl, cotyledon, petiole and root vascular tissues in the absence of auxin. These results suggest that IAA3/SHY2 functions both negatively and positively on early auxin gene expression.
Key words: Arabidopsis thaliana, auxin, Aux/IAA genes, gene expression, GUS expression, IAA, IAA3, indole-3-acetic acid, mutants, shy2-1.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Auxin, typified by indole-3-acetic acid (IAA), is a plant hormone that affects many physiological phenomena in plants (Thimann, 1977). Auxin causes dramatic changes in the pattern of expression of a number of genes and is involved in switching gene cascades on and off (Theologis, 1986; Abel and Theologis, 1996). Aux/IAA genes are primary auxin-response genes, which are transiently expressed within minutes of auxin application (Abel et al., 1995; Abel and Theologis, 1996). Products of Aux/IAA genes are short-lived nuclear-localized proteins containing four conserved domains designated domain I, II, III and IV, respectively (Abel et al., 1994; Abel and Theologis, 1995). Aux/IAA proteins form homo-dimers as well as hetero-dimers with other Aux/IAAs and auxin response factors (ARFs) (Kim et al., 1997; Ulmasov et al., 1997a), which are specific DNA binding proteins that bind to synthetic auxin-responsive elements (Ulmasov et al., 1997a). ARFs have a conserved N-terminal DNA binding domain and a C-terminal domain that is homologous to domains III and IV of Aux/IAAs (Ulmasov et al., 1997a, 1999b). Domains III and IV are involved in dimerization among Aux/IAAs and ARFs and are required for stable binding of ARFs to auxin-responsive elements (AuxREs) (Kim et al., 1997; Ulmasov et al., 1999b). Over-expression of Aux/IAA proteins in carrot protoplasts specifically represses the expression of the genes whose promoters contain AuxREs (Ulmasov et al., 1997b). In similar experiments, over-expression of ARFs activates and represses the transcription of reporter genes under the control of AuxRE (Ulmasov et al., 1999a). Thus, combinational interaction among Aux/IAAs and ARFs may regulate the expression of early auxin genes including feedback regulation of Aux/IAA genes themselves, and various late genes.
A semi-dominant mutant suppressor of hy2 (shy2-1D) of Arabidopsis thaliana was originally isolated as a photomorphogenesis mutant by screening suppressor mutants of hy2 (Kim et al., 1996). The dark-grown shy2-1D mutant has short hypocotyls, shows cotyledon expansion, and forms leaves, inflorescence and flowers (Kim et al., 1996, 1998). In addition, light-induced CAB and PSBA genes are expressed in dark-grown shy2-1D seedlings (Kim et al., 1998). A detailed morphological analysis of shy2-1D and other shy2 mutants showed that the SHY2 gene is involved in auxin-dependent root growth, lateral root formation and gravitropism (Soh et al., 1999; Tian and Reed, 1999). Map-based cloning revealed that SHY2 is identical to IAA3, an early auxin gene that belongs to the Aux/IAA family (Soh et al., 1999; Tian and Reed, 1999). These findings suggest that IAA3/SHY2 functions not only as a regulatory component of photomorphogenesis but also as a mediator of the auxin signal.
As described above, Aux/IAAs regulate early auxin gene expression via interactions with ARFs. Thus, a mutation in IAA3/SHY2 may affect the expression of the IAA3/SHY2 gene itself and other early auxin genes. In this paper, we investigated the effect of IAA3/SHY2-1D on early auxin gene expression using RNA hybridization and histochemical analyses. We demonstrate the expression pattern of early auxin genes in the iaa3/shy2-1D mutant and discuss the possible role of IAA3/SHY2 on auxin-dependent early gene expression.
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MATERIALS AND METHODS |
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Plant growth conditions
The arabidopsis BA3 line (Oono et al., 1998) and the iaa3/shy2-1D mutant line (Kim et al., 1996) were used. For synchronous germination, seeds were imbibed in distilled water, kept at 4 °C for 2 d, and sowed on soil consisting of Metro-Mix® 350 (Scotts, Marysville, OH, USA), vermiculite and perlite in a ratio of 1 : 1 : 1. Plants were grown in a glasshouse for crossing and harvesting seeds. Surface-sterilized seeds were plated on germination media (GM) [0·5 x Murashige and Skoog salts (Giboco BRL, Gaithersburg, MD, USA), 10 % sucrose, 1 x B5 vitamins, and 500 µg ml–1 MES, pH 5·8] containing 0·8 % Bacto agar (Difco, Detroit, MI, USA). For a kanamycin test, 25 µg ml–1 kanamycin was added to the medium. Plates were kept in the dark for 2 d at 4 °C for synchronous germination and then transferred to 23 °C with white light (12 h light/12 h dark, 140 µmol m–2 s–1). Five-day-old seedlings grown vertically on GM containing 0·8 % agar were treated with GM with or without IAA at room temperature and subjected to a histochemical analysis of GUS expression and RNA hybridization analysis.
GUS reporter assay
Seedlings treated with or without IAA for 6 h were rinsed three times with staining buffer (100 mM sodium phosphate, pH 7·0, 10 mM EDTA, 0·5 mM K4Fe[CN]6, 0·5 mM K3Fe[CN]6 and 0·1 % Triton X-100), and incubated for 18 h in staining buffer containing 1 mM 5-bromo-4-chloro-3-indolyl ß-D-glucuronic acid (X-gluc). GUS staining patterns were observed using a Nikon SMZ-U or Leica MZFLIII dissecting microscope and recorded using a camera with positive film or an Olympus DP-50 digital camera. Images were processed with Adobe Photoshop 5·5.
RNA hybridization analysis
Total RNA was isolated from seedlings treated with or without IAA for 2 h following the procedure of Theologis et al. (1985), size-fractionated with a 1 % agarose gel containing formaldehyde and transferred onto a Nytran (Schleicher & Schuell, Dassel, Germany) membrane. Hybridization was performed by using 32P-labelled probes according to the manual provided by Schleicher & Schuell.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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mRNA expression of early auxin genes
To analyse the effects of the iaa3/shy2-1D mutation on the steady-state level of early auxin gene expression, total RNA was extracted from seedlings of wild type and iaa3/shy2-1D mutants of arabidopsis ecotype Landsberg, followed by RNA hybridization analysis using DNA fragments of early auxin genes as probes (Fig. 1). In the wild type, strong auxin induction of mRNA was observed in IAA1, IAA5 and SAUR-AC1, and relatively weak induction was observed in IAA3 and IAA4 mRNA. No significant change was observed in the presence or absence of auxin in GST5 mRNA. These results are consistent with previous results using the Columbia ecotype (Gil et al., 1994; Abel et al., 1995; Oono et al., 1998). The mRNA levels of auxin-induced genes IAA1, IAA3, IAA5 and SAUR-AC1 are strongly suppressed in the iaa3/shy2-1D mutant, compared with the wild type, while the suppression of IAA4 mRNA levels was weak. The GST5 gene, whose mRNA is not significantly increased by 20 µM IAA in the wild type, showed the same level of mRNA accumulation in the wild type and in the iaa3/shy2-1D mutant, suggesting that the suppression effect caused by the iaa3/shy2-1D mutation is specific to auxin-response genes. The relative level of suppression in auxin-response genes depends on each gene. IAA1 mRNA in the iaa3/shy2-1D mutant was induced with 20 µM IAA at the same level as in the wild type without IAA, while IAA3 and SAUR-AC1 mRNA in the iaa3/shy2-1D mutant was induced with 20 µM IAA at a lower level than in the wild type without IAA.
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Histochemical expression pattern of AuxRD-GUS
The arabidopsis line BA3 is a transgenic line with an introduced BA-GUS gene consisting of the A and B domains of the AuxRD in the PS-IAA4/5 promoter and GUS gene (Ballas et al., 1995; Oono et al., 1998). GUS expression is specifically induced in the root elongation zone after treatment of young seedlings with IAA (Oono et al., 1998). To investigate the effects of the IAA3/SHY2-1D mutation on BA-GUS expression, the BA-GUS gene was introduced into the iaa3/shy2-1D mutant by crossing the BA3 line with the iaa3/shy2-1D line. Because the genetic backgrounds of the BA3 line and iaa3/shy2-1D are the Columbia and Landsberg ecotypes, respectively, we analysed several F4 lines derived from one F3 line that is homozygous with respect to the BA-GUS transgene and heterozygous with respect to the iaa3/shy2-1D allele, to eliminate the effect of the genetic background. F5 seeds from individual F4 lines were harvested. The F5 seedlings were subsequently treated or not treated with 20 µM IAA, and GUS expression was observed in the root elongation zone. Results are summarized in Table 1 and are shown in Fig. 2. GUS expression was shown in the root elongation zone in all roots in the wild-type population, while almost no GUS expression was seen in the root elongation zone in the iaa3/shy2-1D homozygous population. Under higher magnification, we were able to detect weak GUS expression in the root vascular tissue of the iaa3/shy2-1D homozygous lines (data not shown). In the heterozygous population, both types of roots with and without GUS expression were detected. Approximately 75 % of the roots were GUS-stained. Unlike the wild-type homozygous population, the heterozygous population had many roots with weak GUS staining. Of 582 roots of F5 seedlings from 18 F4 heterozygous lines, 151 had strong GUS staining, 284 had weak GUS staining and 147 had no GUS staining, implying a 1 : 2 : 1 segregation (
2 = 0·391 < 20·05,2 = 5·99). These findings indicate that IAA-induced BA-GUS expression in the root elongation zone is suppressed in the iaa3/shy2-1D background. The weak GUS expression in heterozygous iaa3/shy2-1D plants suggests one-half of IAA3/SHY2-1D is insufficient to suppress completely IAA-induced BA-GUS expression. The dose responses of GUS expression in the wild type and the iaa3/shy2-1D mutant are shown in Fig. 3. In the wild type, BA-GUS expression in the root elongation zone is induced in the presence of IAA concentrations as low as 100 nM. This result is consistent with a previous experiment described by Oono et al. (1998). On the other hand, in iaa3/shy2-1D, BA-GUS expression in the root elongation zone was not detected in the presence of 100 nM IAA. Increasing the IAA concentration did not induce GUS expression in the root elongation zone in iaa3/shy2-1D mutants. GUS staining patterns in the aerial part of the seedlings are shown in Fig. 4. In WT/BA3, only weak GUS staining was detected in hypocotyl and cotyledon petioles in 5-day-old light-grown seedlings in the absence of auxin. Incubation with auxin for 6 h enhanced this GUS expression in both cotyledon petioles and hypocotyls. In the iaa3/shy2-1D mutants, strong GUS expression was observed even in the absence of IAA. Ectopic GUS expression in hypocotyls and cotyledon petioles as well as in root vascular tissue in the iaa3/shy2-1D mutants was enhanced slightly by incubating with 20 µM IAA.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Using RNA hybridization and histochemical analyses of the BA-GUS root tip system, we have shown that levels of expression of early auxin genes are reduced in iaa3/shy2-1D mutants compared with the wild type. In addition, BA-GUS in the iaa3/shy2-1D mutant is expressed ectopically in hypocotyls, cotyledon petioles and root vascular tissue.
In the RNA hybridization analysis, mRNA accumulation in the iaa3/shy2-1D mutant was still enhanced with IAA (see IAA1 in Fig. 1), while GUS accumulation in the root tip was not induced even by a high concentration of IAA (100 µM). This difference in auxin response could be due to different effects of IAA3/SHY2-1D on different tissues. The iaa3/shy2-1D mutation may completely suppress auxin-dependent expression in the elongation zone but only partly suppress it at the whole plant level. The difference in RNA hybridization and GUS staining may also be due to a difference in promoter activity between early auxin genes and BA-GUS.
We have previously shown that the pattern of expression of BA-GUS in auxin-resistant mutants can be classified into two groups (Oono et al., 1998). axr1-12, axr4-3 and aux1-7 mutants required 10- to 100-fold higher concentrations of auxin than the wild type to show GUS staining in the root elongation zone. On the other hand, axr2-1 and axr3-1 failed to show this cell-specific GUS staining in the root elongation zone even at the highest levels of auxin. The expression pattern of BA-GUS in iaa3/shy2-1D is very similar to that in the latter group. In particular, the dominant axr2-1 mutant was the most similar to the iaa3/shy2-1D mutant; the expression levels of Aux/IAAs and SAUR-AC1 were strongly suppressed in an RNA hybridization analysis (Gil et al., 1994; Timpte et al., 1994; Abel et al., 1995); BA-GUS expression in the root tip was not observed following treatment with 100 µM IAA; and ectopic expression in aerial parts as well as root vascular tissues was detected (Oono et al., 1998). In contrast, axr3, another dominant auxin-resistant mutant, showed no consistent differences in the accumulation of SAUR-AC1 transcript compared with wild-type plants, although ectopic expression of BA-GUS and SAUR-AC1-GUS was detected (Leyser et al., 1996; Oono et al., 1998). It is not known whether levels of expression of other early auxin genes are changed in axr3-1. Molecular cloning revealed that AXR2 and AXR3 genes are identical to IAA7 and IAA17, respectively, and that all the partially dominant mutants, iaa7/axr2-1, iaa17/axr3-1 and iaa3/shy2-1D are caused by point mutations that alter a conserved proline residue in domain II of Aux/IAA proteins (Rouse et al., 1998; Soh et al., 1999; Tian and Reed, 1999; Nagpal et al., 2000). It has been demonstrated that partially dominant mutations in domain II increase the stability of Aux/IAA proteins (Colon-Carmona et al., 2000; Worley et al., 2000). Thus, the low levels of early auxin gene mRNAs and no induction of BA-GUS in the root tip in iaa3/shy2-1D mutants suggest that IAA3/SHY2 and probably other Aux/IAAs act as negative factors for early auxin gene expression. This negative feedback regulation could lead to transient responses of most of the early auxin genes to exogenous auxin (Abel et al., 1995).
Tian and Reed (1999) reported that IAA3/SHY2 functions as both a negative and positive regulator of auxin responses based on detailed morphological observations of gain- and loss-of-function of iaa3/shy2 mutants. Our histochemical analysis also showed negative and positive effects of the IAA3/SHY2-1D mutation on BA-GUS expression; auxin-dependent expression of BA-GUS in the root elongation zone was suppressed while GUS was ectopically expressed in hypocotyls and root vascular tissue without auxin. This suggests that IAA3/SHY2-1D regulates the expression of early auxin genes not only negatively but also positively. We have previously observed a similar ectopic pattern of expression of BA-GUS in iaa7/axr2-1, iaa17/axr3-1, age1 and age2 (Oono et al., 1998). mRNA levels of early auxin genes in these mutants except age2 were lower than those in the wild type. Ectopic expression seems to be a common phenomenon when the normal regulation system of early auxin gene expression is disturbed. One possible explanation for ectopic expression is that wild-type IAA3/SHY2 acts positively in the tissues in which ectopic expression occurs. Increasing the stability of the IAA3/SHY2 protein by a mutation in domain II could cause BA-GUS expression in the absence of auxin. If this explanation is correct, mRNA expression of other early auxin genes should be increased in the iaa3/shy2-1D mutant because the mutated IAA3/SHY2 protein should also enhance expression of early auxin genes including the IAA3/SHY2 gene itself. Furthermore, the volume of tissues in which BA-GUS is ectopically expressed is larger than that where BA-GUS is suppressed. However, the high levels of mRNA expression of early auxin genes were not found in our RNA expression analysis. Another possible explanation is that increasing the stability of the IAA3/SHY2 protein in the iaa3/shy2-1D mutant suppresses expression of other Aux/IAAs whose products inhibit BA-GUS expression more effectively than IAA3/SHY2 in the tissue showing ectopic BA-GUS expression. Tissue-specific expression of Aux/IAA and ARFs has been reported in various experimental systems (Abel et al., 1995; Wong et al., 1996; Sessions et al., 1997; Dargeviciute et al., 1998; Hardtke and Berleth, 1998; Fujii et al., 2000; Nebenführ et al., 2000). Furthermore, Aux/IAAs interact with the same or another member of Aux/IAAs or ARFs with different affinities (Kim et al., 1997). Thus, it is possible that each member of the Aux/IAAs contributes differently, depending on the tissues, to regulate BA-GUS expression. The iaa7/axr2-1, iaa17/axr3-1 and iaa3/shy2-1D mutants, caused by similar mutations in different members of the Aux/IAA genes, exhibit distinct morphologies even though some morphological characters are common (Nagpal et al., 2000). The distinct morphology may result because each member of the Aux/IAA genes has a different effect on expression of downstream genes of Aux/IAA. Further analysis of the interaction between Aux/IAA, ARF and auxin-regulated promoters are needed to understand the molecular basis of the physiological role of each Aux/IAA protein.
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ACKNOWLEDGEMENTS |
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We thank Dr Hong Gil Nam (Pohang University of Science and Technology) for iaa3/shy2-1D seeds, Dr Nobuharu Fujii (Tohoku University) for critically reading the manuscript, and Dr Hiroshi Watanabe and members of the Department of Radiation Research for Environmental and Resources at JAERI for valuable help and discussions.
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