Skip to main content

The Role of Auxin in Root-Symbiont and Root-Pathogen Interactions: From Development to Defense

  • Chapter
  • First Online:
Progress in Botany 71

Part of the book series: Progress in Botany ((BOTANY,volume 71))

Abstract

Plants live in constant contact with microorganisms, many of which have profound effects on the growth and development of plant hosts. The plant hormone auxin regulates cell enlargement, cell division, and organogenesis, and is therefore a likely target for microorganisms that manipulate plants. In context of this chapter, the term microorganisms will be used to include bacteria, fungi, nematodes, and protozoans. Many microorganisms can synthesize auxin themselves. Others produce specific signals that indirectly alter the plant auxin balance, for example, through effects on auxin transport, metabolism, or signaling. This chapter highlights plant–microorganism interactions, in which auxin is targeted by symbionts and pathogens to manipulate the development of their plant host. Auxin signaling is also necessary for the regulation of plant defense responses against pathogens, and downregulation of auxin signaling has emerged as a strategy of plants to inhibit pathogen infection. Thus, the regulation of auxin signaling is a balancing act between influences of both the plant and the microbial partner. One future challenge will be to identify the microbial signal molecules that regulate the plant auxin balance, and to find out how the plant integrates the perception of several of these signals at the same time.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aloni R (2004) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer, Dordrecht, pp 471–492

    Google Scholar 

  • Aloni R, Pradel KS, Ullrich CI (1995) The three-dimensional structure of vascular tissues in Agrobacterium tumefaciens-induced crown galls and in the host stems of Ricinus communis L. Planta 196:597–605

    CAS  Google Scholar 

  • Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080

    PubMed  CAS  Google Scholar 

  • Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073–2076

    PubMed  CAS  Google Scholar 

  • Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends Plant Sci 11:217–223

    PubMed  CAS  Google Scholar 

  • Balasubramanian M, Rangaswami G (1962) Presence of indole compounds in nematode galls. Nature 194:774–775

    CAS  Google Scholar 

  • Barash I, Manulis-Sasson S (2007) Virulence mechanisms and host specificity of gall-forming Pantoea agglomerans. Trends Microbiol 15:538–545

    PubMed  CAS  Google Scholar 

  • Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154

    PubMed  CAS  Google Scholar 

  • Barker SJ, Tagu D, Delp G (1998) Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol 116:1201–1207

    CAS  Google Scholar 

  • Bauer WD, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Bernasconi P (1996) Effect of synthetic and natural protein tyrosine kinase inhibitors on auxin efflux in zucchini (Cucurbita pepo) hypocotyls. Physiol Plant 96:205–210

    CAS  Google Scholar 

  • Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631

    Google Scholar 

  • Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34:1709–1715

    CAS  Google Scholar 

  • Boot KJM, van Brussel AAN, Tak T, Spaink HP, Kijne JW (1999) Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp nigra roots. Mol Plant Microbe Interact 12:839–844

    CAS  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    PubMed  CAS  Google Scholar 

  • Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140:1384–1396

    PubMed  CAS  Google Scholar 

  • Burg SP, Burg EA (1966) The interaction between auxin and ethylene and its role in plant growth. Am J Bot 55:262

    Google Scholar 

  • Caetano-Anollés G, Gresshoff PM (1991) Plant genetic control of nodulation. Annu Rev Microbiol 45:345–382

    PubMed  Google Scholar 

  • Campanella JJ, Smith SM, Leibu D, Wexler S, Ludwig-Müller J (2008) The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts. J Plant Growth Regul 27:26–38

    CAS  Google Scholar 

  • Chalupowicz L, Barash I, Schwartz M, Aloni R, Manulis S (2006) Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity. Planta 224:429–437

    PubMed  CAS  Google Scholar 

  • Chen ZY, Agnew JL, Cohen JD, He P, Shan LB, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    PubMed  CAS  Google Scholar 

  • Clark E, Manulis S, Ophir Y, Barash I, Gafni Y (1993) Cloning and Characterization of iaaM and iaaH from Erwinia herbicola pathovar gypsophilae. Phytopathology 83:234–240

    CAS  Google Scholar 

  • Coenen C, Lomax TL (1997) Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends Plant Sci 2:351–356

    PubMed  CAS  Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-assotiated bacteria. Crit Rev Microbiol 21:1–18

    PubMed  Google Scholar 

  • Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Physiol Mol Plant Pathol 49:1–20

    CAS  Google Scholar 

  • de Almeida-Engler J, De Vleesschauwer V, Burssens S, Celenza JL, Inzé D, Van Montague M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncythia. Plant Cell 11:793–807

    PubMed  Google Scholar 

  • de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14:267–277

    PubMed  Google Scholar 

  • Depuydt S, Dolezal K, Van Lijsebettens M, Moritz T, Holsters M, Vereecke D (2008) Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol 146:1267–1281

    PubMed  CAS  Google Scholar 

  • Devos S, Laukens K, Deckers P, Van der Straeten D, Beeckman T, Inzé D, Van Onckelen H, Witters E, Prinsen E (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Mol Plant Microbe Interact 19:1431–1443

    PubMed  CAS  Google Scholar 

  • Devos S, Vissenberg K, Verbelen JP, Prinsen E (2005) Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance. New Phytol 166:241–250

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    PubMed  CAS  Google Scholar 

  • Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J, Paciorek T, Petrasek J, Seifertova D, Tejos R, Meisel LA, Zazimalova E, Gadella TWJ, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci USA 105:4489–4494

    PubMed  CAS  Google Scholar 

  • Ding XH, Cao YL, Huang LL, Zhao J, Xu CG, Li XH, Wang SP (2008) Activation of the indole-3-acetic acid-amido synthetase GH3–8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240

    PubMed  CAS  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164

    CAS  Google Scholar 

  • Doyle EA, Lambert KN (2003) Meloidogyne javanica chorismate mutase 1 alters plant cell development. Mol Plant Microbe Interact 16:123–131

    PubMed  CAS  Google Scholar 

  • Escobar MA, Dandekar AM (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 8:380–386

    PubMed  CAS  Google Scholar 

  • Fedorova EE, Zhiznevskaya GY, Kalibernaya ZV, Artemenko EN, Izmailov SF, Gus'kov AV (2000) IAA metabolism during development of symbiosis between Phaseolus vulgaris and Rhizobium phaseoli. Russ J Plant Physiol 47:203–206

    CAS  Google Scholar 

  • Foucher F, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43:773–786

    PubMed  CAS  Google Scholar 

  • Friml J (2003) Auxin transport – shaping the plant. Curr Opin Plant Biol 6:7–12

    PubMed  CAS  Google Scholar 

  • Fritze D, Wiepning A, Kaldorf M, Ludwig-Müller J (2005) Auxins in the development of an arbuscular mycorrhizal symbiosis in maize. J Plant Physiol 162:1210–1219

    Google Scholar 

  • Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137

    PubMed  CAS  Google Scholar 

  • Gamalero E, Berta G, Massa N, Glick BR, Lingua G (2008) Synergistic interactions between the ACC deaminase-producing bacterium Pseudomonas putida UW4 and the AM fungus Gigaspora rosea positively affect cucumber plant growth. FEMS Microbiol Ecol 64:459–467

    PubMed  CAS  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejenda KFK, Smith AP, Baroux C, Grossniklaus U, Müller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194

    PubMed  CAS  Google Scholar 

  • Gelvin SB (1990) Crown gall disease and hairy root disease – a sledgehammer and a tackhammer. Plant Physiol 92:281–285

    PubMed  CAS  Google Scholar 

  • Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219

    PubMed  CAS  Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    PubMed  Google Scholar 

  • Goethals K, Vereecke D, Jaziri M, Van Montagu M, Holsters M (2001) Leafy gall formation by Rhodococcus fascians. Annu Rev Phytopathol 39:27–52

    PubMed  CAS  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    PubMed  CAS  Google Scholar 

  • Goverse A, Engler JD, Verhees J, van der Krol S, Helder J, Gheysen G (2000a) Cell cycle activation by plant parasitic nematodes. Plant Mol Biol 43:747–761

    PubMed  CAS  Google Scholar 

  • Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000b) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129

    PubMed  CAS  Google Scholar 

  • Gravel V, Antoun H, Tweddell RJ (2007) Effect of indole-acetic acid (IAA) on the development of symptoms caused by Pythium ultimum on tomato plants. Eur J Plant Pathol 119:457–462

    CAS  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    PubMed  CAS  Google Scholar 

  • Gray WM, Muskett PR, Chuang HW, Parker JE (2003) Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15:1310–1319

    PubMed  CAS  Google Scholar 

  • Grsic-Rausch S, Kobelt P, Siemens JM, Bischoff M, Ludwig-Müller J (2000) Expression and localization of nitrilase during symptom development of the clubroot disease in Arabidopsis. Plant Physiol 122:369–378

    PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2001) Auxin response factors. J Plant Growth Regul 20:281–291

    CAS  Google Scholar 

  • Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80:695–720

    CAS  Google Scholar 

  • Hao YU, Charles TC, Glick BR (2007) ACC deaminase from plant growth-promoting bacteria affects crown gall development. Can J Microbiol 53:1291–1299

    PubMed  CAS  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    PubMed  CAS  Google Scholar 

  • Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6:643–654

    CAS  Google Scholar 

  • Hermsmeier D, Mazarei M, Baum TJ (1998) Differential display analysis of the early compatible interaction between soybean and the soybean cyst nematode. Mol Plant Microbe Interact 11:1258–1263

    CAS  Google Scholar 

  • Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122:211–237

    Google Scholar 

  • Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86:1244–1248

    PubMed  CAS  Google Scholar 

  • Hirsch AM, Fang Y, Asad S, Kapulnik Y (1997) The role of phytohormones in plant-microbe symbioses. Plant Soil 194:171–184

    CAS  Google Scholar 

  • Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium-legume symbiosis. Fungal Genet Biol 23:205–212

    PubMed  CAS  Google Scholar 

  • Huang YC, Chang YL, Hsu JJ, Chuang HW (2008) Transcriptome analysis of auxin-regulated genes of Arabidopsis thaliana. Gene 420:118–124

    PubMed  CAS  Google Scholar 

  • Huo XY, Schnabel E, Hughes K, Frugoli J (2006) RNAi phenotypes and the localization of a protein :: GUS fusion imply a role for Medicago truncatula PIN genes in nodulation. J Plant Growth Regul 25:156–165

    PubMed  CAS  Google Scholar 

  • Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Aust J Plant Physiol 26:221–231

    CAS  Google Scholar 

  • Ingram DS, Tommerup IC (1972) Life-history of Plasmodiophora brassicae Woron. Proc R Soc Lond B 180:103–112

    Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007a) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant Microbe Interact 20:293–305

    PubMed  CAS  Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007b) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20:510–525

    PubMed  CAS  Google Scholar 

  • Jacobs M, Rubery PH (1988) Naturally-occurring auxin transport regulators. Science 241:346–349

    PubMed  CAS  Google Scholar 

  • Jameson PE (2000) Cytokinins and auxins in plant-pathogen interactions – an overview. Plant Growth Regul 32:369–380

    CAS  Google Scholar 

  • Jentschel K, Thiel D, Rehn F, Ludwig-Müller J (2007) Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiol Plant 129:320–333

    CAS  Google Scholar 

  • Jones AM (1998) Auxin transport: down and out and up again. Science 282:2201–2202

    PubMed  CAS  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    PubMed  CAS  Google Scholar 

  • Jones JT, Furlanetto C, Phillips MS (2007) The role of flavonoids produced in response to cyst nematode infection of Arabidopsis thaliana. Nematology 9:671–677

    CAS  Google Scholar 

  • Kaldorf M, Ludwig-Müller J (2000) AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis. Physiol Plant 109:58–67

    CAS  Google Scholar 

  • Karczmarek A, Overmars H, Helder J, Goverse A (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 5:343–346

    PubMed  CAS  Google Scholar 

  • Kefford NP, Brockwell J, Zwar JA (1960) The symbiotic synthesis of auxin by legumes and nodule bacteria and its role in nodule development. Aust J Biol Sci 13:456–467

    CAS  Google Scholar 

  • Kepinski S, Leyser O (2003) Plant development – an axis of auxin. Nature 426:132–135

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007) A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode) infection. Planta 226:1423–1447

    PubMed  CAS  Google Scholar 

  • Koltai H, Dhandaydham M, Opperman C, Thomas J, Bird D (2001) Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont. Mol Plant Microbe Interact 14:1168–1177

    PubMed  CAS  Google Scholar 

  • Libbenga KR, van Iren F, Bogers RJ, Schraag-Lamers MF (1973) The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114:29–39

    CAS  Google Scholar 

  • Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474

    PubMed  CAS  Google Scholar 

  • Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Nonmanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104

    PubMed  CAS  Google Scholar 

  • Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272

    PubMed  CAS  Google Scholar 

  • Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J 38:203–214

    PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Campos-Cuevas JC, Hernandez-Calderon E, Velasquez-Becerra C, Farias-Rodriguez R, Macias-Rodriguez LI, Valencia-Cantero E (2007) Bacillus megatenum rhizobacteria promote growth and alter root-system architecture through an auxin-and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217

    PubMed  CAS  Google Scholar 

  • Lopez MA, Bannenberg G, Castresana C (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr Opin Plant Biol 11:420–427

    PubMed  CAS  Google Scholar 

  • Ludwig-Müller J, Bendel U, Thermann P, Ruppel M, Epstein E, Hilgenberg W (1993) Concentrations of indole-3-acetic-acid in plants of tolerant and susceptible varieties of Chinese-cabbage infected with Plasmodiophora brassicae Woron. New Phytol 125:763–769

    Google Scholar 

  • Ludwig-Müller J, Pieper K, Ruppel M, Cohen JD, Epstein E, Kiddle G, Bennett R (1999) Indole glucosinolate and auxin biosynthesis in Arabidopsis thaliana (L.) Heynh. glucosinolate mutants and the development of clubroot disease. Planta 208:409–419

    PubMed  Google Scholar 

  • Ludwig-Müller J, Schuller A (2008) What can we learn from clubroots: alterations in host roots and hormone homeostasis caused by Plasmodiophora brassicae. Eur J Plant Pathol 121:291–302

    Google Scholar 

  • Manulis S, Haviv-Chesner A, Brandl MT, Lindow SE, Barash I (1998) Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol Plant Microbe Interact 11:634–642

    PubMed  CAS  Google Scholar 

  • Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J Exp Bot 52:419–426

    PubMed  CAS  Google Scholar 

  • Mathesius U (2008) Auxin – at the root of nodule development? Funct Plant Biol 35:651–668

    CAS  Google Scholar 

  • Mathesius U, Bayliss C, Weinman JJ, Schlaman HRM, Spaink HP, Rolfe BG, McCully ME, Djordjevic MA (1998a) Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover. Mol Plant Microbe Interact 11:1223–1232

    CAS  Google Scholar 

  • Mathesius U, Mulders S, Gao MS, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449

    PubMed  CAS  Google Scholar 

  • Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998b) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    PubMed  CAS  Google Scholar 

  • Mayda E, Marques C, Conejero V, Vera P (2000) Expression of a pathogen-induced gene can be mimicked by auxin insensitivity. Mol Plant Microbe Interact 13:23–31

    PubMed  CAS  Google Scholar 

  • Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530

    PubMed  CAS  Google Scholar 

  • Mitchell EK, Davies PJ (1975) Evidence for three different systems of movement of indoleacetic-acid in intact roots of Phaseolus coccineus. Physiol Plant 33:290–294

    CAS  Google Scholar 

  • Mitchum MG, Wang XH, Davis EL (2008) Diverse and conserved roles of CLE peptides. Curr Opin Plant Biol 11:75–81

    PubMed  CAS  Google Scholar 

  • Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138

    PubMed  CAS  Google Scholar 

  • Morgan PW, Gausman HW (1966) Effects of ethylene on auxin transport. Plant Physiol 41:45–52

    PubMed  CAS  Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542

    PubMed  CAS  Google Scholar 

  • Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324

    PubMed  CAS  Google Scholar 

  • Murphy A, Taiz L (1999) Localization and characterization of soluble and plasma membrane aminopeptidase activities in Arabidopsis seedlings. Plant Physiol Biochem 37:431–443

    CAS  Google Scholar 

  • Murphy AS, Hoogner KR, Peer WA, Taiz L (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol 128:935–950

    PubMed  CAS  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104

    PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    PubMed  CAS  Google Scholar 

  • Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454

    PubMed  CAS  Google Scholar 

  • Olah B, Briere C, Becard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207

    PubMed  CAS  Google Scholar 

  • Oldroyd GED, Downie JM (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    PubMed  CAS  Google Scholar 

  • Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J (2008) N-acyl-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509

    PubMed  CAS  Google Scholar 

  • Pacios-Bras C, Schlaman HRM, Boot K, Admiraal P, Langerak JM, Stougaard J, Spaink HP (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol Biol 52:1169–1180

    PubMed  CAS  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis on indole-3-acetic acid. Can J Microbiol 42:207–220

    PubMed  CAS  Google Scholar 

  • Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913

    PubMed  CAS  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SI, Chen RJ, Masson PH, Murphy AS (2004) 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 16:1898–1911

    PubMed  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    PubMed  CAS  Google Scholar 

  • Peret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol 144:1852–1862

    PubMed  CAS  Google Scholar 

  • Persello-Cartieaux F, David P, Sarrobert C, Thibaud MC, Achouak W, Robaglia C, Nussaume L (2001) Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas. Planta 212:190–198

    PubMed  CAS  Google Scholar 

  • Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ 26:189–199

    CAS  Google Scholar 

  • Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    PubMed  CAS  Google Scholar 

  • Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7:21

    PubMed  Google Scholar 

  • Prayitno J, Rolfe BG, Mathesius U (2006) The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol 142:168–180

    PubMed  CAS  Google Scholar 

  • Rausch T, Butcher DN, Hilgenberg W (1983) Indole-3-methylglucosinolate biosynthesis and metabolism in clubroot diseased plants. Physiol Plant 58:93–100

    CAS  Google Scholar 

  • Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355

    PubMed  CAS  Google Scholar 

  • Rudawska ML, Kieliszewska-Rokicka B (1997) Mycorrhizal formation by Paxillus involutus strains in relation to their IAA-synthesizing activity. New Phytol 137:509–517

    CAS  Google Scholar 

  • Sanchez-Contreras M, Bauer WD, Gao MS, Robinson JB, Downie JA (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc B 362:1149–1163

    CAS  Google Scholar 

  • Scholl EH, Thorne JL, McCarter JP, Bird DM (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39

    PubMed  Google Scholar 

  • Schwalm K, Aloni R, Langhans M, Heller W, Stich S, Ullrich CI (2003) Flavonoid-related regulation of auxin accumulation in Agrobacterium tumefaciens-induced plant tumors. Planta 218:163–178

    PubMed  CAS  Google Scholar 

  • Sergeeva E, Liaimer A, Bergman B (2002) Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215:229–238

    PubMed  CAS  Google Scholar 

  • Sirrenberg A, Goebel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131:581–589

    PubMed  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    PubMed  CAS  Google Scholar 

  • Spoel SH, Dong XN (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351

    PubMed  CAS  Google Scholar 

  • Sprent JI, Sprent P (1990) Nitrogen fixing organisms: pure and applied aspects. Chapman and Hall, London

    Google Scholar 

  • Stacey G, Libault M, Brechenmacher L, Wan JR, May GD (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121

    PubMed  CAS  Google Scholar 

  • Stafford HA (1997) Roles of flavonoids in symbiotic and defense functions in legume roots. Bot Rev 63:27–39

    Google Scholar 

  • Stenlid G (1976) Effects of flavonoids on the polar transport of auxins. Physiol Plant 38:262–266

    CAS  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273

    PubMed  CAS  Google Scholar 

  • Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci 12:282–285

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, Yazaki K (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17:2922–2939

    PubMed  CAS  Google Scholar 

  • Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157 : H7. Plant J 46:34–53

    PubMed  CAS  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    PubMed  CAS  Google Scholar 

  • van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131

    PubMed  Google Scholar 

  • van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long distance auxin transport regulation in the Medicago truncatula super numerary nodules mutant. Plant Physiol 140:1494–1506

    PubMed  Google Scholar 

  • Vanneste S, Maes L, De Smet I, Himanen K, Naudts M, Inzé D, Beeckman T (2005) Auxin regulation of cell cycle and its role during lateral root initiation. Physiol Plant 123:139–146

    CAS  Google Scholar 

  • Vereecke D, Burssens S, Simon-Mateo C, Inzé D, Van Montagu M, Goethals K, Jaziri M (2000) The Rhodococcus fascians-plant interaction: morphological traits and biotechnological applications. Planta 210:241–251

    PubMed  CAS  Google Scholar 

  • Veselov D, Langhans M, Hartung W, Aloni R, Feussner I, Gotz C, Veselova S, Schlomski S, Dickler C, Bachmann K, Ullrich CI (2003) Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta 216:512–522

    PubMed  CAS  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168

    PubMed  CAS  Google Scholar 

  • von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482

    Google Scholar 

  • von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta. doi:10.1007/s00425-008-0811-4

    Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong XN (2007a) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

    PubMed  CAS  Google Scholar 

  • Wang XH, Mitchum MG, Gao BL, Li CY, Diab H, Baum TJ, Hussey RS, Davis EL (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 6:187–191

    PubMed  Google Scholar 

  • Wang XH, Replogle A, Davis EL, Mitchum MG (2007b) The tobacco Cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Mol Plant Pathol 8:423–436

    PubMed  CAS  Google Scholar 

  • Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18:1617–1629

    PubMed  CAS  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: Cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    PubMed  CAS  Google Scholar 

  • Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc Natl Acad Sci USA 102:3147–3152

    PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    PubMed  CAS  Google Scholar 

  • Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883–883

    PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    PubMed  CAS  Google Scholar 

  • Wu CW, Dickstein R, Cary AJ, Norris JH (1996) The auxin transport inhibitor N- (1-naphthyl) phthalamic acid elicits pseudonodules on nonnodulating mutants of white sweetclover. Plant Physiol 110:501–510

    PubMed  CAS  Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida CR12–2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71

    CAS  Google Scholar 

  • Xie Z-P, Müller J, Wiemken A, Broughton WJ, Boller T (1997) Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureum. New Phytol 139:361–366

    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

    PubMed  CAS  Google Scholar 

  • Yu PK, Viglierchio DR (1964) Plant growth substances and parasitic nematodes.1. Root knot nematodes and tomato. Exp Parasitol 15:242–248

    PubMed  CAS  Google Scholar 

  • Zhang ZQ, Li Q, Li ZM, Staswick PE, Wang MY, Zhu Y, He ZH (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145:450–464

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank the Australian Research Council (ARC) for funding through an Australian Research Fellowship (DP0557692) and through the ARC Centre of Excellence for Integrative Legume Research (CE0348212).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ulrike Mathesius .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Mathesius, U. (2010). The Role of Auxin in Root-Symbiont and Root-Pathogen Interactions: From Development to Defense. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 71. Progress in Botany, vol 71. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02167-1_8

Download citation

Publish with us

Policies and ethics