Skip to main content
SpringerLink
Log in

Involvement of secondary messengers and small organic molecules in auxin perception and signaling

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Auxin is a major phytohormone involved in most aspects of plant growth and development. Generally, auxin is perceived by three distinct receptors: TRANSPORT INHIBITOR RESISTANT1-Auxin/INDOLE ACETIC ACID, S-Phase Kinase-Associated Protein 2A and AUXIN-BINDING PROTEIN1. The auxin perception is regulated by a variety of secondary messenger molecules, including nitric oxide, reactive oxygen species, calcium, cyclic GMP, cyclic AMP, inositol triphosphate, diacylglycerol and by physiological pH. In addition, some small organic molecules, including inositol hexakisphosphate, yokonolide B, p-chlorophenoxyisobutyric acid, toyocamycin and terfestatin A, are involved in auxin signaling. In this review, we summarize and discuss the recent progress in understanding the functions of these secondary messengers and small organic molecules, which are now thoroughly demonstrated to be pervasive and important in auxin perception and signal transduction.

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

Fig. 1

Similar content being viewed by others

References

  • Andreeva Z, Barton D, Armour WJ, Li MY, Liao LF, McKellar HL, Pethybridge KA, Marc J (2010) Inhibition of phospholipase C disrupts cytoskeletal organization and gravitropic growth in Arabidopsis roots. Planta 232:1263–1279

    CAS  PubMed  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391

    PubMed Central  CAS  PubMed  Google Scholar 

  • Beavo JA, Brunton LL (2002) Cyclic nucleotide research—still expanding after half a century. Nat Rev Mol Cell Biol 3:710–718

    CAS  PubMed  Google Scholar 

  • Blomster T, Salojarvi J, Sipari N, Brosche M, Ahlfors R, Keinanen M, Overmyer K, Kangasjarvi J (2011) Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol 157:1866–1883

    PubMed Central  CAS  PubMed  Google Scholar 

  • Calderon Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L, Sheard LB, Tan X, Parry G, Mao H, Zheng N, Napier R, Kepinski S, Estelle M (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8:477–485

    CAS  PubMed  Google Scholar 

  • Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249:187–195

    CAS  PubMed  Google Scholar 

  • Cheng YF, Dai XH, Zhao Y (2004) AtCAND1, a HEAT-repeat protein that participates in auxin signaling in arabidopsis. Plant Physiol 135:1020–1026

    PubMed Central  CAS  PubMed  Google Scholar 

  • Choi Y, Lee Y, Kim SY, Lee Y, Hwang JU (2013) Arabidopsis ROP-interactive CRIB motif-containing protein 1 (RIC1) positively regulates auxin signalling and negatively regulates abscisic acid (ABA) signalling during root development. Plant Cell Environ 36:945–955

    CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    CAS  PubMed  Google Scholar 

  • Cousson A (2003) Two potential Ca(2+)-mobilizing processes depend on the abscisic acid concentration and growth temperature in the Arabidopsis stomatal guard cell. J Plant Physiol 160:493–501

    CAS  PubMed  Google Scholar 

  • Cousson A (2010) Indolyl-3-butyric acid-induced Arabidopsis stomatal opening mediated by 3′,5′-cyclic guanosine-monophosphate. Plant Physiol Bioch 48:977–986

    CAS  Google Scholar 

  • Dechant R, Binda M, Lee SS, Pelet S, Winderickx J, Peter M (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J 29:2515–2526

    PubMed Central  CAS  PubMed  Google Scholar 

  • del Pozo JC, Estelle M (2000) F-box proteins and protein degradation: an emerging theme in cellular regulation. Plant Mol Biol 44:123–128

    PubMed  Google Scholar 

  • del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057–3071

    PubMed Central  PubMed  Google Scholar 

  • del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–2235

    PubMed Central  PubMed  Google Scholar 

  • Delage E, Puyaubert J, Zachowski A, Ruelland E (2013) Signal transduction pathways involving phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: convergences and divergences among eukaryotic kingdoms. Prog Lipid Res 52:1–14

    CAS  PubMed  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    CAS  PubMed  Google Scholar 

  • DePaoli HC, Brito MS, Quiapim AC, Teixeira SP, Goldman GH, Dornelas MC, Goldman MH (2011) Stigma/style cell cycle inhibitor 1 (SCI1), a tissue-specific cell cycle regulator that controls upper pistil development. New Phytol 190:882–895

    CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    CAS  PubMed  Google Scholar 

  • Dong Z, Jin W (2013) Pleiotropic effects of ZmLAZY1 on the auxin-mediated responses to gravity and light in maize shoot and inflorescences. Plant Signal Behav 8:e27452

    PubMed Central  PubMed  Google Scholar 

  • Du L, Poovaiah BW (2005) Ca2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745

    CAS  PubMed  Google Scholar 

  • Frescas D, Pagano M (2008) Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer 8:438–449

    PubMed Central  CAS  PubMed  Google Scholar 

  • Galon Y, Snir O, Fromm H (2010) How calmodulin binding transcription activators (CAMTAs) mediate auxin responses. Plant Signal Behav 5:1311–1314

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gazarian IG, Lagrimini LM (1998) Anaerobic stopped-flow studies of indole-3-acetic acid oxidation by dioxygen catalysed by horseradish C and anionic tobacco peroxidase at neutral pH: catalase effect. Biophys Chem 72:231–237

    CAS  PubMed  Google Scholar 

  • Gehring CA, Irving HR, Parish RW (1990) Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proc Natl Acad Sci USA 87:9645–9649

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ, Hagen G (2012) Getting a grasp on domain III/IV responsible for Auxin Response Factor-IAA protein interactions. Plant Sci 190:82–88

    CAS  PubMed  Google Scholar 

  • Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505

    CAS  PubMed  Google Scholar 

  • Hashimoto K, Tsujita M, Miyazaki T, Kitamura K, Yamazaki M, Shin HS, Watanabe M, Sakimura K, Kano M (2011) Postsynaptic P/Q-type Ca2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum. Proc Natl Acad Sci USA 108:9987–9992

    PubMed Central  CAS  PubMed  Google Scholar 

  • Havens KA, Guseman JM, Jang SS, Pierre-Jerome E, Bolten N, Klavins E, Nemhauser JL (2012) A synthetic approach reveals extensive tunability of auxin signaling. Plant Physiol 160:135–142

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hayashi K, Jones AM, Ogino K, Yamazoe A, Oono Y, Inoguchi M, Kondo H, Nozaki H (2003) Yokonolide B, a novel inhibitor of auxin action, blocks degradation of AUX/IAA factors. J Biol Chem 278:23797–23806

    CAS  PubMed  Google Scholar 

  • Hayashi K, Yamazoe A, Ishibashi Y, Kusaka N, Oono Y, Nozaki H (2008) Active core structure of terfestatin A, a new specific inhibitor of auxin signaling. Bioorg Med Chem 16:5331–5344

    CAS  PubMed  Google Scholar 

  • Hayashi K, Kamio S, Oono Y, Townsend LB, Nozaki H (2009) Toyocamycin specifically inhibits auxin signaling mediated by SCFTIR1 pathway. Phytochemistry 70:190–197

    CAS  PubMed  Google Scholar 

  • Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ichikawa T, Suzuki Y, Czaja I, Schommer C, Lessnick A, Schell J, Walden R (1997) Identification and role of adenylyl cyclase in auxin signalling in higher plants. Nature 390:698–701

    CAS  PubMed  Google Scholar 

  • Iglesias MJ, Terrile MC, Bartoli CG, D’Ippolito S, Casalongue CA (2010) Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol 74:215–222

    CAS  PubMed  Google Scholar 

  • Isner JC, Nuhse T, Maathuis FJ (2012) The cyclic nucleotide cGMP is involved in plant hormone signalling and alters phosphorylation of Arabidopsis thaliana root proteins. J Exp Bot 63:3199–3205

    PubMed Central  CAS  PubMed  Google Scholar 

  • Isom DG, Sridharan V, Baker R, Clement ST, Smalley DM, Dohlman HG (2013) Protons as second messenger regulators of G protein signaling. Mol Cell 51:531–538

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jiao Y, Sun L, Song Y, Wang L, Liu L, Zhang L, Liu B, Li N, Miao C, Hao F (2013) AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. J Exp Bot 64:4183–4192

    CAS  PubMed  Google Scholar 

  • Jones AM, Venis MA (1989) Photoaffinity labeling of indole-3-acetic acid-binding proteins in maize. Proc Natl Acad Sci USA 86:6153–6156

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jurado S, Trivino SD, Abraham Z, Manzano C, Gutierrez C, Del Pozo C (2008) SKP2A protein, an F-box that regulates cell division, is degraded via the ubiquitin pathway. Plant Signal Behav 3:810–812

    PubMed Central  PubMed  Google Scholar 

  • Jurado S, Abraham Z, Manzano C, Lopez-Torrejon G, Pacios LF, Del Pozo JC (2010) The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell 22:3891–3904

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kang B, Zhang Z, Wang L, Zheng L, Mao W, Li M, Wu Y, Wu P, Mo X (2013) OsCYP2, a chaperone involved in degradation of auxin-responsive proteins, plays crucial roles in rice lateral root initiation. Plant J 74:86–97

    CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    CAS  PubMed  Google Scholar 

  • Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lager I, Andreasson O, Dunbar TL, Andreasson E, Escobar MA, Rasmusson AG (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant Cell Environ 33:1513–1528

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lavy M, Prigge MJ, Tigyi K, Estelle M (2012) The cyclophilin DIAGEOTROPICA has a conserved role in auxin signaling. Development 139:1115–1124

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee DS, Kim BK, Kwon SJ, Jin HC, Park OK (2009) Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling. Biochem Biophys Res Commun 379:1038–1042

    CAS  PubMed  Google Scholar 

  • Li J, Jia H (2013) Hydrogen peroxide is involved in cGMP modulating the lateral root development of Arabidopsis thaliana. Plant Signal Behav 8:8

    Google Scholar 

  • Li H, Kundu TK, Zweier JL (2009) Characterization of the magnitude and mechanism of aldehyde oxidase-mediated nitric oxide production from nitrite. J Biol Chem 284:33850–33858

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lobler M, Klambt D (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). II. Localization of a putative auxin receptor. J Biol Chem 260:9854–9859

    CAS  PubMed  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    PubMed Central  PubMed  Google Scholar 

  • Long JA, Woody S, Poethig S, Meyerowitz EM, Barton K (2002) Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129:2797–2806

    CAS  PubMed  Google Scholar 

  • Ma Q, Robert S (2014) Auxin biology revealed by small molecules. Physiol Plant 151:25–42

    CAS  PubMed  Google Scholar 

  • Mangeon A, Bell EM, Lin WC, Jablonska B, Springer PS (2011) Misregulation of the LOB domain gene DDA1 suggests possible functions in auxin signalling and photomorphogenesis. J Exp Bot 62:221–233

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    CAS  PubMed  Google Scholar 

  • Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001

    PubMed Central  CAS  PubMed  Google Scholar 

  • Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341–2356

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mosblech A, Thurow C, Gatz C, Feussner I, Heilmann I (2011) Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J 65:949–957

    CAS  PubMed  Google Scholar 

  • Munnik T, Irvine RF, Musgrave A (1998) Phospholipid signalling in plants. Biochim Biophys Acta 1389:222–272

    CAS  PubMed  Google Scholar 

  • Nakamura A, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S (2006) Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type. Plant J 45:193–205

    CAS  PubMed  Google Scholar 

  • Nan W, Wang X, Yang L, Hu Y, Wei Y, Liang X, Mao L, Bi Y (2014) Cyclic GMP is involved in auxin signalling during Arabidopsis root growth and development. J Exp Bot 65:1571–1583

    PubMed Central  CAS  PubMed  Google Scholar 

  • Napier RM, David KM, Perrot-Rechenmann C (2002) A short history of auxin-binding proteins. Plant Mol Biol 49:339–348

    CAS  PubMed  Google Scholar 

  • Ohto MA, Hayashi S, Sawa S, Hashimoto-Ohta A, Nakamura K (2006) Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. Plant Cell Physiol 47:1603–1611

    CAS  PubMed  Google Scholar 

  • Oono Y, Ooura C, Rahman A, Aspuria ET, Hayashi K, Tanaka A, Uchimiya H (2003) p-Chlorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiol 133:1135–1147

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    PubMed Central  CAS  PubMed  Google Scholar 

  • Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peer WA, Jenness MK, Murphy AS (2014) Measure for measure: determining, inferring and guessing auxin gradients at the root tip. Physiol Plant 151:97–111

    CAS  PubMed  Google Scholar 

  • Perera IY, Hung CY, Brady S, Muday GK, Boss WF (2006) A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol 140:746–760

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peters C, Kim SC, Devaiah S, Li M, Wang X (2014) Non-specific phospholipase C5 and diacylglycerol promote lateral root development under mild salt stress in Arabidopsis. Plant Cell Environ 37:2002–2013

    CAS  PubMed  Google Scholar 

  • Poovaiah BW, Reddy AS (1993) Calcium and signal transduction in plants. Crit Rev Plant Sci 12:185–211

    CAS  PubMed  Google Scholar 

  • Ren H, Santner A, del Pozo JC, Murray JA, Estelle M (2008) Degradation of the cyclin-dependent kinase inhibitor KRP1 is regulated by two different ubiquitin E3 ligases. Plant J 53:705–716

    CAS  PubMed  Google Scholar 

  • Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12:198–207

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sauer M, Kleine-Vehn J (2011) AUXIN BINDING PROTEIN1: the outsider. Plant Cell 23:2033–2043

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sauer M, Robert S, Kleine-Vehn J (2013) Auxin: simply complicated. J Exp Bot 64:2565–2577

    CAS  PubMed  Google Scholar 

  • Scherer GF (2002) Secondary messengers and phospholipase A2 in auxin signal transduction. Plant Mol Biol 49:357–372

    CAS  PubMed  Google Scholar 

  • Scherer GF (2011) AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J Exp Bot 62:3339–3357

    CAS  PubMed  Google Scholar 

  • Simon S, Petrasek J (2011) Why plants need more than one type of auxin. Plant Sci 180:454–460

    CAS  PubMed  Google Scholar 

  • Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57:4059–4070

    CAS  PubMed  Google Scholar 

  • Spartz AK, Gray WM (2008) Plant hormone receptors: new perceptions. Genes Dev 22:2139–2148

    PubMed Central  CAS  PubMed  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    CAS  PubMed  Google Scholar 

  • Tamas L, Bocova B, Huttova J, Liptakova L, Mistrik I, Valentovicova K, Zelinova V (2012) Impact of the auxin signaling inhibitor p-chlorophenoxyisobutyric acid on short-term Cd-induced hydrogen peroxide production and growth response in barley root tip. J Plant Physiol 169:1375–1381

    CAS  PubMed  Google Scholar 

  • Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    CAS  PubMed  Google Scholar 

  • Tanimoto M, Jowett J, Stirnberg P, Rouse D, Leyser O (2007) pa1–1 partially suppresses gain-of-function mutations in Arabidopsis AXR3/IAA17. BMC Plant Biol 7:20

    PubMed Central  PubMed  Google Scholar 

  • Terrile MC, Paris R, Calderon-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongue CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tian H, Klambt D, Jones AM (1995) Auxin-binding protein 1 does not bind auxin within the endoplasmic reticulum despite this being the predominant subcellular location for this hormone receptor. J Biol Chem 270:26962–26969

    CAS  PubMed  Google Scholar 

  • Torres MA (2010) ROS in biotic interactions. Physiol Plant 138:414–429

    CAS  PubMed  Google Scholar 

  • Trewavas AJ (1997) Plant cyclic AMP comes in from the cold. Nature 390:657–658

    CAS  PubMed  Google Scholar 

  • Tromas A, Paque S, Stierle V, Quettier AL, Muller P, Lechner E, Genschik P, Perrot-Rechenmann C (2013) Auxin-Binding Protein 1 is a negative regulator of the SCFTIR1/AFB pathway. Nat Commun 4:2496

    PubMed  Google Scholar 

  • Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3:525–536

    PubMed Central  PubMed  Google Scholar 

  • Wang R, Estelle M (2014) Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Curr Opin Plant Biol 21C:51–58

    Google Scholar 

  • Wen R, Wang S, Xiang D, Venglat P, Shi X, Zang Y, Datla R, Xiao W, Wang H (2014) UBC13, an E2 enzyme for Lys63-linked ubiquitination, functions in root development by affecting auxin signaling and Aux/IAA protein stability. Plant J 80:424–436

    CAS  PubMed  Google Scholar 

  • Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence responses. Curr Opin Plant Biol 7:449–455

    CAS  PubMed  Google Scholar 

  • Wimalasekera R, Pejchar P, Holk A, Martinec J, Scherer GF (2010) Plant phosphatidylcholine-hydrolyzing phospholipases C NPC3 and NPC4 with roles in root development and brassinolide signaling in Arabidopsis thaliana. Mol Plant 3:610–625

    CAS  PubMed  Google Scholar 

  • Wu M, Wang F, Zhang C, Xie Y, Han B, Huang J, Shen W (2013) Heme oxygenase-1 is involved in nitric oxide- and cGMP-induced alpha-Amy2/54 gene expression in GA-treated wheat aleurone layers. Plant Mol Biol 81:27–40

    CAS  PubMed  Google Scholar 

  • Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusova H, Wang W, Jones AM, Friml J, Patterson SE, Bleecker AB, Yang Z (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025–1028

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xuan W, Xu S, Li M, Han B, Zhang B, Zhang J, Lin Y, Huang J, Shen W, Cui J (2012) Nitric oxide is involved in hemin-induced cucumber adventitious rooting process. J Plant Physiol 169:1032–1039

    CAS  PubMed  Google Scholar 

  • Yamazoe A, Hayashi K, Kepinski S, Leyser O, Nozaki H (2005) Characterization of terfestatin A, a new specific inhibitor for auxin signaling. Plant Physiol 139:779–789

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang T, Poovaiah BW (2000) An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death. J Biol Chem 275:38467–38473

    CAS  PubMed  Google Scholar 

  • Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127

    CAS  PubMed  Google Scholar 

  • Yang F, Song Y, Yang H, Liu Z, Zhu G, Yang Y (2014) An auxin-responsive endogenous peptide regulates root development in Arabidopsis. J Integr Plant Biol 56:635–647

    CAS  PubMed  Google Scholar 

  • Zhang X, Dai Y, Xiong Y, DeFraia C, Li J, Dong X, Mou Z (2007) Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J 52:1066–1079

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Chinese National Science Foundation (31030045 and 31371431) and the Fundamental Research Funds for the Central Universities (223000-861123).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

    Authors and Affiliations

    1. Institute of Cell Biology, School of Life Sciences, Lanzhou University, Lanzhou, 73000, China

      Dong-Wei Di & Guang-Qin Guo

    2. Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO, 80045, USA

      Caiguo Zhang

    Authors
    1. Dong-Wei Di
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Caiguo Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Guang-Qin Guo
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Dong-Wei Di.

    Additional information

    Communicated by N. Stewart.

    D.-W. Di and C. Zhang contribute equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Di, DW., Zhang, C. & Guo, GQ. Involvement of secondary messengers and small organic molecules in auxin perception and signaling. Plant Cell Rep 34, 895–904 (2015). https://doi.org/10.1007/s00299-015-1767-z

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00299-015-1767-z

    Keywords

    Search

    Navigation