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Plant Immunity Induced by Oligogalacturonides Alters Root Growth in a Process Involving Flavonoid Accumulation in Arabidopsis thaliana

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Abstract

Plants adapt to challenging environmental factors by modulating morphogenetic processes. Although it has been speculated that activation of defense responses against pathogens leads to plant growth adjustment, little is known about developmental and architectural responses to defense stimulators. In this report we evaluated the activity of oligogalacturonides (OGs), a class of molecules directly involved in plant immunity, to modulate root system architecture in Arabidopsis thaliana. We show that OGs induce PAD3 expression and camalexin synthesis, two well-known markers of defense responses. These effects were related to primary root growth inhibition and increased lateral root and root hair formation, which are reminiscent of altered auxin responses. Cellular analysis showed that the effect of these compounds on primary root growth was due to changes in cell elongation and increased flavonoid accumulation at the root elongation region. Moreover, the observations that similar changes in primary root growth were induced by naphthylphthalamic acid supply and that auxin- or flavonoid-related mutants tir1, doc1, pgp1, pgp4, pgp19, and tt4-1 show differential responses to primary root growth inhibition by OGs suggest that auxin homeostasis plays a role in the oligogalacturonide-induced alteration of root cell patterning. Our results suggest that OGs might play a dual function in adaptation of plants to pathogen challenge by inducing defense responses and plant architecture adjustment.

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References

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826

    Article  CAS  PubMed  Google Scholar 

  • Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281:30603–30612

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490

    Article  CAS  PubMed  Google Scholar 

  • Buer CS, Muday GK, Djordjevic MA (2009) Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana. J Exp Bot 60:751–763

    Article  CAS  PubMed  Google Scholar 

  • Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P (2008) Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18:473–482

    Article  CAS  PubMed  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennett MJ (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    Article  CAS  PubMed  Google Scholar 

  • Davidson EA (1966) Analysis of sugars found in mucopolysaccharides. Methods Enzymol 8:52–60

    Article  CAS  Google Scholar 

  • Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J (2008) Activation of defense response pathways by OGS and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 3:423–445

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Jennings AC, Davies LA, Gerrish C, Murphy DL (1989) Elicitor-active components from French bean hypocotyls. Physiol Mol Plant Pathol 34:99–115

    Article  CAS  Google Scholar 

  • Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene or jasmonate signaling but requires Phytoalexin Deficient3. Plant Physiol 144:367–379

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146:669–681

    Article  CAS  PubMed  Google Scholar 

  • Geisler M, Kolukisaoglu HU, Bouchard R, Billion K, Berger J, Saal B, Frangne N, Koncz-Kalman Z, Koncz C, Dudler R, Blakeslee JJ, Murphy AS, Martinoia E, Schulz B (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14:4238–4249

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959

    Article  CAS  PubMed  Google Scholar 

  • Hahn MG, Darvill AG, Albersheim P (1981) Host-pathogen interactions. XIX. The endogenous elicitor. A fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybean. Plant Physiol 68:1161–1169

    Article  CAS  PubMed  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hernández GM, Sepulveda B, Richards A, Soriano E (2006) The architecture of Phaseolus vulgaris root is altered when a defense response is elicited by an oligogalacturonide. Braz J Plant Physiol 18:351–355

    Google Scholar 

  • Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176:7–21

    Article  CAS  PubMed  Google Scholar 

  • Kieffer M, Neve J, Kepinski S (2010) Defining auxin response contexts in plant development. Curr Opin Plant Biol 13:12–20

    Article  CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18:3170–3181

    Article  Google Scholar 

  • Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Pérez-Torres A, Ramírez-Pimentel JG, Sánchez-Calderón L, Herrera-Estrella L (2005) Root architecture. In: Turnbull C (ed) Plant architecture and its manipulation. Annu Rev Ser. Wiley-Blackwell, Oxford, pp 181–206

  • Malamy JE, Benfey PN (1997a) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    CAS  PubMed  Google Scholar 

  • Malamy JE, Benfey PN (1997b) Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci 2:390–396

    Article  Google Scholar 

  • Mauro ML, De Lorenzo G, Costantino P, Bellincampi D (2002) Oligogalacturonides inhibit the induction of late but not of early auxin-responsive genes in tobacco. Planta 215:494–501

    Article  CAS  PubMed  Google Scholar 

  • Mravec J, Kubes M, Bielach A, Gaykova V, Petrášek J, Skůpa P, Chand S, Benková E, Zažímalova E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354

    Article  CAS  PubMed  Google Scholar 

  • Muday GK (2001) Auxins and tropisms. J Plant Growth Regul 20:226–243

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA, Glazebrook J (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19:2039–2052

    Article  CAS  PubMed  Google Scholar 

  • Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113

    Article  CAS  PubMed  Google Scholar 

  • Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, 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

    Article  CAS  PubMed  Google Scholar 

  • Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94:1462–1466

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-Chávez E, López-Bucio J, Herrera-Estrella L, Molina-Torres J (2004) Alkamides isolated from plants promotes growth and alters root development in Arabidopsis. Plant Physiol 134:1058–1068

    Article  PubMed  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967

    Article  CAS  PubMed  Google Scholar 

  • Spiro MD, Ridley BL, Eberhard S, Kates KA, Mathieu Y, O’Neill MA, Mohnen D, Guern J, Darvill A, Albersheim P (1998) Biological activity of reducing-end-derivatized oligogalacturonides in tobacco tissue cultures. Plant Physiol 116:1289–1298

    Article  CAS  PubMed  Google Scholar 

  • Spiro MD, Bowers JF, Cosgrove DJ (2002) A comparison of oligogalacturonide- and auxin-induced extracellular alkalinization and growth responses in roots of intact cucumber seedlings. Plant Physiol 130:895–903

    Article  CAS  PubMed  Google Scholar 

  • Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 106:5430–5435

    Article  CAS  PubMed  Google Scholar 

  • Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653

    Article  CAS  PubMed  Google Scholar 

  • Swarup R, Kargul J, Marchant A, Zadik DP, Rahman A, Mills R, Yemm A, May ST, Williams L, Millner P, Tsurumi S, Moore I, Napier R, Kerr ID, Bennett MJ (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16:3069–3083

    Article  CAS  PubMed  Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatio temporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Titapiwatanakun B, Murphy AS (2008) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J Exp Bot 60:1093–1107

    Article  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle T (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed  Google Scholar 

  • Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Lewis DR, Spalding ER (2007) Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell 19:1826–1837

    Article  CAS  PubMed  Google Scholar 

  • Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419–2428

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Professors Angus Murphy for pgp1, pgp4, and pgp19 mutant seeds and Jane Glazebrook for providing camalexin standard and extraction methodology. Dr. Rosa Elva del Río Torres, Dr. Lourdes Macias Rodriguez, and LDG A. Kanek Ballesteros Coria are thanked for excellent technical support in the chemical inactivation of OGs, interpretation of MALDI TOF-TOF analysis, and photographic work, respectively. We gratefully acknowledge the Unidad de Proteómica y Metabolómica, CINVESTAV, IPN for MALDI-TOF-TOF analysis. This research was supported in part by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, grant No. 47239 and 48712) and Universidad Michoacana de San Nicolás de Hidalgo (grant No. CIC 2.11).

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Correspondence to Eva Luz Soriano-Bello.

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Hernández-Mata, G., Mellado-Rojas, M.E., Richards-Lewis, A. et al. Plant Immunity Induced by Oligogalacturonides Alters Root Growth in a Process Involving Flavonoid Accumulation in Arabidopsis thaliana . J Plant Growth Regul 29, 441–454 (2010). https://doi.org/10.1007/s00344-010-9156-x

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