| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online April 13, 2005; 10.1105/tpc.105.030981 © 2005 American Society of Plant Biologists
Crown rootless1, Which Is Essential for Crown Root Formation in Rice, Is a Target of an AUXIN RESPONSE FACTOR in Auxin Signaling
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
; Casson and Lindsey, 2003; Schiefelbein, 2003). However, only a small number of mutants have been found in monocots, and no genes corresponding to these mutants have been identified.
The endogenous phytohormone auxin is essential for root development. Exogenous treatment with auxin induces the ectopic formation of lateral and adventitious roots, although the optimal auxin concentration for inducing ectopic formation differs between lateral and adventitious roots (Schiefelbein, 2003). It has also been reported that genes involved in the auxin signaling pathway function in root development. Gain-of-function mutants of Arabidopsis AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) genes, which encode negative regulators of auxin signaling, produce phenotypes with reduced or no lateral roots (Reed, 2001; Marchant et al., 2002). AUX/IAA proteins regulate gene expression by interacting with AUXIN RESPONSE FACTOR (ARF) proteins, which function as positive regulators of auxin signaling (Reed, 2001). The loss-of-function mutant of Arabidopsis ARF8 showed increased lateral root formation, and overexpression of ARF8 in transgenic Arabidopsis inhibited lateral root formation (Tian et al., 2004). Based on this evidence, the important role that auxin plays in root development is apparent; however, the targets and molecular mechanisms downstream of AUX/IAA and ARF proteins in root development are still unresolved.
To study the mechanism of root formation, we previously isolated a rice crown rootless1 (crl1) mutant that was defective in the formation of crown roots (Inukai et al., 2001). Because crl1 shows severe defects in crown root formation as well as a reduced number of lateral roots on seminal roots, we suspected that Crl1 is involved in auxin-related root formation. In this work, we isolated the Crl1 gene and characterized its biological function in terms of auxin signaling. Crl1 encodes an ASYMMETRIC LEAVES2 (AS2)/LATERAL ORGAN BOUNDARIES (LOB) domain transcription factor, which has not previously been reported as modulating root development. We also showed that auxin and an AUX/IAA protein tightly regulate Crl1 expression and that Crl1 is a direct target of an ARF protein in rice (Oryza sativa). Thus, these findings have important implications for our understanding of the function of auxin in root development.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
70% of that in the wild type (Figures 1A and 1B), indicating that Crl1 is involved in both crown root and lateral root formation. At later stages of development, crl1 occasionally produced crown roots (Figures 1E and 1F). Given adequate supplies of water and fertilizer, the aboveground tissues and organs of crl1 grew normally and did not differ significantly from the wild type morphologically, even at harvest (Figures 1G and 1H). This indicates that Crl1 is specifically involved in root formation but not in shoot development.
|
|
|
in Figure 2B). Approximately 80% of wild-type roots had root tip angles of 61 to 80°, and no plants had an angle of <40°; by contrast, 60% of crl1 roots had angles of <40° (Figure 2C). Therefore, the gravitropic response was also impaired in crl1.
|
6 kb apart (Figure 3A). This region includes two predicted open reading frames (ORFs). By comparing the nucleotide sequences of crl1 and the wild type, we concluded that Crl1 has an ORF that encodes a protein of 259 amino acid residues in two exons (Figure 4A). There was a single nucleotide substitution in crl1 that produced a single amino acid change, whereas no mutation was detected in the other ORF. Complementation analysis based on introduction of a 4.6-kb genomic DNA fragment containing the entire candidate gene confirmed that the crl1 phenotype is caused by a loss-of-function mutation in this predicted Crl1 gene (Figure 3B).
|
|
100 amino acid residues (Iwakawa et al., 2002; Shuai et al., 2002). The AS2/LOB domain of Crl1 shared the conserved amino acid residues of Arabidopsis AS2/LOB proteins (i.e., CX2CX6CX3C at the N terminus [C-motif] and a GAS region at the C terminus [GAS-motif]). We performed a BLAST search using the AS2/LOB domain sequence of Crl1 and found that some AS2/LOB proteins in Arabidopsis, maize (Zea mays), and rice are more similar to Crl1 than to other AS2/LOB proteins (Figure 4C). It is interesting that AS2-LIKE18/LOB DOMAIN16 (ASL18/LBD16) and ASL16/LBD29, which are classified in the same group with Crl1, are specifically expressed in the roots of Arabidopsis (Shuai et al., 2002), suggesting that the members in this group are involved in root formation or development, as is the case with Crl1.
Analysis of Crl1 Expression
We examined the expression of Crl1 in various organs. Because no band was detected on RNA gel blots, we performed semiquantitative RT-PCR analysis to estimate Crl1 transcript levels (Figure 5A). High levels of Crl1 transcripts accumulated in unelongating basal internodes. Crl1 was moderately expressed in roots and flowers but not in other organs. In rice, root formation occurs not only in basal internodes and roots but also at the base of spikelets (flowers of rice) when grown under stress conditions (Takeoka and Shimizu, 1974); consequently, all organs expressing Crl1 have the ability to form roots, whereas organs without Crl1 expression do not.
|
; Figures 5I and 5J). In the initial stage of primordium formation, GUS staining was observed in the pericycle cells (Figures 5I and 5J), and then it gradually disappeared in the developed primordium (Figures 5G and 5H). The localized expression of Crl1 in stems and roots corresponds well to the areas of crown and lateral root initiation, confirming that Crl1 is involved in the initiation of these root systems.
Auxin Signaling Regulates Crl1 Expression
We examined the effect of auxin on Crl1 expression using semiquantitative RT-PCR. The expression of Crl1 was induced within 1 h and increased dramatically until 3 h after IAA treatment, after which it gradually decreased (Figure 6A). We also observed the expression of OsIAA4, which is a member of the early auxin response AUX/IAA family in rice (I. Umemura and M. Matsuoka, unpublished results). The induction profile of OsIAA4 was similar to that of Crl1 (Figure 6A). The early auxin response of Crl1 expression suggests that Crl1 is a member of the early auxin response family. Therefore, we examined the effect of the protein synthesis inhibitor cycloheximide (CHX) on the auxin-dependent induction of Crl1 and OsIAA4 (Figure 6B). As expected, the auxin-dependent induction of OsIAA4 was not inhibited by CHX, and slight expression was induced by CHX alone, as with Arabidopsis AUX/IAA genes (Abel et al., 1995). A similar induction profile was observed in the case of Crl1, strongly suggesting that de novo protein synthesis is not required for Crl1 induction by auxin.
|
). This promoter was also used as a marker to visualize the in vivo distribution of auxin in rice (Scarpella et al., 2003). The GUS staining controlled by the DR5 promoter was broadly observed in the outer parenchyma cells of the peripheral vascular cylinder in the stem (Figure 6D), including where Crl1 was expressed (Figures 5D and 6C). This confirms that the Crl1 expression colocalizes with auxin distribution in vivo.
Recent studies have revealed that auxin signaling is regulated by the auxin-stimulated degradation of a family of negative regulators called AUX/IAA proteins (Gray et al., 2001; Tiwari et al., 2001; Zenser et al., 2001). These negative regulator proteins interact with another large family of plant-specific transcription factors called ARF proteins, which are positive transcriptional regulators in auxin signaling (Hagen and Guilfoyle, 2002). Because RT-PCR and GUS analyses indicated that the expression of Crl1 is under control of auxin (Figures 6A to 6D), we analyzed whether Crl1 expression depends on the degradation of AUX/IAA proteins.
To produce constitutively active rice AUX/IAA protein, we mutagenized the conserved Pro of OsIAA3, which is located in the degradation-related domain (domain II), to Leu (Figure 6E). Because the mutagenesis of OsIAA3 caused the constitutive suppression of auxin signaling, transformed calli rarely formed regenerated seedlings. To alleviate this problem, we used a steroid hormone-inducible system to control the suppressive function of the mutagenized OsIAA3 on treatment with the steroid hormone dexamethasone (DEX). We generated >20 transgenic plants expressing a fusion protein of OsIAA3P58L and the steroid hormone binding domain of the glucocorticoid receptor (GR). Few of the transgenic plants showed abnormalities without DEX treatment, whereas they showed diverse auxin-related abnormalities, including defects in root formation and stunted seedlings, with DEX treatment (our unpublished results). Using these transgenic plants, we examined the AUX/IAA-dependent expression of Crl1 with or without DEX treatment. We used two independent lines, which showed severely or mildly altered phenotypes when treated with DEX. As mentioned above, Crl1 expression was clearly induced by IAA treatment (cf. IAA– DEX– and IAA+ DEX– in Figure 6F). However, the induction by auxin was almost completely inhibited by DEX treatment in line 1 (the severe phenotype) and strongly inhibited in line 2 (the intermediate phenotype) (IAA+ DEX+ in Figure 6F). These results demonstrate that the degradation of AUX/IAA proteins is essential for the auxin-dependent expression of Crl1 and strongly suggest that Crl1 expression is positively regulated by ARF proteins.
ARF Protein Binds to the Auxin Response Element in the 5' Flanking Sequences of Crl1
The auxin response element (AuxRE) containing the TGTCTC motif has been identified in the promoters of some early auxin response genes, and ARFs bind AuxRE to regulate the transcription of these genes (Hagen and Guilfoyle, 2002). Because Crl1 contains two TGTCTC motifs (AuxRE1 and AuxRE2 with its inverted sequence, GAGACA) in its promoter region (Figure 7A), we wondered whether ARFs interact with these sequences. To examine this possibility, we performed an electrophoresis mobility shift assay. The recombinant rice ARF protein (OsARF1; Waller et al., 2002) expressed in Escherichia coli bound to fragment 3 containing AuxRE2. This resulted in a band with lower mobility than that of the free fragment, whereas the other fragments, including fragment 1 containing AuxRE1, were not shifted (Figure 7B). The binding of OsARF1 with fragment 3 did not occur when one nucleotide of the AuxRE2 sequence was changed (fragment M3), demonstrating that the interaction between fragment 3 and OsARF1 depends on AuxRE2.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
Crl1 encodes a member of the plant-specific AS2/LOB protein family. There are 43 genes for AS2/LOB proteins in the Arabidopsis genome (Shuai et al., 2002), and one of them, AS2, is required for the formation of symmetric leaves (Iwakawa et al., 2002). However, there is no information about the biochemical activity of AS2/LOB domain proteins. Recently, Zgurski et al. (2005) reported that an asymmetric auxin response precedes asymmetric cell division patterns and leaf expansion in as2. Treatment of as2 leaves with either exogenous auxin or an auxin transport inhibitor eliminates the asymmetric auxin response and the subsequent asymmetric leaf development. This result suggests that AS2 functions in regulating the symmetric auxin response in Arabidopsis leaves. As discussed below, however, we believe that Crl1 is specifically involved in AUX/IAA auxin signaling in root development and that Crl1-like AS2/LOB proteins, such as Crl1, ASL18/LBD16, and ASL16/LBD29, may belong to a new small protein family, which specifically functions in auxin-regulated root development. Consistent with this hypothesis, the expression of both ASL18/LBD16 and ASL16/LBD29 was induced by auxin, and their auxin-dependent induction was severely impaired in T-DNA insertion lines for ARF genes of Arabidopsis (Okushima et al., 2005).
The pattern of Crl1 expression was similar to the pattern of GUS expression driven by the DR5 promoter, and Crl1 expression was upregulated by auxin without the de novo synthesis of any other proteins. Moreover, the constitutive activation of an AUX/IAA protein in transgenic rice disturbed the induction of Crl1 expression by auxin treatment. Recent molecular genetic studies have demonstrated that AUX/IAAs play a central role in auxin signaling (Hagen and Guilfoyle, 2002; Liscum and Reed, 2002). AUX/IAAs function as negative regulators in auxin signaling by direct interaction to prevent the functions of ARFs (Ulmasov et al., 1997; Tiwari et al., 2001, 2003). Auxin treatment promotes the degradation of AUX/IAAs by enhancing the interaction with an SCFTIR complex to release the prevented ARF function (Gray et al., 2001). These observations and our results strongly suggest that Crl1 is a direct target of ARF. Indeed, Crl1 contains two putative AuxREs in its promoter region, and the proximal AuxRE specifically interacts with rice ARF and acts as a cis-motif for Crl1 expression in rice.
The control of AUX/IAAs by the auxin signaling pathway regulates a wide variety of plant growth and developmental processes. For example, mutations in AXR3/IAA17 result in diverse auxin-related phenotypes, including reduced root elongation, increased adventitious root formation, and a lack of root gravitropism (Leyser et al., 1996; Rouse et al., 1998). The SLR/IAA14 and IAA28 gain-of-function mutations confer severe defects in lateral root formation (Rogg et al., 2001; Fukaki et al., 2002). The AUX/IAA-controlling pathway also regulates the expression of a variety of genes. The most thoroughly studied of these are members of the AUX/IAA, GH3, and SAUR gene families, which are early auxin response genes (Hagen and Guilfoyle, 2002). Although the biological function of the SAUR genes remains unclear, AUX/IAAs function as mediators in auxin responses, as mentioned above, and GH3s function in auxin homeostasis by producing amino acid conjugates of IAA (Staswick et al., 2005). However, there has been no evidence that these early auxin response genes are directly involved in auxin-related phenotypes, such as root formation, root elongation, and root gravitropism (i.e., there has been no direct link between the AUX/IAA-controlling signal pathway and auxin-regulated phenotypes).
In this study, we demonstrated that Crl1 functions as a mediator linking the control of AUX/IAAs by auxin to the initiation of crown and lateral root development. In our model of Crl1 function in root development (Figure 8), auxin triggers the degradation of AUX/IAAs, which interact with ARFs. The released ARFs interact with the AuxRE in the Crl1 promoter to trigger its transcription in the crown and lateral root initiation areas, resulting in root initiation. Crl1 expression is insufficient to initiate crown or lateral roots because the ectopic expression of Crl1 by the constitutive rice Actin1 promoter did not induce any ectopic roots in transgenic rice (our unpublished results). This indicates that there is another factor(s) essential for crown and lateral root formation in addition to Crl1. Further studies are needed to understand how Crl1 functions and what factors mediate the signal after Crl1 to initiate root formation.
|
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
). To investigate the effects of auxin on root growth and development, seeds of the wild type and crl1 were sown on agar medium containing various concentrations of IAA, 2,4-D, and NAA (Sigma-Aldrich, St. Louis, MO).
Molecular Cloning, Sequence Alignment, and Phylogenetic Tree Construction
To map Crl1, linkage analysis was performed using an F2 population of 2500 plants derived from the cross between crl1 (japonica variety) and Kasalath (indica variety). A BLAST search was performed, as previously reported (Sakamoto et al., 2004). The predicted protein sequences were initially clustered using ClustalW (Thompson et al., 1994; see Supplemental Figure 1 online). TreeView was used to generate the graphical output (Page, 1996). The numbers at the branching points indicate the percentage of times that each branch topology was found during bootstrap analysis (n = 1000).
Expression Analysis
Semiquantitative RT-PCR was performed with DNase-treated total RNA using the Omniscript reverse transcription kit (Qiagen, Valencia, CA). The PCR (30 cycles) was performed essentially as described by the manufacturer. The primer sequences were 5'-AGCAACGTGTCCAAGCTGCT-3' and 5'-GTCCTGGTGGTGTATCCCTT-3' for Crl1 and 5'-GGCATTCCCGGTGCCCATGA-3' and 5'-GTCCATCGCCTATGGTGCGAC-3' for OsIAA4. These primers specifically amplified the target gene sequences (data not shown). To examine the effect of exogenous auxin treatment on Crl1 and OsIAA4 expression, roots of wild-type or transgenic seedlings were submerged in a solution of 1 µM IAA. For inhibition of protein synthesis, seedlings were first soaked in a solution of 10 µM CHX (Sigma-Aldrich) and then incubated for 3 h in a solution containing 10 µM CHX and 1 µM IAA, or 10 µM CHX and ethanol as a control. To induce the function of constitutive active OsIAA3, roots of transgenic seedlings were submerged for 3 h in a solution of 1 µM IAA with or without 10 µM DEX (Sigma-Aldrich).
Plasmid Constructs and Plant Transformation
For complementation of the crl1 mutation, the wild-type genomic sequence from –2581 to +1969 (taking the translation initiation site as +1) was amplified by PCR and cloned into pBI121. For the Crl1 promoter-GUS construct, the wild-type genomic sequence from –2581 to +518 was amplified by PCR and introduced in front of the GUS reporter gene of pBI-Hm (kindly provided by Kenzo Nakamura, Nagoya University, Nagoya, Japan) to produce a fusion with the GUS reporter gene. The DR5 promoter-GUS construct was generated as reported previously (Scarpella et al., 2003). Nucleotide substitutions in the Crl1 promoter and OsIAA3 cDNA were introduced by PCR as previously reported (Sakamoto et al., 1999). To create the OsIAA3P58L:GR fusion protein, the stop codon of mutated OsIAA3 was replaced with a SmaI site by PCR and introduced in front of the steroid binding domain of the human GR as previously reported (Sakamoto et al., 2001). OsIAA3P58L:GR was then cloned between the rice actin1 promoter and the nopaline synthase polyadenylation signal of the hygromycin-resistant binary vector pAct-Hm. This vector is modified from pBI-Hm (Ohta et al., 1990) and contains a rice actin1 promoter. The resulting fusion construct was introduced into Agrobacterium tumefaciens strain EHA101 by electroporation. Agrobacterium-mediated transformation of rice was performed as described previously (Hiei et al., 1994). Transgenic plants were selected on media containing 50 mg L–1 hygromycin, and we analyzed 30, 20, and 25 transformants carrying Crl1, DR5, and the mutated Crl1 promoter-GUS construct, respectively.
Electrophoresis Mobility Shift Assay
To produce a recombinant OsARF1 protein, the full-length OsARF1 cDNA was inserted in the sense orientation as a translational fusion into the pET-32a expression vector (Novagen, Madison, WI) and expressed in BL21 (DE3) Escherichia coli cells (Stratagene, La Jolla, CA). The Crl1 promoter fragments (350 bp) were labeled with [32P]dATP using the Klenow fragment and purified on Sephadex G-50 columns. DNA binding reactions were performed as previously reported (Sakamoto et al., 2001).
Sequence data for the AS2/LOB genes have been deposited with the EMBL/GenBank data libraries under the following accession numbers: ASL4/LOB, AF447897; AS2/LBD6, AF447887; ASL18/LBD16, AF447890; ASL20/LBD18, AF447891; ASL23/LBD19, AF432232; ASL3/LBD25, AF447892; ASL16/LBD29, AF447893; Crl1, AB200234; OsCrll1, AB200235; OsCrll2, AB200236; OsCrll3, AB200237; OsCrll4, AB200238; ZmCrll1, BG873644; ZmCrll2, BE050765.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Makoto Matsuoka (makoto{at}nuagr1.agr.nagoya-u.ac.jp).
Online version contains Web-only data.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.105.030981.
Received January 19, 2005; accepted March 17, 2005.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
|---|
Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P., Sandberg, G., and Bennett, M.J. (2003). Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165–171.[CrossRef][Web of Science][Medline]
Casson, S.A., and Lindsey, K. (2003). Genes and signaling in root development. New Phytol. 158, 11–38.[CrossRef]
Fukaki, H., Tameda, S., Masuda, H., and Tasaka, M. (2002). Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153–168.[CrossRef][Web of Science][Medline]
Gray, W.M., Kepinski, S., Rouse, D., Leyser, O., and Estelle, M. (2001). Auxin regulates SCFTIR1-dependent degradation of Aux/IAA proteins. Nature 414, 271–276.[CrossRef][Medline]
Hagen, G., and Guilfoyle, T. (2002). Auxin-responsive gene expression: Genes, promoters and regulatory factors. Plant Mol. Biol. 46, 373–385.
Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of boundaries of the T-DNA. Plant J. 6, 271–282.[CrossRef][Web of Science][Medline]
Inukai, Y., Miwa, M., Nagato, Y., Kitano, H., and Yamauchi, A. (2001). Characterization of rice mutants deficient in the formation of crown roots. Breed. Sci. 51, 123–129.[CrossRef]
Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S., Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C., and Machida, Y. (2002). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 43, 467–478.
Kawata, S., and Shibayama, H. (1965). On the lateral root primordia formation in the crown roots of rice plants. Proc. Crop Sci. Soc. Jpn. 33, 423–431.
Leyser, H.M.O., Pickett, F.B., Dharmasiri, S., and Estelle, M. (1996). Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J. 10, 403–413.[CrossRef][Web of Science][Medline]
Liscum, E., and Reed, J.W. (2002). Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387–400.[CrossRef][Web of Science][Medline]
Marchant, A., Bhalerao, R., Casimiroc, I., Eklöf, J., Caseroc, P.J., Bennetta, M., and Sandberg, G. (2002). AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14, 589–597.
Ohta, S., Mita, S., Hattori, T., and Nakamura, K. (1990). Construction and expression in tobacco of a ß-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol. 31, 805–813.
Okushima, Y., et al. (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell 17, 444–463.
Page, R.D. (1996). TreeView: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358.
Reed, J.W. (2001). Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420–425.[CrossRef][Web of Science][Medline]
Rogg, L.E., Lasswell, J., and Bartel, B. (2001). A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13, 465–480.
Rouse, D., Mackay, P., Stirnberg, P., Estelle, M., and Leyser, O. (1998). Changes in auxin response from mutations in an AUX/IAA gene. Science 279, 1371–1373.
Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., and Scheres, B. (1999). An auxin-dependent distal organizer of pattern and polarity in the root. Cell 99, 463–472.[CrossRef][Web of Science][Medline]
Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S., and Matsuoka, M. (2001). KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 15, 581–590.
Sakamoto, T., et al. (2004). An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134, 1642–1653.
Sakamoto, T., Nishimura, A., Tamaoki, M., Kuba, M., Tanaka, H., Iwahori, S., and Matsuoka, M. (1999). The conserved KNOX domain mediates specificity of tobacco KNOTTED1-type homeodomain proteins. Plant Cell 11, 1419–1431.
Scarpella, E., Rueb, S., and Meijer, A.H. (2003). The RADICLELESS1 gene is required for vascular pattern formation in rice. Development 130, 645–658.
Schiefelbein, J.W. (2003). Cell-fate specification in the epidermis: A common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74–78.[CrossRef][Web of Science][Medline]
Shuai, B., Reynaga-Peña, C.G., and Springer, P.S. (2002). The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol. 129, 747–761.
Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M., Maldonado, M.C., and Suza, W. (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17, 616–627.
Takeoka, Y., and Shimizu, M. (1974). Vegetative proliferations of floral spikelets in Oryza sativa L. III. The external morphology of the proliferation in the spikelets of a mutant strain induced by the treatment of ethylene imine. Proc. Crop. Sci. Soc. Jpn. 43, 252–260.
Tian, C.E., Muto, H., Higuchi, K., Matamura, T., Tatematsu, K., Koshiba, T., and Yamamoto, K.T. (2004). Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J. 40, 333–343.[CrossRef][Web of Science][Medline]
Tiwari, S.B., Hagen, G., and Guilfoyle, T.J. (2003). The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15, 533–543.
Tiwari, S.B., Wang, X.-J., Hagen, G., and Guilfoyle, T.J. (2001). Aux/IAA proteins are active repressors and their stability and activity are modulated by auxin. Plant Cell 13, 2809–2822.
Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.
Ulmasov, T., Murfett, J., Hagen, F., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971.[Abstract]
Waller, F., Furuya, M., and Nick, P. (2002). OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol. Biol. 50, 415–425.[CrossRef][Web of Science][Medline]
Zenser, N., Ellsmore, A., Leasure, C., and Callis, J. (2001). Auxin modulates the degradation rate of Aux/IAA proteins. Proc. Natl. Acad. Sci. USA 98, 11795–11800.
Zgurski, J.M., Sharma, R., Bolokoski, D.A., and Schultz, E.A. (2005). Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves. Plant Cell 17, 77–92.
Related articles in Plant Cell:
This article has been cited by other articles:
|
|
 |
|
  D. Albinsky, M. Kusano, M. Higuchi, N. Hayashi, M. Kobayashi, A. Fukushima, M. Mori, T. Ichikawa, K. Matsui, H. Kuroda, et al. Metabolomic Screening Applied to Rice FOX Arabidopsis Lines Leads to the Identification of a Gene-Changing Nitrogen Metabolism Mol Plant, January 1, 2010; 3(1): 125 - 142. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. W. Lee, N. Y. Kim, D. J. Lee, and J. Kim LBD18/ASL20 Regulates Lateral Root Formation in Combination with LBD16/ASL18 Downstream of ARF7 and ARF19 in Arabidopsis Plant Physiology, November 1, 2009; 151(3): 1377 - 1389. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. J. Donner, I. Sherr, and E. Scarpella Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves Development, October 1, 2009; 136(19): 3235 - 3246. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Gutierrez, J. D. Bussell, D. I. Pacurar, J. Schwambach, M. Pacurar, and C. Bellini Phenotypic Plasticity of Adventitious Rooting in Arabidopsis Is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance PLANT CELL, October 1, 2009; 21(10): 3119 - 3132. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Zhao, Y. Hu, M. Dai, L. Huang, and D.-X. Zhou The WUSCHEL-Related Homeobox Gene WOX11 Is Required to Activate Shoot-Borne Crown Root Development in Rice PLANT CELL, March 1, 2009; 21(3): 736 - 748. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Soyano, S. Thitamadee, Y. Machida, and N.-H. Chua ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 Regulate Tracheary Element Differentiation in Arabidopsis PLANT CELL, December 1, 2008; 20(12): 3359 - 3373. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-F. Lo, S.-Y. Yang, K.-T. Chen, Y.-I. Hsing, J. A.D. Zeevaart, L.-J. Chen, and S.-M. Yu A Novel Class of Gibberellin 2-Oxidases Control Semidwarfism, Tillering, and Root Development in Rice PLANT CELL, October 1, 2008; 20(10): 2603 - 2618. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Lau, G. Jurgens, and I. De Smet The Evolving Complexity of the Auxin Pathway PLANT CELL, July 1, 2008; 20(7): 1738 - 1746. [Full Text] [PDF]
|
|
|
|
 |
|
 A. Husbands, E. M. Bell, B. Shuai, H. M.S. Smith, and P. S. Springer LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins Nucleic Acids Res., October 8, 2007; 35(19): 6663 - 6671. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Morita and J. Kyozuka Characterization of OsPID, the Rice Ortholog of PINOID, and its Possible Involvement in the Control of Polar Auxin Transport Plant Cell Physiol., March 1, 2007; 48(3): 540 - 549. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Okushima, H. Fukaki, M. Onoda, A. Theologis, and M. Tasaka ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis PLANT CELL, January 1, 2007; 19(1): 118 - 130. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Bortiri, G. Chuck, E. Vollbrecht, T. Rocheford, R. Martienssen, and S. Hake ramosa2 Encodes a LATERAL ORGAN BOUNDARY Domain Protein That Determines the Fate of Stem Cells in Branch Meristems of Maize PLANT CELL, March 1, 2006; 18(3): 574 - 585. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Woll, L. A. Borsuk, H. Stransky, D. Nettleton, P. S. Schnable, and F. Hochholdinger Isolation, Characterization, and Pericycle-Specific Transcriptome Analyses of the Novel Maize Lateral and Seminal Root Initiation Mutant rum1 Plant Physiology, November 1, 2005; 139(3): 1255 - 1267. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Xu, L. Zhu, H. Shou, and P. Wu A PIN1 Family Gene, OsPIN1, involved in Auxin-dependent Adventitious Root Emergence and Tillering in Rice Plant Cell Physiol., October 1, 2005; 46(10): 1674 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. A. Eckardt MicroRNAs Regulate Auxin Homeostasis and Plant Development PLANT CELL, May 1, 2005; 17(5): 1335 - 1338. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | THE PLANT CELL | PLANT PHYSIOLOGY | |
|---|---|---|---|
