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Integration of Ethylene and Auxin Signaling and the Developmental Consequences of Their Crosstalk

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Ethylene in Plants

Abstract

Ethylene and auxin have overlapping effects on growth and development of young seedlings, with either synergistic or antagonistic actions depending on the developmental process. This chapter introduces the growth and developmental processes that are regulated by these two hormones and explores recent studies that provide insight into the mechanistic basis for the regulation of these processes. Ethylene and auxin both inhibit root elongation and stimulate root hair elongation, while acting in opposition on lateral root development and hypocotyl elongation. The interplay between the hormones is even more complex in differential growth processes, such as gravitropism, nutation, and apical hook opening. The presence of well characterized mutants with altered ethylene and auxin signaling and synthesis, as well as auxin transport, has been essential to demonstrate the mechanistic basis of crosstalk between these hormones. As both of these hormones lead to profound changes in gene expression, genome-wide transcript abundance data sets are identifying additional genes that are induced or repressed through this hormonal crosstalk. Experimental tests of predicted regulatory networks involving these genes will likely yield the next set of new insights into the mechanisms by which these hormones control plant growth and development.

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References

  • Abbas M, Alabadi D, Blazquez MA. Differential growth at the apical hook: all roads lead to auxin. Front Plant Sci. 2013;4:441.

    PubMed  PubMed Central  Google Scholar 

  • Abel S, Nguyen MD, Theologis A. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J Mol Biol. 1995a;251:533–49.

    PubMed  CAS  Google Scholar 

  • Abel S, Nguyen MD, Chow W, Theologis A. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J Biol Chem. 1995b;270:19093–9.

    PubMed  CAS  Google Scholar 

  • Alarcon MV, Lloret PG, Salguero J. Auxin-ethylene interaction in transversal and longitudinal growth in maize primary root. Botany. 2013;91:680–5.

    CAS  Google Scholar 

  • Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science. 1999;284:2148–52.

    PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, Ecker JR. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA. 2003;100:2992–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem. 2008;283:21817–26.

    PubMed  CAS  Google Scholar 

  • Baldwin KL, Strohm AK, Masson PH. Gravity sensing and signal transduction in vascular plant primary roots. Am J Bot. 2013;100:126–42.

    PubMed  CAS  Google Scholar 

  • Barry CS, Giovannoni JJ. Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci USA. 2006;103:7923–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Basu P, Brown KM, Pal A. Detailed quantitative analysis of architectural traits of basal roots of young seedlings of bean in response to auxin and ethylene. Plant Physiol. 2011;155:2056–65.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bellini C, Pacurar DI, Perrone I. Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol. 2014;65:639–66.

    PubMed  CAS  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602.

    PubMed  CAS  Google Scholar 

  • Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science. 1996;273:948–50.

    PubMed  CAS  Google Scholar 

  • Beyer EM, Morgan PW. Abscission: the role of ethylene modification of auxin transport. Plant Physiol. 1971;48:208–12.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bhalerao RP, Eklöf J, Ljung K, Marchant A, Bennett M, Sandberg G. Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 2002;29:325–32.

    PubMed  CAS  Google Scholar 

  • Binder BM, O’Malley RC, Wang WY, Zutz TC, Bleecker AB. Ethylene stimulates nutations that are dependent on the ETR1 receptor. Plant Physiol. 2006;142:1690–700.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bleecker AB, Estelle MA, Somerville C, Kende H. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science. 1988;241:1086–9.

    PubMed  CAS  Google Scholar 

  • Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Onckelen H, Van Montagu M, Inze D. Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell. 1995;7:1405–19.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Britz SJ, Galston AW. Physiology of movements in stems of seedling pisum-sativum-L Cv alaska. 2. The role of the apical hook and of auxin in nutation. Plant Physiol. 1982;70:1401–4.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 2001;126:524–35.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Buer CS, Muday GK. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell. 2004;16:1191–205.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Buer CS, Wasteneys GO, Masle J. Ethylene modulates root-wave responses in Arabidopsis. Plant Physiol. 2003;132:1085–96.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Buer CS, Sukumar P, Muday GK. Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol. 2006;140:1384–96.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Burg SP, Burg EA. The interaction between auxin and ethylene and its role in plant growth. Proc Natl Acad Sci USA. 1966;55:262–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Burg SP, Burg EA. Inhibition of polar auxin transport by ethylene. Plant Physiol. 1967;42:1224–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett M. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell. 2001;13:843–52.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993;262:539–44.

    PubMed  CAS  Google Scholar 

  • Chang SC, Kim YS, Lee JY, Kaufman PB, Kirakosyan A, Yun HS, Kim TW, Kim SY, Cho MH, Lee JS, Kim SK. Brassinolide interacts with auxin and ethylene in the root gravitropic response of maize (Zea mays). Physiol Plant. 2004;121:666–73.

    CAS  Google Scholar 

  • Chapman EJ, Estelle M. Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet. 2009;43:265–85.

    PubMed  CAS  Google Scholar 

  • Chen RJ, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH. The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci USA. 1998;95:15112–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cho M, Lee SH, Cho HT. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell. 2007;19:3930–43.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ. Root formation in ethylene-insensitive plants. Plant Physiol. 1999;121:53–60.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cluis CP, Mouchel CF, Hardtke CS. The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J. 2004;38:332–47.

    PubMed  CAS  Google Scholar 

  • Coleman WK, Huxter TJ, Reid DM, Thorpe TA. Ethylene as an endogenous inhibitor of root regeneration in tomato leaf-disks cultured in vitro. Physiol Plantarum 1980;48:519–25.

    Google Scholar 

  • Collett CE, Harberd NP, Leyser O. Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol. 2000;124:553–61.

    PubMed  CAS  PubMed Central  Google Scholar 

  • De-Klerk G, Krieken W, Wada T, DeJong J. The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Biol-Plant. 1999;35:481–90.

    Google Scholar 

  • de Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D. Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol. 2005;46:827–36.

    PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature. 2005;435:441–5.

    PubMed  CAS  Google Scholar 

  • Dolan L. The role of ethylene in root hair growth in Arabidopsis. J Plant Nutr Soil Sci. 2001;164:141–5.

    CAS  Google Scholar 

  • Estelle MA, Somerville C. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol Gen Genet. 1987;206:200–6.

    CAS  Google Scholar 

  • Friml J, Palme K. Polar auxin transport–old questions and new concepts? Plant Mol Biol. 2002;49:273–84.

    PubMed  CAS  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M. Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 2002;29:153–68.

    PubMed  CAS  Google Scholar 

  • Ganguly A, Lee SH, Cho M, Lee OR, Yoo H, Cho HT. Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol. 2010;153:1046–61.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Garbers C, DeLong A, Deruère J, Bernasconi P, Soll D. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J. 1996;15:2115–24.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Geisler M, Wang B, Zhu J. Auxin transport during root gravitropism: transporters and techniques. Plant Biol (Stuttg). 2014;16(Suppl 1):50–7.

    Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, Muller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 2005;44:179–94.

    PubMed  CAS  Google Scholar 

  • Giovannoni JJ. Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol. 2007;10:283–9.

    PubMed  CAS  Google Scholar 

  • Gupta A, Singh M, Jones AM, Laxmi A. Hypocotyl directional growth in Arabidopsis: a complex trait. Plant Physiol. 2012;159:1463–76.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Guzman P, Ecker JR. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell. 1990;2:513–23.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hall JL, Brummell DA, Gillespie J. Does auxin stimulate the elongation of intact plant stems? New Phyt. 1985;100:341–5.

    CAS  Google Scholar 

  • Hashiguchi Y, Tasaka M, Morita MT. Mechanism of higher plant gravity sensing. Am J Bot. 2013;100:91–100.

    Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E. The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell. 2000;12:757–70.

    PubMed  CAS  PubMed Central  Google Scholar 

  • He W, Brumos J, Li H, Ji Y, Ke M, Gong X, Zeng Q, Li W, Zhang X, An F, Wen X, Li P, Chu J, Sun X, Yan C, Yan N, Xie DY, Raikhel N, Yang Z, Stepanova AN, Alonso JM, Guo H. A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell. 2011;23:3944–60.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Huang Y, Li H, Hutchison CE, Laskey J, Kieber JJ. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. 2003;33:221–33.

    PubMed  CAS  Google Scholar 

  • Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol. 2009;11:731–8.

    PubMed  CAS  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG. Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J. 2008;55:335–47.

    PubMed  CAS  Google Scholar 

  • Jacobs M, Rubery PH. Naturally-occurring auxin transport regulators. Science. 1988;241:346–9.

    PubMed  CAS  Google Scholar 

  • Jensen PJ, Hangarter RP, Estelle M. Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 1998;116:455–62.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS. Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol. 2009;11:78–84.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kendrick MD, Chang C. Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol. 2008;11:479–85.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kepinski S, Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 2005;435:446–51.

    PubMed  CAS  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell. 1993;72:427–41.

    PubMed  CAS  Google Scholar 

  • Kim H, Helmbrecht EE, Stalans MB, Schmitt C, Patel N, Wen CK, Wang WY, Binder BM. Ethylene receptor ethylene receptor1 domain requirements for ethylene responses in Arabidopsis seedlings. Plant Physiol. 2011;156:417–29.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kim HJ, Lynch JP, Brown KM. Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant, Cell Environ. 2008;31:1744–55.

    CAS  Google Scholar 

  • King JJ, Stimart DP, Fisher RH, Bleecker AB. A mutation altering auxin homeostasis and plant morphology in Arabidopsis. Plant Cell. 1995;7:2023–37.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B. Root system architecture from coupling cell shape to auxin transport. PLoS Biol. 2008;6:14.

    Google Scholar 

  • Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 2013;18:450–8.

    PubMed  CAS  Google Scholar 

  • Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP. In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol. 2001;125:519–22.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lee DJ, Park JW, Lee HW, Kim J. Genome-wide analysis of the auxin-responsive transcriptome downstream of iaa1 and its expression analysis reveal the diversity and complexity of auxin-regulated gene expression. J Exp Bot. 2009;60:3935–57.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lee JS, Chang WK, Evans ML. Effects of ethylene on the kinetics of curvature and auxin redistribution in gravistimulated toots of Zea mays. Plant Physiol. 1990;94:1770–5.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lehman A, Black R, Ecker JR. HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell. 1996;85:183–94.

    PubMed  CAS  Google Scholar 

  • Lewis D, Muday G. Ethylene regulates root growth and development. In: Eschel A, Beeckman T, editors. Plant roots: the hidden half. Boca Raton: CRC Press; 2013. p. 1–27.

    Google Scholar 

  • Lewis D, Olex A, Lundy S, Turkett W, Fetrow J, Muday G. A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell. 2013;25:3329–46.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lewis DR, Negi S, Sukumar P, Muday GK. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development. 2011a;138:3485–95.

    PubMed  CAS  Google Scholar 

  • Lewis DR, Ramirez MV, Miller ND, Vallabhaneni P, Ray WK, Helm RF, Winkel BS, Muday GK. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 2011b;156:144–64.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell. 2007;19:1838–50.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Leyser HM, Pickett FB, Dharmasiri S, Estelle M. Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J. 1996;10:403–13.

    PubMed  CAS  Google Scholar 

  • Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR. Convergence of signaling of differential cell growth pathways in the control in Arabidopsis. Dev Cell. 2004;7:193–204.

    PubMed  CAS  Google Scholar 

  • Li J, Dai X, Zhao Y. A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol. 2006;140:899–908.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu X, Cohen JD, Gardner G. Low-fluence red light increases the transport and biosynthesis of auxin. Plant Physiol. 2011;157:891–904.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Luschnig C, Gaxiola RA, Grisafi P, Fink GR. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–87.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Maher EP, Martindale SJ. Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem Genet. 1980;18:1041–53.

    PubMed  CAS  Google Scholar 

  • Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 1999;18:2066–73.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell. 2002;14:589–97.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Markakis MN, De Cnodder T, Lewandowski M, Simon D, Boron A, Balcerowicz D, Doubbo T, Taconnat L, Renou JP, Hofte H, Verbelen JP, Vissenberg K. Identification of genes involved in the ACC-mediated control of root cell elongation in Arabidopsis thaliana. BMC Plant Biol. 2012;12:208.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Masucci JD, Schiefelbein JW. The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol. 1994;106:1335–46.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mockaitis K, Estelle M. Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol. 2008;24:55–80.

    PubMed  CAS  Google Scholar 

  • Morgan P, Hall W. Effect of 2,4-Dichlorophenoxyacetic acid on the production of ethylene by cotton and grain sorghum. Physiol Plant. 1962;15:420–7.

    CAS  Google Scholar 

  • Muday GK, Rahman A. Auxin transport and the integration of gravitropic growth. In: Gilroy S, Masson P, editors. Plant tropisms. Oxford: Blackwell Publishing; 2008. p. 47–8.

    Google Scholar 

  • Muday GK, Lomax TL, Rayle DL. Characterization of the growth and auxin physiology of roots of the tomato mutant, diageotropica. Planta. 1995;195:548–53.

    PubMed  CAS  Google Scholar 

  • Muday GK, Rahman A, Binder BM. Auxin and ethylene: collaborators or competitors? Trends Plant Sci. 2012;17:181–95.

    PubMed  CAS  Google Scholar 

  • Muday GK, Brady SR, Argueso C, Deruere J, Kieber JJ, DeLong A. RCN1-regulated phosphatase activity and EIN2 modulate hypocotyl gravitropism by a mechanism that does not require ethylene signaling. Plant Physiol. 2006;141:1617–29.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Müller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 1998;17:6903–11.

    PubMed  PubMed Central  Google Scholar 

  • Negi S, Ivanchenko MG, Muday GK. Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J. 2008;55:175–87.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Negi S, Sukumar P, Liu X, Cohen JD, Muday GK. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 2010;61:3–15.

    PubMed  CAS  Google Scholar 

  • Nordstrom A, Eliasson L. Regulation of root formation by auxin-ethylene interaction in pea stem cuttings. Physiol Plant. 1984;61:298–302.

    Google Scholar 

  • Okada K, Shimura Y. Modulation of root growth by physical stimuli. In Arabidopsis. Cold Spring Harbor Press; 1994. pp. 665–84.

    Google Scholar 

  • Okamoto T, Tsurumi S, Shibasaki K, Obana Y, Takaji H, Oono Y, Rahman A. Genetic dissection of hormonal responses in the roots of Arabidopsis grown under continuous mechanical impedance. Plant Physiol. 2008;146:1651–62.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T. Auxin control of root development. Cold Spring Harb Perspect Biol. 2010;2:a001537.

    PubMed  PubMed Central  Google Scholar 

  • Pacheco-Villalobos D, Sankar M, Ljung K, Hardtke CS. Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots. PLoS Genet. 2013;9:e1003564.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pacurar DI, Pacurar ML, Bussell JD, Schwambach J, Pop TI, Kowalczyk M, Gutierrez L, Cavel E, Chaabouni S, Ljung K, Fett-Neto AG, Pamfil D, Bellini C. Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J Exp Bot. 2014;65:1605–18.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Paponov IA, Paponov M, Teale W, Menges M, Chakrabortee S, Murray JA, Palme K. Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant. 2008;1:321–37.

    PubMed  CAS  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell. 2004;16:1898–911.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pickett FB, Wilson AK, Estelle M. The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 1990;94:1462–6.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M. Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J. 1998;16:553–60.

    PubMed  CAS  Google Scholar 

  • Poupart J, Rashotte AM, Muday GK, Waddell CS. The rib1 mutant of Arabidopsis has alterations in indole-3-butyric acid transport, hypocotyl elongation, and root architecture. Plant Physiol. 2005;139:1460–71.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Radwanski ER, Barczak AJ, Last RL. Characterization of tryptophan synthase alpha subunit mutants of Arabidopsis thaliana. Mol Gen Genet. 1996;253:353–61.

    PubMed  CAS  Google Scholar 

  • Rahman A, Amakawa T, Goto N, Tsurumi S. Auxin is a positive regulator for ethylene-mediated response in the growth of Arabidopsis roots. Plant Cell Physiol. 2001;42:301–7.

    PubMed  CAS  Google Scholar 

  • Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S. Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol. 2002;130:1908–17.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI. Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J. 2007;50:514–28.

    PubMed  CAS  Google Scholar 

  • Rashotte AM, DeLong A, Muday GK. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell. 2001;13:1683–97.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rashotte AM, Poupart J, Waddell CS, Muday GK. Transport of the two natural auxins, indole-3-butyric acid and indole-3-acetic acid, in Arabidopsis. Plant Physiol. 2003;133:761–72.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 2000;122:481–90.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Raz V, Ecker JR. Regulation of differential growth in the apical hook of Arabidopsis. Development. 1999;126:3661–8.

    PubMed  CAS  Google Scholar 

  • Reed RC, Brady SR, Muday GK. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol. 1998;118:1369–78.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Robles LM, Deslauriers SD, Alvarez AA, Larsen PB. A loss-of-function mutation in the nucleoporin AtNUP160 indicates that normal auxin signalling is required for a proper ethylene response in Arabidopsis. J Exp Bot. 2012;63:2231–41.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rogg LE, Lasswell J, Bartel B. A gain-of-function mutation in iaa28 suppresses lateral root development. Plant Cell. 2001;13:465–80.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics. 1995;139:1393–409.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007;19:2197–212.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Santisree P, Nongmaithem S, Vasuki H, Sreelakshmi Y, Ivanchenko MG, Sharma R. Tomato root penetration in soil requires a coaction between ethylene and auxin signaling. Plant Physiol. 2011;156:1424–38.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sargent JA, Atack AV, Osborne DJ. Auxin and ethylene control of growth in epidermal cells of Pisum sativum—biphasic response to auxin. Planta. 1974;115:213–25.

    PubMed  CAS  Google Scholar 

  • Schiefelbein JW. Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 2000;124:1525–31.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schlicht M, Samajova O, Schachtschabel D, Mancuso S, Menzel D, Boland W, Baluska F. D’orenone blocks polarized tip growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex. Plant J. 2008;55:709–17.

    PubMed  CAS  Google Scholar 

  • Shibasaki K, Uemura M, Tsurumi S, Rahman A. Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell. 2009;21:3823–38.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shin K, Lee RA, Lee I, Lee S, Park SK, Soh MS. Genetic identification of a second site modifier of ctr1-1 that controls ethylene-responsive and gravitropic root growth in Arabidopsis thaliana. Mol Cells. 2013;36:88–96.

    PubMed  PubMed Central  Google Scholar 

  • Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS. Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genet. 2006;2:e202.

    PubMed  PubMed Central  Google Scholar 

  • Skottke KR, Yoon GM, Kieber JJ, DeLong A. Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 2011;7:e1001370.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smalle J, Haegman M, Kurepa J, Van Montagu M, Straeten DV. Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci U S A. 1997;94:2756–61.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 1998;12:3703–14.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Stepanova AN, Alonso JM. Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol. 2009;12:548–55.

    PubMed  CAS  Google Scholar 

  • Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell. 2005;17:2230–42.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 2007;19:2169–85.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–91.

    PubMed  CAS  Google Scholar 

  • Stowe-Evans EL, Harper RM, Motchoulski AV, Liscum E. NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol. 1998;118:1265–75.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Strader LC, Chen GL, Bartel B. Ethylene directs auxin to control root cell expansion. Plant J. 2010;64:874–84.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sukumar P. Role of auxin and ethylene in adventitious root formation in Arabidopsis and tomato. In Biology. Winston Salem: Wake Forest University; 2010.

    Google Scholar 

  • Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK. PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol. 2009;150:722–35.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Suttle JC. Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-Naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiol. 1988;88:795–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennett MJ. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19:2186–96.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tian Q, Reed JW. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development. 1999;126:711–21.

    PubMed  CAS  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ. Dimerization and DNA binding of auxin response factors. Plant J. 1999;19:309–19.

    PubMed  CAS  Google Scholar 

  • Utsuno K, Shikanai T, Yamada Y, Hashimoto T. AGR, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. 1998;39:1111–8.

    PubMed  CAS  Google Scholar 

  • van Norman JM, Xuan W, Beeckman T, Benfey PN. To branch or not to branch: the role of pre-patterning in lateral root formation. Development. 2013;140:4301–10.

    PubMed  Google Scholar 

  • Vandenbussche F, Vriezen WH, Smalle J, Laarhoven LJ, Harren FJ, Van Der Straeten D. Ethylene and auxin control the Arabidopsis response to decreased light intensity. Plant Physiol. 2003;133:517–27.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Vandenbussche F, Petrasek J, Zadnikova P, Hoyerova K, Pesek B, Raz V, Swarup R, Bennett M, Zazimalova E, Benkova E, Van Der Straeten D. The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development. 2010;137:597–606.

    PubMed  CAS  Google Scholar 

  • Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inze D, Fukaki H, Beeckman T. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell. 2005;17:3035–50.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ. An ethylene-inducible component of signal transduction encoded by never- ripe. Science. 1995;270:1807–9.

    PubMed  CAS  Google Scholar 

  • Wilson AK, Pickett FB, Turner JC, Estelle M. A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet. 1990;222:377–83.

    PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot (Lond). 2005;95:707–35.

    CAS  Google Scholar 

  • Wu G, Lewis DR, Spalding EP. Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell. 2007;19:1826–37.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yamamoto M, Yamamoto KT. Differential effects of 1-naphthaleneacetic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid on the gravitropic response of roots in an auxin-resistant mutant of Arabidopsis, aux1. Plant Cell Physiol. 1998;39:660–4.

    PubMed  CAS  Google Scholar 

  • Yang S, Hoffman N. Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol. 1984;35:155–89.

    CAS  Google Scholar 

  • Zadnikova P, Petrasek J, Marhavy P, Raz V, Vandenbussche F, Ding Z, Schwarzerova K, Morita MT, Tasaka M, Hejatko J, Van Der Straeten D, Friml J, Benkova E. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development. 2010;137:607–17.

    PubMed  CAS  Google Scholar 

  • Zazimalova E, Murphy AS, Yang HB, Hoyerova K, Hosek P. Auxin transporters—why so many? Cold Spring Harb Perspect Biol. 2010;2:a00152.

    Google Scholar 

  • Zhang YJ, Lynch JP, Brown KM. Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot. 2003;54:2351–61.

    PubMed  CAS  Google Scholar 

  • Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science. 2001;291:306–9.

    PubMed  CAS  Google Scholar 

  • Zheng Z, Guo Y, Novak O, Dai X, Zhao Y, Ljung K, Noel JP, Chory J. Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol. 2013;9:244–46.

    Google Scholar 

  • Zobel RW. Some physiological characteristics of the ethylene-requiring tomato mutant diageotropica. Plant Physiol. 1973;52:385–9.

    PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by grants to GKM from the United States Department of Agriculture National Institute of Food and Agriculture program (2009-65116-20436) and from the National Science Foundation (NSF) Arabidopsis 2010 Program (IOB-0820717). The NSF Major Research Instrumentation Program supported the purchase of the LSCM used to generate the confocal images used in the figures in this article (Grant number MRI-0722926).

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  1. Department of Biology, Wake Forest University, Winston-Salem, NC, 27106, USA

    Gloria K. Muday, Gregory S. Maloney & Daniel R. Lewis

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Correspondence to Gloria K. Muday .

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  1. Inst. of Plant Physiology and Ecology, National Key Laboratory of Plant Molecular Genetics, Shanghai Inst. for Biological Sciences Chinese Academy of Sciences, Shanghai, China

    Chi-Kuang Wen

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Muday, G.K., Maloney, G.S., Lewis, D.R. (2015). Integration of Ethylene and Auxin Signaling and the Developmental Consequences of Their Crosstalk. In: Wen, CK. (eds) Ethylene in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9484-8_10

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