| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online August 26, 2005; 10.1104/pp.105.063495 Plant Physiology 139:192-203 (2005) © 2005 American Society of Plant Biologists Interaction of Auxin and ERECTA in Elaborating Arabidopsis Inflorescence Architecture Revealed by the Activation Tagging of a New Member of the YUCCA Family Putative Flavin Monooxygenases1Department of Biology, University of Washington, Seattle, Washington 98195–5325 (C.W., S.M.B., E.J.H., K.U.T.); Department of Biological Sciences, University of Tokyo, Hongo, Tokyo 113–0033, Japan (S.S.); and Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192–0397, Japan (T.K.)
The aboveground body of higher plants has a modular structure of repeating units, or phytomers. As such, the position, size, and shape of the individual phytomer dictate the plant architecture. The Arabidopsis (Arabidopsis thaliana) ERECTA (ER) gene regulates the inflorescence architecture by affecting elongation of the internode and pedicels, as well as the shape of lateral organs. A large-scale activation-tagging genetic screen was conducted in Arabidopsis to identify novel genes and pathways that interact with the ER locus. A dominant mutant, super1-D, was isolated as a nearly complete suppressor of a partial loss-of-function allele er-103. We found that SUPER1 encodes YUCCA5, a novel member of the YUCCA family of flavin monooxygenases. The activation tagging of YUCCA5 conferred increased levels of free indole acetic acid, increased auxin response, and mild phenotypic characteristics of auxin overproducers, such as elongated hypocotyls, epinastic cotyledons, and narrow leaves. Both genetic and cellular analyses indicate that auxin and the ER pathway regulate cell division and cell expansion in a largely independent but overlapping manner during elaboration of inflorescence architecture.
The aboveground body of higher plants is a consequence of the continual activity of the shoot apical meristem (SAM), which generates repeating units called phytomers. Each phytomer is composed of a node, stem (internode), leaf (lateral organ), and axillary bud, the latter of which allows branching. Modification of the position, size, and shape of the individual phytomer provides immense variations in plant architecture. Such diversity in plant architecture has significance in the domestication and breeding of crop plants. For instance, the maize (Zea mays) teosinte branched1 gene regulates branching pattern, and alteration in the teosinte branched1 expression level played a pivotal role in the domestication of maize (spp. mays) from its wild ancestor, Teosinte (maize spp. Parviglumis; Doebley et al., 1997  ). Another example is semidwarf varieties of cereals, in which reduction in the internode length has directly contributed to dramatic yield increase (Chrispeels and Sadava, 1994; Peng et al., 1999).
The model plant Arabidopsis (Arabidopsis thaliana) forms a typical rosette. During the vegetative stage, the Arabidopsis plant produces rosette leaves with no apparent internodal elongation. As the SAM acquires reproductive characteristics, the primary inflorescence stem elongates rapidly (bolting). First, the SAM gives rise to a shoot that has both vegetative and reproductive characteristics, including bracts (cauline leaves), axillary buds, and branches. Subsequently, the SAM generates multiple floral meristems, each of which differentiates a flower at the tip and a pedicel at the base, while the SAM itself maintains its indeterminate state (Schultz and Haughn, 1991
Molecular-genetic studies have highlighted the in vivo role of phytohormones and growth regulators for normal growth of the inflorescence. For instance, mutants defective in biosynthesis or signaling pathways of auxin, gibberellin, brassinosteroids, and sporamin conferred dwarfism due to reduced cell elongation and/or cell division in the internode (Feldmann et al., 1989
Loss-of-function mutations in the Arabidopsis ERECTA (ER) gene dramatically modify inflorescence architecture due to altered organ shape and internodal elongation pattern (Torii et al., 1996
ER exhibits strong genetic interactions with multiple phytohormone and growth regulatory pathways. For example, ER was identified as a strong suppressor of dwarfism caused by two gibberellin response mutants, gai and shi (Peng et al., 1997
To better understand how ER promotes inflorescence growth, it is necessary to identify genes that interact with the ER pathway. We initiated an activation-tagging screen to isolate dominant, extragenic suppressors of the er inflorescence phenotype using a partial loss-of-function allele er-103. The strategy is based on a random insertion of 4x cauliflower mosaic virus (CaMV) 35S enhancers that, if inserted in cis-regulatory elements, will lead to up-regulation of nearby open reading frames (Kakimoto, 1996
Isolation of suppressor of er1-Dominant as a Suppressor of er-103
To identify genes whose overexpression suppresses the er phenotype, a gain-of-function activation-tagging screen was performed using the intermediate allele er-103 (Torii et al., 1996
super1-D Suppresses Internodal and Pedicel Elongation Defects of er-103
We subsequently analyzed the morphological phenotype of super1-D er-103 during vegetative and reproductive development (Fig. 1). Unlike wild-type plants, er-103 plants develop a compact rosette leaf with a short petiole and round blade (Fig. 1, D and E; Torii et al., 1996 The inflorescence architecture of super-1D er-103 highly resembles that of the wild type. Flower buds of the wild type fold on to each other to cover the SAM, and older flowers have elongated pedicels (Fig. 1A). In contrast, the inflorescence tip of er-103 forms a characteristic disc-shaped, flat surface due to defective elongation of internodes and pedicels (Fig. 1B). super1-D suppressed the flower-clustered phenotype of er-103 (Fig. 1C). Furthermore, mature super1-D er-103 plants are as tall as wild-type plants (Fig. 1G), and elongation of er-103 pedicels is fully rescued by super1-D (Fig. 1H). In addition, super1-D conferred reduced fertility (data not shown). These results indicate that overexpression of SUPER1 by activation tagging suppresses stem and pedicel elongation defects of er but also confers additional developmental phenotypes, such as altered leaf shape and reduced fertility.
To understand the nature of genetic interaction, the super1-D mutation was subsequently introduced into wild-type ER and null er-105 allele backgrounds. It has been shown that the severity of er mutations directly reflects reduction in plant height, pedicel length, and fruit (silique) length in a quantitative manner (Torii et al., 1996
In contrast to stems and pedicels, er and super1-D exhibited distinct interaction in fruit development. While the wild-type ER allele suppressed the fertility defects of super1-D er-103, the null er-105 allele enhanced the fertility defect. Notably, super1-D er-105 plants produced short siliques that contain very few seeds (Fig. 2C and data not shown). Thus, a functional ER pathway is required for proper fruit development in the super1-D background. From these findings, we conclude that SUPER1 acts in pathways independent from ER, with possible interplay during the development of specific organs, such as the silique.
To gain insights into the molecular nature of the super1-D phenotype, we cloned the genomic DNA fragment flanking the right border of the T-DNA insertion (Fig. 3A). Sequencing analysis revealed that the CaMV35S 4x enhancer elements were inserted approximately 5.6 kb upstream of an open reading frame on Chromosome V (bacterial artificial chromosome F6B6). This corresponds to At5g43890/BAA98069, which encodes a 424-amino acid putative flavin-containing monooxygenase (Fig. 3A). It belongs to the YUCCA family genes implicated in biosynthesis of auxins, with BLAST scores of 1e-127, 1e-162, and 1e-128 to Arabidopsis YUCCA (At4g32540), YUCCA3 (At1g04610), and petunia (Petunia hybrida) FLOOZY (FLZ), respectively (Zhao et al., 2001
Overexpression of YUCCA5 Confers Suppression of the er-103 Phenotype To gain direct evidence that the suppression of the er-103 phenotype is due to YUCCA5 overexpression, the full-length cDNA of YUCCA5 was placed under the constitutive CaMV35S promoter and transformed into er-103 plants. As shown in Figure 4, the transgenic plants recapitulated the suppressed inflorescence phenotype of er-103. Furthermore, additional phenotypes, such as narrow leaf blades and reduced fertility, were also recapitulated (data not shown). From these results, we conclude that elevated expression of YUCCA5, a new member of the YUCCA family of putative flavin monooxygenases, confers all aspects of the super1-D phenotype.
YUCCA5 Is Normally Expressed in Roots and Young Vegetative Tissues We next investigated the expression levels of YUCCA5 in different organs by RT-PCR. YUCCA5 was predominantly expressed in roots and young vegetative tissues, while it was under detectable levels in reproductive tissues, such as inflorescence stems, pedicels, and floral buds (Fig. 5). Our result was consistent with the expression profiles of YUCCA5 obtained using the Arabidopsis full genome chip array (Affymetrix ATH1: analysis by AtGenExpress [http://web.uni-frankfurt.de/fb15/botanik/mcb/AFGN/atgenex.htm]; virtual northern analysis by Expression Angler [http://bbc.botany.utoronto.ca/ntools/cgi-bin/ntools_expression_angler.cgi]).
Overexpression of YUCCA5 by super1-D Results in Elevated Auxin Level and Response
It has been shown that elevated expression of YUCCA, YUCCA3, and FLZ results in overproduction of auxin, and that recombinant YUCCA protein can catalyze the rate-limiting step in Trp-dependent auxin biosynthesis (Zhao et al., 2001
To understand the relationship between elevated auxin levels and the suppressed er-103 inflorescence phenotype by super1-D, we sought to visualize cellular auxin distribution and response using genetic tools. For this purpose, we used a reporter construct that expresses the  -glucuronidase (GUS) gene under the 0.6-kb promoter of auxin-responsive gene AtAux2-11/IAA4 (Wyatt et al., 1993). This promoter can respond to a range of auxin concentration from 10–8 to 10–4 M (Wyatt et al., 1993). The well-known reporter construct, DR5::GUS (Ulmasov et al., 1997), did not drive strong GUS expression in the inflorescence and floral tissues; thus, it was not used in this study (data not shown). The super1-D mutation led to increased AtAux2-11::GUS activity both in seedlings and inflorescences. In seedlings, the elongation zone of hypocotyls and petioles, as well as developing leaves, showed extensive staining (Fig. 6B). Fully expanded cotyledons also displayed increased GUS activity. At the reproductive stage, inflorescence stems at the tip and elongating pedicels exhibited strong staining (Fig. 6B). GUS activity diminished in older pedicels and stems that are no longer elongating (Fig. 6B; data not shown). These results demonstrate that overexpression of YUCCA5 by super1-D leads to elevated levels of free auxin and, importantly, that increased auxin distribution and response in elongating regions of internodes and pedicels likely cause the suppressed er-103 phenotype.
While super1-D dramatically suppressed the elongation defects of er-103, the wild-type plants with additional super1-D mutation exhibited only a modest increase in inflorescence and pedicel elongation (Fig. 2). This is not due to reduction in YUCCA5 overexpression by outcrossing into wild-type plants, as YUCCA5 transcripts are equally up-regulated in the wild-type ER background (data not shown). One possibility is that er mutant plants may be defective in responding to normal levels of endogenous auxin to promote organ growth, but they can respond to increased auxin levels resulting from YUCCA5 overexpression. To test this hypothesis, we analyzed induction kinetics of Aux2-11::GUS by exogenous IAA in wild-type and er-103 plants. A 6-h incubation with IAA resulted in increased GUS activity both in wild-type and er-103 seedlings carrying Aux2-11::GUS (Fig. 7). While the GUS induction was most striking in the root tips, entire rosettes displayed some increase in the GUS staining (Fig. 7A and data not shown). However, we did not detect any clear difference in GUS induction levels between wild-type and er-103 seedlings, either by quantitative GUS activity assay or by GUS tissue staining. These results indicate that the er mutation does not significantly alter auxin response and further imply that suppression of the er phenotype by YUCCA5 involves interaction at downstream processes, such as cell proliferation and elongation.
super1-D Is Epistatic to er during Seedling Development and Confers Hypocotyl Cell Elongation
The activation-tagged allele of YUCCA was originally isolated from its seedling-long hypocotyls and epinastic cotyledons, both of which are characteristics of auxin overproduction (Zhao et al., 2001
We next analyzed the genetic interaction of er and super1-D during seedling development. We found that the null er-105 mutation resulted in a very subtle yet statistically significant reduction in hypocotyl length (P = 0.0013). Overexpression of YUCCA5 by the super1-D mutation led to elongated hypocotyls regardless of the presence or absence of er mutations (Fig. 8, A and B). Thus, with respect to the long hypocotyl phenotype, super1-D appears epistatic to er. The cellular basis of super1-D-mediated hypocotyl elongation was subsequently investigated. As shown in Figure 8C, both epidermal and cortex cell files show significant elongation under the super1-D background. The results indicate that super1-D confers a long hypocotyl phenotype by increasing cell elongation.
Unlike hypocotyl elongation, er and super1-D exhibited largely additive effects as well as complex interactions during internode and pedicel elongation, and this led to a complete rescue of er-103 inflorescence architecture (Figs. 1 and 2). To understand the cellular basis of the phenotypic rescue, we next examined the cellular phenotype of mature pedicels. It has been shown that the short pedicel phenotype of er-105 is due primarily to a reduced number of cortex cells, which are abnormally expanded (Shpak et al., 2003
In this study, we isolated a dominant suppressor of er by activation tagging and further identified that suppression of the er inflorescence phenotype was due to overexpression of YUCCA5, a previously undescribed member of the YUCCA family of putative flavin monooxygenases. Our findings highlight an intersection of auxin and ER-RLK signaling that is important for plant growth and elaboration of inflorescence architecture.
Among 10 Arabidopsis YUCCA family members, SUPER1/YUCCA5 belongs to a subfamily with two additional members, At1g04180 (AAC16744 and BAS3/At4g28720 (CAA22980. These subfamily members possess either no intron (YUCCA5 and BAS3) or one intron (At1g04180), as opposed to three introns in conserved locations in orthotypical YUCCA members (e.g. YUCCA2, THREAD/YUCCA4, and petunia FLZ; Tobeña-Santamaria et al., 2002
Although their IAA contents have not been quantified, the activation tagging/overexpression of other YUCCA members, namely YUCCA2, YUCCA3, and THREAD/YUCCA4 also conferred a signature phenotype of yucca: elongated hypocotyls, epinastic leaves, severely weak and lanky inflorescences, increased apical dominance, and reduced fertility (Zhao et al., 2001
The difference in the growth phenotype between super1-D and other YUCCA overexpressors may reflect redundant but distinct roles of each YUCCA member during plant growth and development. One possibility is that the activation-tagged YUCCA5 leads to a relatively moderate increase in free IAA amounts in the inflorescence. This may be because the YUCCA5 enzyme is not as active as the other members. Alternatively, the super1-D mutation may not drive high expression of YUCCA5 as compared to other activation-tagged YUCCA genes. In wild-type plants, YUCCA5 is predominantly expressed in young vegetative tissues and roots (Fig. 5). Further analysis to correlate tissue-specific accumulation of activation-tagged transcripts and IAA among different yucca family mutants will be necessary to clarify these two possibilities. The recently developed technique of microscale IAA quantification in tissue sections (Mori et al., 2005
It has been reported that loss-of-function mutations in YUCCA and YUCCA2 confer no visible phenotype, most likely due to redundancy (Zhao et al., 2001
While our screen did not identify novel ER-signaling components, it highlighted the intersection of ER- and auxin-mediated organ growth and internodal elongation, which in turn translates to inflorescence architecture. Previous studies have shown that both ER and auxin are required for elongation of the inflorescence and that they display synergism. For instance, a large-scale genetic screen for clustered, er-like inflorescence phenotype led to the isolation of 10 novel er-like1 mutants that are allelic to tir3 (Lease et al., 2001
The effects of super1-D in promoting elongation of inflorescences and pedicels, as well as reducing fertility, are more pronounced in er plants than in wild-type plants (see Fig. 2), implying that er plants may be more sensitive to elevated levels of auxin. The mechanism by which er mutation confers elevated response to auxin-mediated growth is not clear. It is highly unlikely that ER directly affects auxin biosynthesis or homeostasis for the following reasons: First, er mutations do not significantly alter the endogenous levels of free IAA (Fig. 4). Second, the er mutations do not affect expression of auxin-responsive promoter activity of AtAux2-11::GUS during vegetative and inflorescence development under normal growth condition (data not shown; Wyatt et al., 1993 The super1-D mutation conferred elongation of the epidermal pavement cells of both wild-type and er mutant pedicels to a similar extent (Fig. 9), while elongation of wild-type pedicels was not nearly as dramatic as er mutant pedicels (Fig. 2). This implies that it is not simply the extent of the epidermal cell elongation that specifies the overall elongation of pedicels as a whole. Unlike the epidermis, the cortex cell size was not altered by the super1-D mutation (Fig. 9). Therefore the sensitivity of er to super1-D may involve auxin-mediated cell proliferation.
Perhaps both auxin and ER promote inflorescence growth via largely independent pathways but with overlaps in their ultimate downstream processes (e.g. cell proliferation). Thus the excessive activity of either pathway may partly mask the loss of the other. Plant growth is under the control of both environmental stimuli and developmental programs. Multiple environmental and endogenous pathways may overlap or be redundant. Recently, the cross talk of hormone-signaling pathways has emerged as a central theme in plant growth regulation, as exemplified by the recent finding that interaction of auxin and brassinosteroids in promoting seedling growth occurs via transcriptional control of downstream targets (Goda et al., 2004
Plant Materials and Growth Conditions Arabidopsis (Arabidopsis thaliana ecotype Col) was used as the wild type. The yucca recapitulated line is a generous gift from Dr. Yunde Zhao (University of California at San Diego, La Jolla, CA) and Dr. Joanne Chory (Salk Institute, La Jolla, CA), and the AtAux2-11::GUS line is a generous gift from Dr. Masao Tasaka (NAIST, Ikoma, Japan). er-103, er-105, yucca, and AtAux2-11::GUS lines are all in the Col background. Plants were grown on soil mixtures (Sunshine Mix4:Vermiculite:Perlite = 2:1:1 with 0.85 mg/cm3 of Osmocoat14-14-14) under 18/6 light-dark cycle at 21°C. For plate cultures, seeds were surface sterilized with 30% bleach and 0.01% Triton X-100 (Sigma) for 12 min and subsequently washed five times with sterile distilled water. Seedlings were grown in Murashige and Skoog media supplemented with 1% (w/v) Suc.
The er-105 mutation was detected by using a primer pair ERg2248 (AAG AAG TCA TCT AAA GAT GTG A) and er-105rc (AGC TGA CTA TAC CCG ATA CTG A), and the absence of the wild-type allele was confirmed by a primer pair ERg2248 and ERg3016rc (AGA ATT TTC AGG TTT GGA ATC TGT). er-103 plants were genotyped using a primer pair ERg3588 (GAC TTG TCC TAC AAT CAG CTA ACT) and ERg4056rc (TAG ACC AGT CAG CTT GTT ACT GTG). The amplified fragment was subsequently digested with NlaIII to detect 3 cleaved amplified polymorphic sequences (CAPS): Bands obtained for wild type are 209 bp, 150 bp, 70 bp, and 65 bp; bands for er-103 are 274 bp, 150 bp, and 70 bp.
er-103 plants were vacuum infiltrated with the vector pSKI015 (a generous gift from Dr. Detlef Weigel; Weigel et al., 2000
The genomic DNA was isolated from 2-week-old super1-D plants using Nucleon Phytopure plant DNA extraction kit (Amersham Pharmacia LKB). The T-DNA flanking sequence of super1-D was recovered by the inverse-PCR (iPCR) as described by Li et al. (2001)
Total RNA was prepared by using an RNeasy mini kit (Qiagen) and subsequently treated with DNaseI (Invitrogen) prior to the RT-PCR reaction. cDNA was synthesized from 0.2 mg of the total RNA by using Thermoscript reverse transcriptase (Invitrogen) and a random hexiamer as a primer. One-fifth of the synthesized cDNA was used for the PCR reaction with a YUCCA5 gene-specific primer pair: May2FMO5 (cggaattccc ATG GAG AAC ATG TTT AGG CT) and May2FMO3rc (ccggatcc CTA AGC AAC TGA AAT GCA TC). The Arabidopsis actin (ACT2) gene was amplified as a template control using a primer pair: ACT2-1 (GCC ATC CAA GCT GTT CTC TC) and ACT2-2 (GCT CGT AGT CAA CAG CAA CAA).
The YUCCA5 cDNA was cloned into the EcoRI and BamHI sites of pSP73 (Promega) and the sequence was confirmed. The plasmid was partially digested with NcoI and BamHI and inserted into pRTL2-GUS to replace the GUS gene. This construct, which drives the YUCCA5 expression under a dual-enhanced CaMV35S promoter, was cloned into the HindIII site of pPZP222 (Hajdukiewics et al., 1994
Fixation, embedding, and sectioning of tissues for light microscopy using Olympus BX40 were performed as described by Shpak et al. (2003)
Two-week-old seedlings were transferred from plates to full-strength Murashige and Skoog liquid media and incubated for 5 d with shaking (100 rpm) at 18-h-light/6-h-dark condition. Seedlings were then treated with 0, 1, 10, or 100 µM IAA (Sigma) for 6 h with shaking. Subsequently, 150 to 200 mg of plant tissue was ground in liquid nitrogen and homogenized in 500 µL extraction buffer containing 50 mM sodium phosphate (pH 7.0), 10 mM EDTA, 0.1% sodium laurylsarcosine, 0.1% Triton X-100, and 10 mM
For gas chromatography, single-ion-monitoring mass spectrometry (GC-SIM-MS) analyses, fresh plant material (corresponding to a pool of 10 seedlings grown on agar plates for 7 d under continuous light) was carefully weighed, frozen in liquid nitrogen, and stored at –80°C. For extraction of free IAA, the material was ground in liquid nitrogen using a mortar and pestle. After addition of 0.6 ng of [13C6]IAA (Cambridge Isotope Lab) as an internal standard, the material was extracted in 80% acetone and 0.1 mg/mL 2,6-Di-tret.-butyl-4-methylphenol for 60 min. After centrifugation, the supernatant was collected. The pellet was reextracted again for 90 min, and the supernatant was brought to a water phase in a rotary evaporator. IAA was partially purified from the residual aqueous solution by partitioning using ether, and then purified by HPLC connecting with a fluorometer (Hitachi FL Detector L-7485; 280 nm excitation, 355 nm emmition). The HPLC was performed using a Nucleosil N(CH3)2 column (Senshu) with an isocratic system of 100% methanol and 0.03% acetic acid. The purified IAA fraction was dried under a nitrogen stream and trimethylsilylated with N-methyl-N-trimethylsilyltrifluoroacetamide at 60°C for 15 min. Splitless injections were made into a GC-single-ion-monitoring-MS system (QP5050A, Shimazu), equipped with a capillary column (DB-1, 0.25 mm i.d.x30 m, film thickness 0.25 mm; J&W Scientific). A linear temperature gradient was applied from 80°C to 280°C with an increase of 20°C/min. The injection temperature of the GC was 250°C, the ion source temperature of the MS was 250°C, and a helium flow of 1.2 mL/min was applied. The ionization potential was 70 electron volt, and the scan time was 0.2 s. The percentages of molecules of IAA labeled with 13C were calculated from the relative intensities of m/z 202 to 208 and 319 to 325 ions after subtraction of background. Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requestor. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number DQ159070.
We thank Dr. Detlef Weigel for a generous gift of pSKI015 plasmid, Drs. Yunde Zhao and Joanne Chory for yucca seeds, Dr. Masao Tasaka for AtAux2-11::GUS seeds, and Drs. Robert Cleland, Elena Shpak, Jessica McAbee, and Lynn Pillitteri for commenting on the manuscript. We are thankful to Kensuke Yamazaki for his help on GC-MS analysis of IAA, May Chen-Lee and Maria Malzone for technical assistance in mutant screen and plasmid rescue, and Drs. Lynn Riddiford, Jay Hesselberth, and Bruce Godfrey for letting us use their equipment (a differential interference contrast microscope and a microplate reader). Received March 30, 2005; returned for revision June 14, 2005; accepted June 14, 2005.
1 This work was supported by the Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, and the U.S. Department of Energy (grant no. DE–FG02–03ER15448 to K.U.T.), and by Grants-in-Aid from the Ministry of Education, Science, Sport and Culture of Japan (grant no. 15031222 to T.K.). K.U.T. was a University of Washington ADVANCE Professor (National Science Foundation/ADVANCE Cooperative Agreement no. SBE–0123552). 
2 These authors contributed equally to the paper. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.063495. * Corresponding author; e-mail ktorii{at}u.washington.edu; fax 206–685–1728.
Abel S, Oeller PW, Theologis A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci USA 91: 326–330
Azpiroz R, Wu Y, LoCascio JC, Feldmann KA (1998) An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10: 219–230 Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8: 394–401[CrossRef][ISI][Medline] Chrispeels MJ, Sadava DE (1994) Plants, Genes, and Agriculture. Jones and Bartlett, Boston, pp 298–327
Diévart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131: 251–261 Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 485–488[CrossRef][Medline]
Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14: 547–558
Feldmann KA, Marks MD, Christianson ML, Quatrono RS (1989) A dwarf mutant of Arabidopsis generated by T-DNA insertion. Science 243: 1351–1354
Fridborg I, Kuusk S, Robertson M, Sundberg E (2001) The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley. Plant Physiol 127: 937–948
Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 15: 1985–1997
Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134: 1555–1573 Hajdukiewics P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25: 989–994[CrossRef][ISI][Medline] Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19: 4248–4256[CrossRef][ISI][Medline]
Hedden P, Proebsting WM (1999) Genetic analysis of gibberellin biosynthesis. Plant Physiol 119: 365–370
Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274: 982–985 Kanyuka K, Praekelt U, Franklin KA, Billingham OE, Hooley R, Whitelam GC, Halliday KJ (2003) Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J 35: 57–70[CrossRef][ISI][Medline] Komeda Y, Takahashi T, Hanzawa Y (1998) Development of inflorescneces in Arabidopsis thaliana. J Plant Res 111: 283–288[CrossRef]
Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein beta subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631–2641 Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161–164[CrossRef][Medline] Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938[CrossRef][ISI][Medline]
Li J, Lease KA, Tax FE, Walker JC (2001) BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 5916–5921 Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272: 398–401[Abstract]
Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071–1080
Marsch-Martinez N, Greco R, Van Arkel G, Herrera-Estrella L, Pereira A (2002) Activation tagging using the En-I maize transposon system in Arabidopsis. Plant Physiol 129: 1544–1556 Matsubayashi Y, Yang H, Sakagami Y (2001) Peptide signals and their receptors in higher plants. Trends Plant Sci 6: 573–577[CrossRef][ISI][Medline]
Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17: 2088–2093 Mori Y, Nishimura T, Koshiba T (2005) Vigorous synthesis of indole-3-acetic acid in the apical very tip leads to a constant basipetal flow of the hormone in maize coleoptile. Plant Science 168: 467–473[CrossRef] Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2: E258[CrossRef][Medline] Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell Suppl 14: S61–S80
Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11: 3194–3205 Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, et al (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400: 256–261[CrossRef][Medline] Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9: 745–757[Abstract] Ryan C, Pearce G, Scheer JM, Moura DS (2002) Polypeptide hormones. Plant Cell (Suppl) 14: S251–S264
Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3: 771–781 Sessions A, Weigel D, Yanofsky MF (1999) The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J 20: 259–263[CrossRef][ISI][Medline]
Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131: 1491–1501
Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15: 1095–1110
Soga K, Wakabayashi K, Hoson T, Kamisaka S (2000) Flower stalk segments of Arabidopsis thaliana ecotype Columbia lack the capacity to grow in response to exogenously applied auxin. Plant Cell Physiol 41: 1327–1333
Tobeña-Santamaria R, Bliek M, Ljung K, Sandberg G, Mol JNM, Souer E, Koes R (2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. Genes Dev 16: 753–763 Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234: 1–46[ISI][Medline] Torii KU, Hanson LA, Josefsson CAB, Shpak ED (2003) Regulation of inflorescence architecture and organ shape by the ERECTA gene in Arabidopsis. In T Sekimura, ed, Morphogenesis and Patterning in Biological Systems. Springer-Verlag, Tokyo, pp 153–164 Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746[Abstract] Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963–1971[Abstract] Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2: 505–513[CrossRef][ISI][Medline] Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380–383[CrossRef][Medline]
Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrandiz C, Kardailsky I, Malancharuvil EJ, Neff MM, et al (2000) Activation tagging in Arabidopsis. Plant Physiol 122: 1003–1013 Wyatt RE, Ainley WM, Nagao RT, Conner TW, Key JL (1993) Expression of the Arabidopsis AtAux2-11 auxin-responsive gene in transgenic plants. Plant Mol Biol 22: 731–749[CrossRef][ISI][Medline]
Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291: 306–309 This article has been cited by other articles:
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
TOP
ABSTRACT
RESULTS
