Auxin binding protein: curiouser and curiouser
Post on 11-Feb-2017
TRENDS in Plant Science Vol.6 No.12 December 2001http://plants.trends.com 1360-1385/01/$ see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(01)02150-1586 ReviewReviewCandace TimpteDept Biological Sciences,University of NewOrleans, New Orleans,LA 70148, USA.e-mail: email@example.comCuriouser and curiouser! cried Alice. (As her bodygrew after swallowing a potion, she realized that sheshould give her now-distant feet a new pair of bootsfor Christmas). Alice went on planning to herself howshe would manage it. They must go by the carrier,she thought; and how funny it will seem, sendingpresents to ones own feet! And how odd thedirections will look!Through the Looking Glass (Lewis Carrol)The plant hormone auxin (indole-3-acetic acid, orIAA) is central to diverse plant growth anddevelopmental responses. Some of the best-characterized examples are tropic growth responses(such as to gravity or light), stem elongation, lateralbranching of roots and shoots, and vasculardevelopment1. These whole-plant responses are theresult of changes at the cellular level that includeelongation, division or differentiation. However, themechanisms of auxin perception and response areunderstood poorly. Some responses are rapid andothers occur after a lag period, complicating thesituation further.The first step in a classic hormone responsepathway is a receptor binding a hormone. Manyinvestigators have sought auxin receptors and severalgood candidates have been isolated2. However, as wellas binding auxin, the receptor must also transduce theauxin stimulus into the known responses. Collectingevidence that the auxinreceptor interaction causesdirect changes in the cell has been difficult. Theimmediate short-term auxin responses includechanges in protoplast electrophysiology, guard-cellgating and early-response-gene induction. Longer-term responses include cell elongation, cell divisionand phenotypic changes in the whole plant. The choiceof assay is the key to establishing an auxinreceptorinteraction; one must remember that more than onepathway might be activated by one receptor, anddirect cause-and-effect relations must be established.Auxin-binding proteinTwenty years ago, an auxin-binding activity waspurified from maize coleoptiles by several groups2,3.This auxin-binding protein, ABP1, was shownby photoaffinity labeling to bind auxin4 (itscharacterization is summarized in Ref. 2). The maizeABP1 cDNA encodes a 201 amino acid protein, with a38 residue signal sequence. The unglycosylatedprotein is 20 kDa, whereas the mature protein is22 kDa, containing a high-mannose-typeoligosaccharide2. ABP1 was the first plant proteindiscovered with a C-terminal KDEL sequence, whichis an endoplasmic reticulum (ER) retention signal5.ABP1 has no hydrophobic regions. Thus, to functionas a receptor, it probably associates with amembrane-bound dockingprotein. ABP1 bears noresemblance to well-known hormone receptors fromanimal systems and does not have substantialsimilarity to any mammalian gene. Yet, ABP1 hasbeen identified from many plant species includingmaize, Arabidopsis, tobacco and radish2.In spite of excellent research efforts, importantquestions need to be answered if ABP1 is to beestablished as the auxin receptor. First, does ABP1ligand binding have biological relevance? The auxinreceptor must bind auxin but also must evokechanges in the cell. Second, what is the structure ofthis protein, and how does this structure relate to itssignaling mechanism? Third, where does ABP1reside in the cell? Typically, a mammalian hormonebinds the target ligand at the plasma membrane,although one exception is the steroid hormonereceptor. Paradoxically, the KDEL sequence of ABP1suggests an ER, not a plasma membrane, location.Could it be elsewhere in the cell?ABP1 is crucial for embryogenesisRecent genetic studies provide strong evidence forABP1 mediating responses leading to cell elongationand embryogenesis. Arabidopsis has a single geneencoding ABP1 (Ref. 6) and disruption of this gene isexpected to affect auxin signaling processes and toreveal ABP1s role in plant development. A knockoutplant harboring a T-DNA insertion in the first exon ofthe ABP1 gene has been identified7. Homozygousindividuals were not recovered from this plant line,strongly indicating that disruption of the ABP1 geneis lethal. About 25% of the seeds in transgenic siliqueswere white and nonviable, clear evidence ofsegregation of a lethal homozygous phenotype.Auxin is implicated in a variety of plant developmental processes, yet themolecular mechanism of auxin response remains largely unknown. Auxinbinding protein 1 (ABP1) mediates cell expansion and might be involved in cellcycle control. Structural modeling shows that it is a -barrel dimer, with theC terminus free to interact with other proteins. We do not know where ABP1performs its receptor function. Most ABP1 is detected within the endoplasmicreticulum but the evidence indicates that it functions at the plasma membrane.ABP1 is established as a crucial component of auxin signaling, but its precisemechanism remains unclear.Auxin binding protein: curiouser andcuriouserCandace TimpteAddition of a transgenic, functional copy of ABP1rescued the embryonic-lethal phenotype, suggestingthat normal embryo development requires at leastone copy of ABP1.Examination of the nonviable embryos revealedthat ABP1 is required early in plant development:embryos arrested after the globular stage. Newlyformed cross walls between cells were wronglyoriented and cells failed to elongate, leading toembryo death7. These results provide direct evidencethat ABP1 plays a crucial role in embryonicmorphogenesis. Whether the role is in cell elongation,embryo polarity establishment or individual cellpolarity could not be determined. To address thepolarity versus elongation issue, antisensesuppression was used to create an ABP1 loss-of-function mutation in the BY-2 tobacco cell line. Theresults enabled the two types of expansion commonlyobserved in cultured plant cells to be differentiated8.Auxin-induced elongation to increase cell volumebeyond that of the divided cell was abolished in thesetransgenic cells7. However, cell expansion to replacecell volume following division was not affected in theABP1-antisense lines. Thus, elongation growth is thecrucial auxin response in cultured cells and failure toelongate is the probable cause of embryo lethality inthe transgenic knockout plants.ABP1 mediates cell expansionThe complementary approach, overproducing ABP1,confirms the role of ABP1 in auxin-mediated cellexpansion. Tobacco was transformed with ABP1under the control of an inducible promoter9. In controlplants, auxin only induced growth at the leaf tips,whereas, in overproducing transgenic plants, itinduced growth throughout the leaf. Regions that arenot normally auxin responsive acquired induciblegrowth that was strictly dependent on the presenceof auxin; a structurally similar inactive auxin did notstimulate growth. Thus, overproducing ABP1extended the range of auxin sensitivity in matureleaf tissue9. A meticulous analysis of individual cellsfrom ABP1-overproducing plants reveals thatauxin-inducible cell expansion is a component ofthis growth10. The abundance of ABP1 in each cellcorrelates with the extent of auxin-induced cellexpansion and with cell size in transgenic plants.Evidence from cultured cells supports a role forABP1 in cell expansion. Cultured maize cellsoverproducing ABP1 expanded in an auxin-dependent fashion and were greater in volume thancontrol cells9. Antisense-suppressed ABP1 tobaccoBY-2 cells had undetectable levels of ABP1 proteinand lacked auxin-induced cell expansion whencompared with wild-type cells10.Auxin-induced cell division might involve ABP1Auxin-mediated growth might also have a divisioncomponent. Cells from ABP1-overproducing tobaccoleaves were examined for nuclear division stage10.The proportion of nuclei in G2 stage was double thatof the wild type. By sequential analysis of cells indeveloping leaves, cell expansion was found toprecede the G2 advance in the cycle. The prematureG2 advance is probably an indirect effect of theincreased cell volume of transgenic plants10.A conditional ABP1 knockout mutation has been constructed by producing a transgenic ABP1 antibody in the tobacco BY2 cell line(C. Perrot-Rechenmann, pers. commun.). Thistransgenic antibody presumably binds ABP1in planta and limits its activity within the cell.These knockout cells showed no significant change incell volume but arrested at the G1 phase of the cellcycle. Thus, ABP1 might play a crucial role in theregulation G1 and G2/M phases of the cell cycle.Although the conclusions from these twotransgenic studies differ, the results indicate acrucial role for ABP1 in plant cells. Furthermore,either knocking out or overproducing ABP1 providescrucial evidence that ABP1 mediates perception ofauxin in cultured cells and that disruption of thissignal causes changes in the cell cycle.ABP1 triggers a plasma membrane electrical responseHyperpolarization of the cell membrane occurswithin minutes after applying biologically activeauxin, providing a convenient assay for evaluatingauxin response at the outer face of the plasmamembrane. ABP1 has been implicated in thisresponse in many studies11. Synthetic peptidescorresponding to the C terminus of ABP1 were testedin the hyperpolarization assay12,13 (Table 1). PeptidePz152-163 is a maize-derived sequence. Two othersare tobacco-derived peptides: the first, Nt-C15, ismost similar to the wild-type sequence whereas thesecond, Nt-C12, lacks three conserved residues.The maize and Nt-C15 peptides all inducehyperpolarization, much as auxin does when appliedto tobacco protoplasts. The truncated Nt-C12 peptidefails to induce the hyperpolarization response. Thisstudy confirms previous results that exogenouspeptides derived from ABP1 can elicit an electricalresponse. These results confirm that the homologoussystem is more efficient than the heterologoussystem, because peptides and membranes werederived from the same species13.TRENDS in Plant Science Vol.6 No.12 December 2001http://plants.trends.com587ReviewReviewTable 1. C-terminal sequences tested for hyperpolarizationPeptide Sequence Hyperpolarization?Consensus WDE.C......KEDL Not knownMaize ABP1 WDEDCFEAA..KDEL YesNicotiana tabacum ABP1 WDEECYQTTSWKDEL YesPz152163 .DEDCFEAA..KDEL YesNt-C15 WDEECYQTTSWKDEL YesNt-C12 ..ECYQTTSW.KDEL NoMutation targets WDEECYQTTSWKDELa NoDeletion WDEECYQTTSW.... NoaText in bold indicates target residues for mutation.The C-terminal charged residues in ABP1 weremutagenized and the entire protein was tested in thehyperpolarization assay14. The charged residues weremutated to the cognate amine residues, singly andpaired, and a KDEL deletion mutant protein wasconstructed (Table 1). The KDEL deletion evoked thesame hyperpolarization response as the wild type whenapplied to cells. None of the charge-substituted mutantproteins evoked a hyperpolarization response14. Thus,the substitution of charged residues causes ABP1 tofail to interact with the plasma membrane proteinthat affects hyperpolarization, implicating achargecharge interaction between the proteins.Alternatively, the mutated ABP1 might simply misfoldand fail to interact with the plasma membrane protein.The electrical response of plant cells was affected byantibodies directed against ABP1. Several monoclonalantibodies induce hyperpolarization in tobacco cellprotoplasts and act as auxin agonists13. Three othermonoclonal antibodies act as antagonists and blockauxin action, either by recognizing the auxin-bindingsite as the epitope13 or by immobilizing ABP1 in a non-functional conformation. Similarly, antibodies affectedorchid cell stomatal opening. Both the D16 monoclonalantibody, raised against the putative auxin bindingsite of ABP1 (Ref. 15), and a monoclonal antibodyagainst an ABP1 peptide, induced stomatal openingand acidification, similar to the effects of auxin16. Amonoclonal antibody that targets the C terminus ofABP1 and the peptide Pz152-163 stimulated stomatalclosure and increased pH, similar to the mode ofabscisic acid. A Pz152-163 peptide lacking the KDELsequence had no effect. This result is curious becauseother data suggests that the KDEL is not requiredfor hyperpolarization stimulation. However, smallchanges in a peptide can cause great changes inpeptide structure. These immunological resultsindicate that ABP1 transduces the auxin signal tothe plasma membrane to effect hyperpolarization,perhaps by interacting with another protein.The amount of ABP1 might be tightly regulatedin the cell. As the evidence above indicates,increased production of ABP1 enhances auxinsensitivity9,10,17,18. Examination at the molecular levelreveals that transgenic overexpression of wild-typeABP1 generated a ~100-fold increase in expression byRNA blotting but only a 30% increase in detectableprotein by immunoblotting18. In antisense transgenicplants, maximal inhibition of ABP1 protein wasmerely 50%, indicating that complete inhibition ofABP1 might be detrimental to the plant18.Structure of ABP1The three-dimensional structure of ABP1 could giveclues about the mechanism of signaling or potentialproteinprotein interactions. The first model for theauxin-binding site of ABP1 was based on thestructure and interaction of 45 different auxinanalogs19. This model proposed a planar, indole ring-binding platform, a charged carboxylic acid-bindingsite and a hydrophobic transition region. Byphotoaffinity labeling with azido IAA (Ref. 20) andimmunology21, two regions were implicated in auxinbinding. Structure mapping studies using a panel ofmonoclonal antibodies further defined the identityof residues forming the auxin-binding platform andthe carboxylic acid-binding site13.-Barrel dimerComparisons of amino acid sequences show that thereare several highly conserved residues between auxinbinding proteins in monocots and dicots2,22. Anaugmented model has been proposed based on theseand additional comparisons with the cupin and vicilinsuperfamily of proteins23. The structural basis of thismodel relies on conserved residues corresponding to-barrel turn anchors in the germin protein structure24.The proposed structure is a -barrel homodimer,containing -sheets and no -helix, consistent withcircular dichroism spectra25, and resembles thepseudodimer symmetry of a vicilin monomer23.Recently, ABP1 was crystallized, and X-ray diffractionanalysis to 1.9 resolution shows two glycosylatedhomodimers in asymmetric units26. These crystalstructure data are consistent with a -barrel (Fig. 1).This level of resolution cannot confirm the auxin-binding site. A conserved region might be analogous tothe metal-binding site of oxalate oxidase23 and thusindicate that ABP1 has some unknown enzymefunction. This speculation is intriguing, because noenzymatic activity has been reported for ABP1.Mobile C-terminusExperimental evidence suggests that binding auxincauses a conformational change involving theC-terminus27. Interference mapping studies suggestthat the C-terminus interacts with the auxin-bindingsite, perhaps through disulfide bonds13. Twoantibodies map to overlapping ABP1 regions but haveopposite electrochemical effects, one agonistic and theother antagonistic to auxin action14. In the presence ofauxin, binding by one agonist antibody is completelyabolished and the other antibody has a weakerinteraction with ABP1 (Ref. 14). This result suggestsTRENDS in Plant Science Vol.6 No.12 December 2001http://plants.trends.com588 ReviewReviewTRENDS in Plant Science N-termN-termC-termC-termFig. 1. Conceptual modelof ABP1. ABP1 is a -barrelstructure modeled onsimilarity with cupinfamilies and concavalin Afor dimerization. ResidueW44 (red) and the clusterof residues forming theputative metal-bindingsite (blue) might form theplatform for auxin binding.The purple ribbonindicates conserved-turn anchor residues.Abbreviations: C-term,C-terminal; N-term,N-terminal.that ABP1 undergoes a distinct conformationalchange when auxin is bound, changing the epitope.Circular dichroism data indicate a conformationalchange upon auxin binding25. Although theC-terminus did not have sufficient similarity to thevicilin superfamily to model its location, a C-terminaltryptophan or WDE sequence might occupy thebinding pocket in the absence of auxin23. Theexperimental evidence presented above supportsthe importance of the conserved WDE residues.Conformational changes upon auxin binding mightrelease the C-terminus for signal propagation andinteraction with other proteins.Localization versus site of action remains perplexingThe KDEL sequence of ABP1 appears to be effectiveat localizing ABP1 to the endoplasmic reticulum (ER).Paradoxically, the evidence indicates that ABP1 bindsauxin with low affinity at the pH of the ER (Ref. 28).However, numerous visualization techniques showthat most, but not all, ABP1 is localized to the ER, notthe plasma membrane. ABP1 has been visualized atthe plasma membrane of maize cultured cells byusing immunogold labeling29. ABP1 has also beendetected throughout the Golgi and has been secretedinto culture medium29. A small population of ABP1molecules has been detected at the plasma membraneof maize coleoptile protoplasts using silver-enhancedimmunogold epipolarization microscopy30. Thenumber of ABP1 molecules at the surface wasestimated to be as low as 1000, which represents onlya small proportion of total cellular ABP1. A smallnumber of cell surface receptors requires lesshormone to achieve half-maximal occupancy.Physiologically, this would allow the cell to besensitive to small amounts of hormone29.Because antibodies are unlikely to enter intactcells, the evidence that several antibodies trigger theplasma membrane hyperpolarization responseindicates that at least some portion of the ABP1 poolresides at the plasma membrane11,1416. Because theantibodies and peptides bind a protein in intactprotoplasts that affects membrane conductivity,logically they must bind ABP1 localized to theplasma membrane.The C-terminal KDEL sequence was changed toexamine its role in the localization of ABP1 (Ref. 17).KDEL was mutated to HDEL to enhance its retentionin the ER or mutated to either KDELGL or KEQL tocompromise its retention. As expected, the KDEL orHDEL proteins localized to the ER, whereas theKEQL and KDELGL proteins entered the Golgistacks. However, there was no difference in the cellsurface abundance of ABP1 in cells expressingmutant proteins as examined by electron microscopyor silver-enhanced immunogold epipolarizationmicroscopy17. Thus, even without the KDELsequence, quantities of ABP1 do not localizemassively to the plasma membrane.Similar results confirming the major ERlocalization were obtained by analysis of maizecoleoptile rolled leaves31. Neither immunofluorescencenor immunogold labeling detected ABP1 at theplasma membrane. Double-labeling experiments todetect conformational changes that might sequesterthe KDEL and allow transit to the plasmamembrane were negative. Under conditions ofauxin binding, ABP1 remained in the ER (Ref. 31).Carbohydrate analysis further confirmed the ERlocalization of ABP1. The ABP1 oligosaccharidesare high mannose types, not the more complexcarbohydrates expected if ABP1 traversed theGolgi stacks. Less than 2% of ABP, by glycananalysis, escaped the ER retention system31. At thislow level of escape, a special mechanism to avoidER retention need not be invoked. Bulk flow orassociation with other proteins might be sufficientto allow this tiny amount of ABP1 to escape to theplasma membrane.The mechanism of KDEL-mediated ER retentionand retrieval operates efficiently, such that analternative delivery mechanism to the vacuole wasproposed32. A KDEL terminus was attached to aprotein not normally localized to the ER. Thisconstruct circumvented the Golgi to reach thevacuole. Some such alternate mechanism mightoperate for ABP1. Because overproduction of ABP1increases the sensitivity of cells to auxin, thepresence of ABP1 at the plasma membrane might betightly regulated.Never-ending story of auxin signalingABP1 fits the criteria for a hormone receptor. Ampleevidence indicates that ABP1 mediates auxins effectson normal plant development. However, themolecular mechanism of ABP1 remains at best askeletal model (Fig. 2). To reconcile the diverse effectsof auxin, two sites of ABP1 activity are proposed.TRENDS in Plant Science Vol.6 No.12 December 2001http://plants.trends.com589ReviewReviewTRENDS in Plant Science GolgiERDockingproteinABP1IonchannelHyperpolarizationVesicles to PMCell wallPlasma membraneFig. 2. Model of ABP1localization and action.Most ABP1 resides in theendoplasmic reticulum(ER) but it is alsodetectable in the Golgiand associated with theplasma membrane (PM).ABP1 probably associateswith a transmembranedocking protein topropagate the auxinsignal to the interior of thecell, or it could interactdirectly with ion channels.A conformational changeis induced upon auxinbinding. At the plasmamembrane, auxin bindingeffects a hyperpolarizationevent, which also can bestimulated by ABP1-derived peptides. Becausethe ER does not providethe optimum pH for auxinbinding, auxin-boundABP1 in the Golgi mightdirect vesicle traffic of cellwall materials forexpansion.TRENDS in Plant Science Vol.6 No.12 December 2001http://plants.trends.com590 ReviewBinding at higher or lower concentrations of auxinmight temper the response. Although ABP1 has nohydrophobic regions, the auxin-binding signal mustbe transmitted to the cell. To this end, ABP1 mightinteract with a plasma membrane docking protein(yet to be identified)3,33 or might interact directlywith the ion channel. Auxin binding induces aconformational change in ABP1, enabling interactionwith the docking protein, or alters the ABP1docking-protein complex to transmit the signal. The dockingprotein might be abundant at the plasma membrane;excess docking protein would then be available tointeract with exogenously provided ABP1 orpeptides in assays, and to mediate membranehyperpolarization. Similarly, ER or Golgi-localizedABP1 might interact with a transmembrane proteinto regulate the secretion of cell wall components tomediate cell expansion.Auxin-induced conformational changes in ABP1might alter interactions with other membraneproteins, perhaps heterotrimeric G-proteins. Auxinis known to induce the transcription of severalauxin-regulated genes that are repressed by theactivation of a specific MAPK cascade34.Furthermore, Arabidopsis cells overproducing theplant heterotrimeric G protein mimic the auxin-induced increase in cell division35. These resultssuggest that the auxin signaling pathway mightinvolve the G protein to regulate cell cycle control.However, given the varied plant responses to auxin,there might be more than one type of auxinreceptor in the cell.It has not been possible to cover all aspects ofauxin signaling in this article. The importance ofABP1 in plant development is certain but morepieces of the puzzle remain to be identified. Refiningthe location and site of action of ABP1 might requirethe use of non-plant in vivo systems, such as thepreviously used COS cells28. The proposed dockingprotein or other proteins that interact with ABP1must be identified. Plant development, as theultimate result of cell division and cell elongation, isaffected by numerous hormone signals. Themechanism of integration of these signals andexactly where ABP1 fits into signaling cross-talkremain to be discovered.ReviewReferences1 Davies, P.J., ed. (1995) Plant Hormones:Physiology, Biochemistry and Molecular Biology,Kluwer Academic Publishers2 Jones, A.M. (1994) Auxin-binding proteins. Annu.Rev. Plant Physiol. 45, 3934203 Klambt, D. (1990) A view about the function ofauxin-binding proteins at plasma membranes.Plant Mol. Biol. 14, 104510504 Jones, A.M. and Venis, M. (1989) Photoaffinitylabeling of indole-3-acetic acid binding proteinsin maize. Proc. Natl. Acad. Sci. U. S. A.86, 615361565 Pelham, H.R.B. (1988) Evidence that luminal ERproteins are sorted from secreted proteins in apost-ER compartment. EMBO J. 7, 9139186 Palme, K. et al. (1992) Molecular analysis of anauxin binding protein gene located on chromosome4 of Arabidopsis. Plant Cell 4, 1932017 Chen, J-G. et al. (2001) ABP1 is required fororganized cell elongation and division inArabidopsis embryogenesis. Genes Dev.15, 9029118 Hasezawa, S. and Syono, K. (1983) Hormonalcontrol of elongation of tobacco cells derived fromprotoplasts. Plant Cell Physiol. 24, 1271329 Jones, A.M. et al. (1998) Auxin-dependent cellexpansion mediated by overexpressed auxin-binding protein 1. Science 282, 1114111710 Chen, J-G. et al. The role of auxin-bindingprotein I in the cell expansion of tobacco leaf cells.Plant J. (in press)11 Barbier-Brygoo, H. (1995) Tracking auxinreceptors using functional approaches. Crit. Rev.Plant. Sci. 14, 12512 Leblanc, N. et al. (1999) The auxin-bindingprotein Nt-Erabp1 alone activates an auxin-liketransduction pathway. FEBS Lett. 449, 576013 Leblanc, N. et al. (1999) A novel immunologicalapproach establishes that the auxin bindingprotein Nt-abp1 is an element involved in auxinsignaling at the plasma membrane. J. Biol. Chem.274, 283142832014 David, K. et al. (2001) Conformational dynamicsunderlie the activity of the auxin binding protein,Nt-ABP1. J. Biol. Chem. 276, 345173452315 Venis, M.A. et al. (1992) Antibodies to a peptidefrom the maize auxin-binding protein have auxinagonist activity. Proc. Natl. Acad. Sci. U. S. A.89, 7208721216 Gehring, C.A. et al. (1998) Auxin binding proteinantibodies and peptides influence stomatalopening and alter cytoplasmic pH. Planta205, 58158617 Bauly, J.M. et al. (2000) Overexpression ofauxin binding protein enhances the sensitivityof guard cells to auxin. Plant Physiol.124, 1229123818 Shimomura, S. et al. (1999) Characterization ofauxin-binding protein 1 from tobacco: content,localization and auxin-binding activity. Planta209, 11812519 Edgerton, M.D. et al. (1994) Modeling the auxinbinding site of auxin binding protein 1 of maize.Phytochemistry 35, 1111112320 Brown, J.C. and Jones, A.M. (1994) Mapping theauxin-binding site of auxin-binding protein 1.J. Biol. Chem. 269, 211352114021 Napier, R.M. and Venis, M.A. (1990) Monoclonalantibodies detect an auxin-inducedconformational change in the maize auxin-binding protein. Planta 182, 31331822 Anai, T. et al. (1997) Comparison of ABP1primary sequences from monocotyledonous anddicotyledonous species. J. Plant Physiol.151, 44644923 Warwicker, J. (2001) Modeling of auxin-bindingprotein 1 suggests that its C-terminus and auxincould compete for a binding site that incorporatesa metal ion and tryptophan residue 44. Planta212, 34334724 Dunwell, J.M. et al. (2000) Microbial relatives of the seed storage protein of higher plants:conservation of structure and diversification offunction during evolution of the cupinsuperfamily. Microbiol. Mol. Biol. Rev. 15317925 Shimomura, S. et al. (1986) Purification andproperties of an auxin-binding protein frommaize shoot membranes. J. Biochem.99, 1513152426 Woo, E-J. et al. (2000) Crystallization andpreliminary X-ray analysis of the auxinreceptor ABP1. Acta Crystallogr.D56, 1476147827 Walther, A. et al. (1997) Antibodies againstdistinct ABP1 regions modify auxin binding toABP1 and change the physiological auxinresponse of maize coleoptile sections. J. PlantPhysiol. 150, 11011428 Tian, H. et al. (1995) Auxin-binding protein 1 doesnot bind auxin within the endoplasmic reticulumdespite this being the predominant subcellularlocation for this hormone receptor. J. Biol. Chem.270, 269622696929 Jones, A.M. and Herman, E.M. (1993)KDEL-containing auxin binding protein issecreted to the plasma membrane and cell wall.Plant Physiol. 101, 59560630 Diekman, W. et al. (1995) Auxins induceclustering of the auxin-binding protein at thesurface of maize coleoptile protoplasts. Proc. Natl.Acad. Sci. U. S. A. 92, 3425342931 Henderson, J. et al. (1997) Retention of maizeauxin-binding protein in the endoplasmicreticulum: quantifying escape and the role ofauxin. Planta 202, 31332332 Frigerio, L. et al. (2001) Influence of KDEL on thefate of trimeric or assembly defective phaseolin:selective use of an alternate route to vacuoles.Plant Cell 13, 1109112633 Macdonald, H. (1997) Auxin perception andsignal transduction. Physiol. Plant.100, 42343034 Kovtun, Y. et al. (1998) Suppression of auxinsignal transduction by a MAPK cascade in higherplants. Nature 395, 71672035 Ullah, H. et al. (2001) Modulation of cellproliferation by heterotrimeric G protein inArabidopsis. Science 292, 20662069AcknowledgementsI am grateful to BarbaraTriplett, Sarah Lingle,Hee-Jin Kim, Amy Hermanand several anonymousreviewers for comments.Thanks to Jim Nolan forthe structure figure. I thankAlan Jones and CatherinePerrot-Rechenmann forsharing unpublishedresults.
View more >
Eric Allender Rutgers University Curiouser and Curiouser: The Link between Incompressibility and Complexity CiE Special Session, June 19, 2012.
Maize AUXIN-BINDING PROTEIN 1 and AUXIN-BINDING PROTEIN 4 impact on leaf growth, elongation, and seedling responsiveness to auxin and light
“Curiouser and Curiouser” What Alice, Edward Bear, Dorothy and Dr. Seuss Can Tell Us about Health Care Reform Bob Doherty, SVP, Governmental Affairs and.
P SCHOOL - Dr John Munroe’s ‘Curiouser and Curiouser’ ... I enjoy asking questions to learn about the ... booked an interview time, ...
Philip Freeman Roberta Tevlin. A relatively general introduction to BLACK HOLES Curiouser and Curiouser What are black holes? Can you get there from.