Skip to main content
SpringerLink
Log in

Auxin cross-talk: integration of signalling pathways to control plant development

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Plants sense and respond to endogenous signals and environmental cues to ensure optimal growth and development. Plant cells must integrate the myriad transduction events into a comprehensive network of signalling pathways and responses. The phytohormone auxin occupies a central place within this transduction network, frequently acting in conjunction with other signals, to co-ordinately regulate cellular processes such as division, elongation and differentiation. As a non-cell autonomous signal, auxin also interacts with other signalling pathways to regulate inter-cellular developmental processes. As part of this especially themed edition of Plant Molecular Biology, we will review examples of `cross-talk' between auxin and other signalling pathways. Given the current state of knowledge, we have deliberately focused our efforts reviewing auxin interactions with other phytohormone and light signalling pathways. We conclude by discussing how new genomic approaches and the Arabidopsis genome sequence are likely to impact this area of research in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abel, S. and Theologis, A. 1995. A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to Ps-IAA4 from pea (Pisum sativum). Plant J. 8: 87-96.

    Google Scholar 

  • Abel, S. and Theologis, A. 1996. Early gene and auxin action. Plant Physiol. 111: 9-17.

    Google Scholar 

  • Abel, S., Nguyen, M.D., Chow, W. and Theologis, A. 1995. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterisation, expression in Escherichia coli, and expression characteristics in response to auxin. J. Biol. Chem. 270: 19093-19099.

    Google Scholar 

  • Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.

    Google Scholar 

  • Armstrong, F., Leung, J., Grabov, A., Brearley, J., Giraudat, J. and Blatt M. 1995. Sensitivity to abscisic-acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase. Proc. Natl. Acad. Sci. USA 92: 9520-9524.

    Google Scholar 

  • Bangerth, F. 1994. Response of cytokinin concentration in the xylem exudate of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta 194: 439-442.

    Google Scholar 

  • Beckman, E.P., Saibo, N.J.M., Di Cataldo, A., Regalado, A.P., Ricardo, C.P. and Rodrigues-Pousada, C. 2000. Differential expression of four gene encoding 1-aminocyclopropane-1-carboxylate synthase in Lupinus albus during germination and in response to indole-3-acetic acid and wounding. Planta 211: 663-672.

    Google Scholar 

  • Behringer, F.J. and Davies, P.J. 1992. Indole-3-acetic-acid levels after phytochrome-mediated changes in the stem elongation rate of dark-grown and light-grown Pisum seedlings. Planta 188: 85-92.

    Google Scholar 

  • Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schultz, B. and Feldmann, K.A. 1996. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273: 948-950.

    Google Scholar 

  • Beyer, E.M. and Morgan, P.W. 1971. Abscission: the role of ethylene modification of auxin transport. Plant Physiol. 48: 208-212.

    Google Scholar 

  • Blatt, M.R. and Thiel G. 1994. K+ channels of Stomatal guard cells: Bimodal control of the K+ inward-rectifier evoked by auxin. Plant J. 5: 55-68.

    Google Scholar 

  • Boerjan, W., Cervera, M.T., Delarue, M., Beeckman, T., Dewitte, W., Bellini, C., Caboche, M., Vanonckelen, H., Van Montagu, M. and Inzé, D. 1995. Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7: 1405-1419.

    Google Scholar 

  • Briggs, W.R. and Huala, E. 1999. Blue-light photoreceptors in higher plants. Annu. Rev. Cell Dev. Biol. 15: 33-62.

    Google Scholar 

  • Brzobohaty, B., Moore, I., Kristoffersen, P., Bako, L., Campos, N., Schell, J. and Palme K. 1993. Release of active cytokinin by a β-glucosidase localised to the maize root meristem. Science 262: 1051-1054.

    Google Scholar 

  • Brzobohaty, B., Moore, I. and Palme K. 1994. Cytokinin metabolism: implications for regulation of plant growth and development. Plant Mol. Biol. 26: 1483-1497.

    Google Scholar 

  • Carabelli, M., Morelli, G., Whitelam, G. and Ruberti, I. 1996. Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc. Natl. Acad. Sci. USA 93: 3530-3535.

    Google Scholar 

  • Casimiro, I., Marchant, A., Bhalerao, R., Beeckman, T., Dhooge, S., Inzé, D., Sandberg, G., Casero, P. and Bennett, M.J. 2001. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13: 843-852.

    Google Scholar 

  • Celis, J.E., Kruhoffer, M., Gromova, I., Frederiksen, C., Ostergaard, M., Thykjaer, T., Gromov, P., Yu, J.S., Palsdottir, H., Magnusson, N. and Orntoft, T.F. 2000. Gene expression profiling: monitoring transcription and translation products using DNA microarrays and proteomics. FEBS Lett. 480: 2-16.

    Google Scholar 

  • Celenza, J., Grisafi, P. and Fink, G. 1995. A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 9: 2131-2142.

    Google Scholar 

  • Chatfield, S.P., Stirnberg, P., Forde, B.G. and Leyser, O. 2000. The hormonal regulation of axillary bud growth in Arabidopsis. Plant J. 24: 159-169.

    Google Scholar 

  • Chattopadhyay, S., Ang, L.H., Puente, P., Deng, X.W. and Wei, N. 1998. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10: 673-683.

    Google Scholar 

  • Chaudhury, A.M., Letham, S., Craig, S. and Dennis, E.S. 1993. AMP1: a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J. 4: 907-916.

    Google Scholar 

  • Chen, R., Rosen, E., Guan, C., Boonsirichai, K. and Masson, P.H. 2002. Complex physiological and molecular processes underlying root gravitropism. Plant Mol. Biol. 49: 305-317.

    Google Scholar 

  • Cline, M.G., Chatfield, S.P. and Leyser, O. 2001. NAA restores apical dominance in the axr3-1 mutant of Arabidopsis thaliana. Ann. Bot. 87: 61-65.

    Google Scholar 

  • Colbert, T., Till, B.J., Tompa, R., Reynolds, S., Steine, M.N., Yeung, A.T., McCallum, C.M., Comai, L. and Henikoff, S. 2001. High throughput screening for induced point mutations. Plant Physiol. 126: 480-484.

    Google Scholar 

  • Collett, C.E., Harberd, N.P. and Leyser, O. 2000. Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol. 124: 553-561.

    Google Scholar 

  • Colon-Carmona, A, Chen, D.L., Yeh, K.C. and Abel, S. 2000. Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol. 124: 1728-1738.

    Google Scholar 

  • Darwin, C. 1880. The Power of Movement in Plants. John Murray, London.

    Google Scholar 

  • DeLong, A., Mockaitis, K. and Christensen, S. 2002. Protein phosphorylation in the delivery of and response to auxin signals. Plant Mol. Biol. 49: 285-303.

    Google Scholar 

  • Del Pozo, J.C, and Estelle, M. 1999. Function of the ubquitinproteosome pathway in auxin response. Trends Plant Sci. 4: 107-112.

    Google Scholar 

  • Deshaies, R.J. 1999. SCF and cullin/ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15: 435-467.

    Google Scholar 

  • Eckert, M. and Kaldenhoff, R. 2000. Light-induced stomatal movement of selected Arabidopsis thaliana mutants. J. Exp. Bot. 51: 1435-1442.

    Google Scholar 

  • Eklof, S., Astot, C., Blackwell, J., Moritz, T., Olsson, O. and Sandberg, G. 1997. Auxin-cytokinin interactions in wild-type and transgenic tobacco. Plant Cell Physiol. 38: 225-235.

    Google Scholar 

  • Eklof, S., Astot, C., Stibon, F., Moritz, T., Olsson, O. and Sandberg, G. 2000. Transgenic tobacco plants co-expressing Agrobacterium iaa and ipt genes wild-type hormone levels but display both auxin-and cytokinin-overproducing phenotypes. Plant J. 23: 279-284.

    Google Scholar 

  • Emery, R.J.N., Longnecker, N.E.and Atkins, C.A. 1998. Branch development in Lupinus angustifolius L. II. Relationship with endogenous ABA, IAA and cytokinins in axillary and main stem buds. J. Exp. Bot. 49: 555-562.

    Google Scholar 

  • Ephritikhine, G., Fellner, M., Vannini, C., Lapous, D. and Barbier-Brygoo, H. 1999a. The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid. Plant J. 18: 303-314.

    Google Scholar 

  • Ephritikhine, G., Pagant, S., Fujioka, S., Takatsuto, S., Lapous, D., Caboche, M., Kendrick, R.E. and Barbier-Brygoo, H. 1999b. The sax1 mutation defines a new locus involved in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J. 18: 315-320.

    Google Scholar 

  • Estelle, M.A. and Somerville, C. 1987. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206: 200-206.

    Google Scholar 

  • Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K.C., Putterill, J., Palme K., Estelle, M. and Chory, J. 2001. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15: 1985-1997.

    Google Scholar 

  • Grabov, A. and Blatt, M.R. 1998. Co-ordination of signalling elements in guard cell ion channel control. J. Exp. Bot. 49: 351-360.

    Google Scholar 

  • Gray, W.M and Estelle, M. 2000. Function of the ubiquitinproteosome pathway in auxin response. Trends. Biochem. Sci. 25: 133-138.

    Google Scholar 

  • Guzman, P. and Ecker, J.R. 1990. Exploiting the triple response of Arabidopsis to identify ethylene related mutants. Plant Cell 2: 513-523.

    Google Scholar 

  • Hagen, G. and Guilfoyle, T. 2002. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49: 373-385.

    Google Scholar 

  • Hare, P.D. and van Staden, J. 1994. Cytokinin oxidase: biochemical features and physiological significance. Physiol. Plant. 91: 128-136.

    Google Scholar 

  • Harper, R.M., Stowe-Evans, E.L., Luesse, D.R., Muto, H., Tatematsu, K., Watahiki, M.K., Yamamoto, K. and Liscum, E. 2000. The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12: 757-770.

    Google Scholar 

  • Hemerly, A.S., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G. and Inze D. 1993. cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711-1723.

    Google Scholar 

  • Hobbie, H., Candace, T. Estelle, M. 1994. Molecular genetics of auxin and cytokinin. Plant Mol. Biol. 26: 1499-1519.

    Google Scholar 

  • Hobbie, L. and Estelle, M. 1995. The axr4 auxin resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J. 7: 211-220.

    Google Scholar 

  • Hsieh, H.L., Okamoto, H., Wang, M.L., Ang, L.H., Matsui, M., Goodman, H. and Deng, X.W. 2000. FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev. 14: 1958-1970.

    Google Scholar 

  • Iino, M. and Carr, D.J. 1982. Sources of free IAA in the mesocotyl of etiolated maize seedlings. Plant Physiol. 69: 1109-1112.

    Google Scholar 

  • Ikeda, T., Yakushiji, H., Oda, M., Taji, A. and Imada, S. 1999. Growth dependence of ovaries of facultatively parthenocarpic eggplant in vitro on indole-3-acetic acid content. Sci. Hort. 79: 143-150.

    Google Scholar 

  • Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K. and Kakimoto, T. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063.

    Google Scholar 

  • Irving, H.R., Dyson, G., McConchie, R., Parish, R.W. and Gehring, C.A. 1999. Effects of exogenously applied jasmontes on growth and intracellular pH in maize coleoptile segments. J. Plant Growth Regul. 18: 93-100.

    Google Scholar 

  • Ishitani, M., Xiong, L.M., Stevenson, B. and Zhu, J.K. 1997. Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic aciddependent and abscisic acid-independent pathways. Plant Cell 9: 1935-1949.

    Google Scholar 

  • Jensen, P.J., Hangarter, R.P. and Estelle, M. 1998. Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 116: 455-462.

    Google Scholar 

  • John, P.C.L., Zhang, K., Dong, C., Diederich, L. and Wightman, F. 1993. p34cdc2 related proteins in control of cell cycle progression, the switch between division and differentiation in tissue development, and stimulation of division by auxin and cytokinin. Aust. J. Plant. Physiol. 20: 503-526.

    Google Scholar 

  • Jones, A.M., Cochran, D.S., Lamerson, P.M., Evans, M.L. and Cohen, J.D. 1991. Red light-regulated growth.1. Changes in the abundance of indoleacetic-acid and a 22-kilodalton auxinbinding protein in the maize mesocotyl. Plant Physiol. 97: 352-358.

    Google Scholar 

  • Kakimoto, T. 1996. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274: 982-985.

    Google Scholar 

  • Kende, H. and Zeevaart, J.A.D. 1997. The five 'classical' plant hormones. Plant Cell 9: 1197-1210.

    Google Scholar 

  • Kieber, J.J. 1997. The ethylene response pathway in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 277-296.

    Google Scholar 

  • Kieber, J.J., Haberer, G., D'Agostino, I., Hutchison, C., Deruere, J. and Carson, S. 2001. Cytokinin signalling in Arabidopsis: role of the A type response regulators. Proceedings the 17th International Conference on Plant Growth Substances, Brno, p. 46.

  • Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A. and Ecker, J.R. 1993. Ctr1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein-kinases. Cell 72: 427-441.

    Google Scholar 

  • Kim, S.K., Chang, S.C., Lee, E.J., Chung, W.S., Kim, Y.S., Hwang, S. and Lee, J.S. 2000. Involvement of brassinosteroids in the gravitropic response of primary root of maize. Plant Physiol. 123: 997-1004.

    Google Scholar 

  • Klee, H.J., Horsch, R.B., Hinchee, M.A., Hein, M.B. and Hoffmann, N.L. 1987. The effects of overproduction of 2 Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes. Dev. 1: 86-96.

    Google Scholar 

  • Kotov, A.A. and Kotova, L.M. 2000. The contents of auxins and cytokinins in pea internodes as related to the growth of lateral buds. J. Plant Physiol. 156: 438-448.

    Google Scholar 

  • Kraepiel, Y., Marrec, K., Sotta, B., Caboche, M. and Miginiac, E. 1995. In-vitro morphogenic characteristics of phytochrome mutants in Nicotiana plumbaginifolia are modified and correlated to high indole-3-acetic-acid levels. Planta 197: 142-146.

    Google Scholar 

  • Kuhn, E. 2001. From library screening to microarray technology: strategies to determine gene expression profiles and to identify differentially regulated genes in plants. Ann. Bot. 87: 139-155.

    Google Scholar 

  • Law, D.M. and Davies, P.J. 1990. Comparative indole-3-acetic-acid levels in the slender pea and other pea phenotypes. Plant Physiol. 93: 1539-1543.

    Google Scholar 

  • Lehman, A., Black, R. and Ecker, J.R. 1996. HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85: 183-194.

    Google Scholar 

  • Lester, D.R., Ross, J.J., Davies, P.J. and Reid, J.B. 1997. Mendel's stem length gene (Le) encodes a gibberellin 3-β-hydroxylase. Plant Cell 9: 1435-1443.

    Google Scholar 

  • Letham, D.S, Goodwin, P.B. and Higgins, T.J.V. 1978. Phytohormones and Related Compounds: A Comprehensive Treatise. Elsevier/North-Holland Biomedical Press, Amsterdam, Netherlands.

    Google Scholar 

  • Leyser, H.M.O., Lincoln, C.A., Timpte, C., Lammer, D., Turner, J. and Estelle, M. 1993. Arabidopsis auxin-resistance gene Axr1 encodes a protein related to ubiquitin-activating enzyme-E1. Nature 364: 161-164.

    Google Scholar 

  • 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.

    Google Scholar 

  • Liang, X., Abel, S., Keller, J.A., Shen, N.F. and Theologis, A. 1992. The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89: 11046-11050.

    Google Scholar 

  • Lincoln, C., Britton, J.H. and Estelle, M. 1990. Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071-1080.

    Google Scholar 

  • Liscum, E. and Briggs, W.R. 1996. Mutations of Arabidopsis in potential transduction and response components of the phototropic signaling pathway. Plant Physiol. 112: 291-296.

    Google Scholar 

  • 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.

    Google Scholar 

  • Liu, Z.B., Ulmasov, T., Shi., X.Y., Hagen, G. and Guilfoyle, T.J. 1994. Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6: 645-657.

    Google Scholar 

  • Luschnig, C., Gaxiola, R.A., Grisafi, P. and Fink, G.R. 1998. EIR1: a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12: 2175-2187.

    Google Scholar 

  • Maher, E.P. and Martindale, S.J.B. 1980. Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem. Genet. 18: 1041-1053.

    Google Scholar 

  • Marchant, A., Kargul, J., May, S.T., Muller, P., Delbarre, A., Perrot-Rechenmann, C. and Bennett, M.J. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 18: 2066-2073.

    Google Scholar 

  • Masucci, J.D. and Schiefelbein, J. 1994. The rhd6 mutation of Arabidopsis thaliana alters root epidermal-cell polarity and is rescued by auxin. Dev. Biol. 163: 554-554.

    Google Scholar 

  • McCallum, C.M., Comai, L., Green, E.A. and Henikoff, S. 2000a. Targeted screening for induced mutations. Nature Biotechnol. 18: 455-457.

    Google Scholar 

  • McCallum, C.M., Comai, L., Green, E.A. and Henikoff, S. 2000b. Targeting Induced Local Lesions IN Genomes (TILLING) for plant functional genomics. Plant Physiol.123: 439-442.

    Google Scholar 

  • McCourt, P. 1999. Genetic analysis of hormone signalling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 219-243.

    Google Scholar 

  • McNellis, T.W., von Arnim, A.G., Araki, T., Komeda, Y., Misera, S. and Deng, X.-W. 1994. Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6: 487-500.

    Google Scholar 

  • Medford, J.I., Horgan, R., Elsawi, Z. and Klee, H.J. 1989. Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene. Plant Cell 1: 403-413.

    Google Scholar 

  • Miller, C.O., Scoog, F., Okumura, F.S., von Saltza, M.H. and Strong, F.M. 1956. J. Am. Chem. Soc. 78:1375-1380.

    Google Scholar 

  • Morelli, G. and Ruperti, I. 2000. Shade avoidance responses. Driving auxin along lateral routes. Plant Physiol. 122: 621-626.

    Google Scholar 

  • Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M.J., Wisman, E. and Palme, K. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17: 6903-6911.

    Google Scholar 

  • Nagpal, P., Walker, L., Young, J., Sonawala, A., Timpte, C., Estelle, M. and Reed, J. 2000. AXR2 encodes a member of the Aux/IAA p[rotein family. Plant Physiol. 123: 563-573.

    Google Scholar 

  • Nakazawa, M., Yabe, N., Ichikawa, T., Yamamoto, Y.Y., Yoshizumi, T., Hasunuma, K. and Matsui, M. 2001. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J. 25: 213-221.

    Google Scholar 

  • Nogue, F., Grandjean, O., Craig, S., Dennis, S. and Chaudhury, M. 2000. Higher levels of cell proliferation rate and cyclin CycD3 expression in the Arabidopsis amp1 mutant. Plant Growth Regul. 32: 275-283.

    Google Scholar 

  • Osterlund, M.T., Hardtke, C.S., Wei, N. and Deng, X.W. 2000. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466.

    Google Scholar 

  • Oyama, T., Shimura, Y. and Okada, K. 1997. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Gene. Dev. 11: 2983-2995.

    Google Scholar 

  • Palni, L.M.S., Burch, L. and Horgan, R. 1988. The effect of auxin concentration on cytokinin stability and metabolism. Planta 194: 439-442.

    Google Scholar 

  • Pickett, F.B., Wilson, A.K. and Estelle, M. 1990. The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 94: 1462-1466.

    Google Scholar 

  • Pitts, J.P., Cernac, A. and Estelle, M. 1998. Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J. 16: 553-560.

    Google Scholar 

  • Rahman, A., Amakawa, T., Goto, N. and Tsurumi, S. 2001. Auxin is a positive regulator for ethylene-mediated response in the growth of arabidopsis roots. Plant Cell Physiol. 42: 301-307.

    Google Scholar 

  • Raz, V. and Ecker, J.R. 1999. Regulation of differential growth in the apical hook of Arabidopsis. Development 126: 3661-3668.

    Google Scholar 

  • Richards, D.E., King, K.E., Ait-ali, T. and Harberd, N.P. 2001. How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 67-88.

    Google Scholar 

  • Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541-1544.

    Google Scholar 

  • 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.

    Google Scholar 

  • Roman, G., Lubarsky, B., Kieber, J.J., Rothenberg, M. and Ecker, J.R. 1995. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139: 1393-1409.

    Google Scholar 

  • Romano, C.P., Hein, M.B. and Klee, H.J. 1991. Inactivation of auxin in tobacco transformed with the indoleacetic acid lysine synthetase gene of Pseudomonas savastanoi. Genes Dev. 5: 438-446.

    Google Scholar 

  • Romano, C., Cooper, M. and Klee, H. 1993. Uncoupling auxin and ethylene effects in transgenic tobacco and Arabidopsis plants. Plant Cell 5: 181-189.

    Google Scholar 

  • Romano, C.P., Robson, P.R.H., Smith, H., Estelle, M. and Klee, H. 1995. Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants. Plant Mol. Biol. 27: 1071-1083.

    Google Scholar 

  • Ross, J.J. 1998. Effects of auxin transport inhibitors on gibberellins in pea. J. Plant Growth Regul. 17: 141-146.

    Google Scholar 

  • Ross, J.J. and O'Neill, D. 2001. New interactions between classical plant hormones. Trends Plant Sci. 6: 2-4.

    Google Scholar 

  • Ross, J.J., O'Neill, D.P., Smith, J.J., Kerckhoffs, L.H.J. and Elliott, R.C. 2000. Evidence that auxin promotes gibberellin A(1) biosynthesis in pea. Plant J. 21: 547-552.

    Google Scholar 

  • 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.

    Google Scholar 

  • Ruegger, M., Dewey, E., Hobbie, L., Brown, D., Bernasconi, P., Turner, J., Muday, G. and 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.

    Google Scholar 

  • Ruegger, M., Dewey, E., Gray, W., Hobbie, L., Turner, J. and Estelle, M. 1988. The TIR1 protein of Arabidopsis functions in auxin response and is related human SKP2 and yeast Grr1p. Genes Dev. 12: 198-207.

    Google Scholar 

  • Sastry, T. and Muir, R. 1963. Gibberellins: affect on diffusible auxin in fruit development. Science 140: 494-495.

    Google Scholar 

  • Schmulling, T. 2001. CREam of cytokinin signalling: receptor identified. Trends Plant Sci. 6: 281-284.

    Google Scholar 

  • Schwechheimer, C., Serino, G., Callis, J., Crosby, W.L., Lyapina, S., Deshaies, R.J., Gray, W.M., Estelle, M. and Deng, X.W. 2001. Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIR1 in mediating auxin response. Science 292: 1379-1382.

    Google Scholar 

  • Skoog, F. and Miller, C.O. 1957. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11: 118-131.

    Google Scholar 

  • Skoog, F. and Tsui, C. 1948. Formation of adventitious shoots and roots in tobacco. Am. J. Bot. 35: 782-787.

    Google Scholar 

  • Smalle, J., Haegman, M., Kurepa, J., Van Montagu, M. and Vanderstraeten, D. 1997. Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc. Natl. Acad. Sci. USA 94: 2756-2761.

    Google Scholar 

  • Smith, H. and Whitelam, G.C. 1997. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Envir. 20: 840-844.

    Google Scholar 

  • Soni, R., Carmichael, J.P., Shah, Z.H. and Murray, J.A.H. 1995. A family of cyclin D homologues from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85-103.

    Google Scholar 

  • Sponsel, V.M., Schmidt, F.M., Porter, S.G., Nakayama, M., Kohlstruk, S. and Estelle, M. 1997. Characterization of new gibberellin-responsive semidwarf mutants of Arabidopsis. Plant Physiol. 115: 1009-1020.

    Google Scholar 

  • Steindler, C., Carabelli, M., Borello, U., Morelli, G. and Ruberti, I. 1997. Phytochrome A, phytochrome B and other phytochrome( s) regulate ATHB-2 gene expression in etiolated and green Arabidopsis plants. Plant Cell Envir. 20: 759-763.

    Google Scholar 

  • Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G. and Ruberti, I. 1999. Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126: 4235-4245.

    Google Scholar 

  • Stirnberg, P., Chatfield, S.P. and Leyser, H.M.O. 1999. AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol. 121: 839-847.

    Google Scholar 

  • Tamimi, S. and Firn, R.D. 1985. The basipetal auxin transportsystem and the control of cell elongation in hypocotyls. J. Exp. Bot. 36: 955-962.

    Google Scholar 

  • Tang, Z.J., Sadka, A., Morishige, D.T., and Mullet, J.E. 2001. Homeodomain leucine zipper proteins bind to the phosphate response domamin of the soybean VspB tripartite promoter. Plant Physiol. 125: 797-809.

    Google Scholar 

  • Tian, Q. and Reed, J.W. 1999. Control pf auxin regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126: 711-721.

    Google Scholar 

  • Timpte, C., Wilson, A. and Estelle, M. 1994. The axr2-1 mutation of Arabidopsis thaliana is a gain of function mutation that disrupts an early step in auxin response. Genetics 138: 1239-1249.

    Google Scholar 

  • Torii, K.U., McNellis, T.W. and Deng, X.W. 1998. Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J. 17: 5577-5587.

    Google Scholar 

  • Ueda, J., Miyamoto, K. and Aoki, M. 1994. Jasmonic acid inhibits the IAA-induced elongation of oat coleoptile segments-a possible mechanism involving the metabolism of cell-wall polysaccharides. Plant Cell Physiol. 35: 1065-1070.

    Google Scholar 

  • Vivian-Smith, A. and Koltunow, A.M. 1999. Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol. 121: 437-451

    Google Scholar 

  • von Arnim, A.G., Osterlund, M.T., Kwok, S.F. and Deng, X.W. 1997. Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol. 114: 779-788.

    Google Scholar 

  • Walton, J.D and Ray, P.M. 1981. Evidence for receptor function of auxin binding sites in maize. Red light inhibition of mesophyill elongation and auxin binding. Plant Physiol. 68: 1334-1338.

    Google Scholar 

  • Wang, C.X., Jarlfords, U. and Hildebrand, D.F. 1999. Regulation and subcellular localisation of auxin-induced lipoxygenases. Plant Sci. 148: 147-153.

    Google Scholar 

  • Watahiki, M.K. and Yamamoto, K.T. 1997. The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol. 115: 419-426.

    Google Scholar 

  • Wei, N. and Deng, X.W. 1999. Making sense of the COP9 signalosome: a regulatory protein complex conserved from Arabidopsis to human. Trends Genet. 15: 98-103.

    Google Scholar 

  • Went, F.W. and Thimann, K.V. 1937. Phytohormones. MacMillan, New York.

    Google Scholar 

  • Wickson, M. and Thimann, K.V. 1958. The antagonism of auxin and kinetin in apical dominance. Physiol. Plant. 11: 62-74.

    Google Scholar 

  • Williams, D.M. and Cole, P.A. 2001. Kinase chips hit the proteomics era. Trends Biochem. Sci. 26: 271-273.

    Google Scholar 

  • Wilson, A.K., Pickett, F.B., Turner, J.C. and Estelle, M. 1990. A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol. Gen. Genet. 222: 377-383.

    Google Scholar 

  • Woeste, K.E., Vogel, J.P. and Kieber, J.J. 1999. Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol. Plant. 105: 478-484.

    Google Scholar 

  • Worley, C.K., Zenser, N., Ramos, J., Rouse, D., Leyser, O., Theologis, A. and Callis, J. 2000. Degradation of Aux/IAA proteins is essential for normal auxin signalling. Plant J. 21: 553-562.

    Google Scholar 

  • Xie, D.X. Feys, B.F., James, S., Nieto-Rostro. M. and Turner, J.G. 1998. COI1: an Arabidopsis gene required for jasmonate-regulated defence and fertility. Science 280: 1091-1094.

    Google Scholar 

  • Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., Ashikari, M., Kitano, H. and Matsuoka, M. 2000. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1605.

    Google Scholar 

  • Yang, S.F. and Hoffman, N.E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 35: 155-189.

    Google Scholar 

  • Yip, W. and Yang, S.F.B. 1986. Effect of thidiazuron, a cytokininactive urea derivative, in cytokinin-dependent ethylene production systems. Plant Physiol. 80: 515-519.

    Google Scholar 

  • Yi, H.C., Joo, S., Nam, K.H., Lee, J.S., Kang, B.G. and Kim, W.T. 1999. Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol. Biol. 41: 443-454.

    Google Scholar 

  • Yu, S.J., Kim, S., Lee, J.S. and Lee, D.H. 1998. Differential accumulation of transcripts for ACC synthase and ACC oxidase homologs in etiolated mung bean hypocotyls in response to various stimuli. Mol. Cells 8: 350-358.

    Google Scholar 

  • Zhang, R. Zhang, X., Wang, J., Letham, D.S., McKinney, S.A. and Higgins, T.J.V. 1995. The effect of auxin on cytokinin levels and metabolism in transgenic tobacco tissue expressing an ipt gene. Planta 196: 84-94.

    Google Scholar 

  • Zobel, R.W. 1974. Control of morphogenesis in the ethylene requiring tomato mutant, diageotropica. Can. J. Bot. 52: 735-741.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biosciences, Sutton Bonington, University of Nottingham, Leicestershire, LE12 5RD, UK

    Ranjan Swarup, Geraint Parry, Neil Graham, Trudie Allen & Malcolm Bennett

Authors
  1. Ranjan Swarup
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geraint Parry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Neil Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Trudie Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Malcolm Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Swarup, R., Parry, G., Graham, N. et al. Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49, 409–424 (2002). https://doi.org/10.1023/A:1015250929138

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1015250929138

Search

Navigation