Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Goldacre paper: Auxin: at the root of nodule development?

Ulrike Mathesius
+ Author Affiliations
- Author Affiliations

A School of Biochemistry and Molecular Biology, Australian National University and Australian Research Council Centre of Excellence for Integrative Legume Research, Linnaeus Way, Canberra, ACT 0200, Australia. Email: ulrike.mathesius@anu.edu.au

B This paper originates from the Peter Goldacre Award 2007 of the Australian Society of Plant Scientists, received by the author.

Functional Plant Biology 35(8) 651-668 https://doi.org/10.1071/FP08177
Submitted: 24 June 2008  Accepted: 14 August 2008   Published: 19 September 2008

Abstract

Root nodules are formed as a result of an orchestrated exchange of chemical signals between symbiotic nitrogen fixing bacteria and certain plants. In plants that form nodules in symbiosis with actinorhizal bacteria, nodules are derived from lateral roots. In most legumes, nodules are formed de novo from pericycle and cortical cells that are re-stimulated for division and differentiation by rhizobia. The ability of plants to nodulate has only evolved recently and it has, therefore, been suggested that nodule development is likely to have co-opted existing mechanisms for development and differentiation from lateral root formation. Auxin is an important regulator of cell division and differentiation, and changes in auxin accumulation and transport are essential for lateral root development. There is growing evidence that rhizobia alter the root auxin balance as a prerequisite for nodule formation, and that nodule numbers are regulated by shoot-to-root auxin transport. Whereas auxin requirements appear to be similar for lateral root and nodule primordium activation and organ differentiation, the major difference between the two developmental programs lies in the specification of founder cells. It is suggested that differing ratios of auxin and cytokinin are likely to specify the precursors of the different root organs.

Additional keywords: actinomycetes, auxin transport, cytokinin, flavonoids, lateral root, rhizobia, symbiosis.


Acknowledgements

I am grateful for the encouragement, discussion and collaboration of past and present laboratory members and colleagues involved in the presented research, in particular Giel van Noorden, Anton Wasson, Flavia Pellerone, Karsten Oelkers, Joko Prayitno, Tursun Kerim, Melinda Aprelia, Robert Wiblin, Alexander Ivakov, Julia Frugoli, Brett Ferguson, John Ross, Jim Reid, Peter Gresshoff, Christine Beveridge, Michael Djordjevic and Barry Rolfe. I would also like to thank the reviewers for many constructive comments and the Australian Research Council for funding through an Australian Research Fellowship (DP0557692) and through the ARC Centre of Excellence for Integrative Legume Research (CE0348212). A special ‘thank you’ to the Australian Society of Plant Scientists and Functional Plant Biology for their encouragement through the Goldacre award.


References


Allen EK, Allen ON, Newman AS (1953) Pseudonodulation of leguminous plants induced by 2-bromo-3,5-dichlorobenzoic acid. American Journal of Botany 40, 429–435.
CrossRef | open url image1

Allen ON, Allen EK (1940) Response of the peanut plant to inoculation with rhizobia, with special reference to morphological development of the nodules. Botanical Gazette 102, 121–142.
CrossRef | open url image1

Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97, 883–893.
CrossRef | PubMed | open url image1

Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends in Plant Science 11, 217–223.
CrossRef | PubMed | open url image1

Beeckman T, Burssens S, Inzé D (2001) The peri-cell-cycle in Arabidopsis. Journal of Experimental Botany 52, 403–411.
PubMed |
open url image1

Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057–4067.
PubMed |
open url image1

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.
CrossRef | PubMed | open url image1

Bernasconi P (1996) Effect of synthetic and natural protein tyrosine kinase inhibitors on auxin efflux in zucchini (Cucurbita pepo) hypocotyls. Physiologia Plantarum 96, 205–210.
CrossRef | CAS | open url image1

Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal 29, 325–332.
CrossRef | PubMed | open url image1

Bhuvaneswari TV, Bhagwat AA, Bauer WD (1981) Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiology 68, 1144–1149.
PubMed |
open url image1

Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B , et al . (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. The Plant Cell 19, 131–147.
CrossRef | PubMed | open url image1

Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Onckelen H, van Montagu M, Inzé D (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. The Plant Cell 7, 1405–1419.
CrossRef | PubMed | open url image1

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. Molecular Plant-Microbe Interactions 12, 839–844.
CrossRef | open url image1

Bright LJ, Liang Y, Mitchell DM, Harris JM (2005) The LATD gene of Medicago truncatula is required for both nodule and root development. Molecular Plant-Microbe Interactions 18, 521–532.
CrossRef | PubMed | open url image1

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 Physiology 126, 524–535.
CrossRef | PubMed | open url image1

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. The Plant Cell 16, 1191–1205.
CrossRef | PubMed | open url image1

Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiology 140, 1384–1396.
CrossRef | PubMed | open url image1

Burg SP, Burg EA (1966) The interaction between auxin and ethylene and its role in plant growth. Proceedings of the National Academy of Sciences of the United States of America 55, 262–269.
CAS | CrossRef | PubMed |
open url image1

Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211, 98–104.
CrossRef | PubMed | open url image1

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. Journal of Plant Growth Regulation 27, 26–38.
CrossRef | open url image1

Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S , et al . (2001) Auxin transport promotes Arabidopsis lateral root initiation. The Plant Cell 13, 843–852.
CrossRef | PubMed | open url image1

Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang HM, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171.
CrossRef | PubMed | open url image1

Charon C, Johansson C, Kondorosi E, Kondorosi A, Crespi M (1997) enod40 induces dedifferentiation and division of root cortical cells in legumes. Proceedings of the National Academy of Sciences of the United States of America 94, 8901–8906.
CrossRef | PubMed | open url image1

Christiansen-Weniger C (1998) Endophytic establishment of diazotrophic bacteria in auxin-induced tumors of cereal crops. Critical Reviews in Plant Sciences 17, 55–76.
CrossRef | open url image1

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.
CrossRef | open url image1

Crespi MD, Jurkevitch E, Poiret M, d’Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A (1994) ENOD40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO Journal 13, 5099–5122.
PubMed |
open url image1

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. Molecular Plant-Microbe Interactions 14, 267–277.
CrossRef | PubMed | open url image1

De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Molecular Biology 60, 871–887.
CrossRef | PubMed | open url image1

De Smet I, Tetsumura T, De Rybel B, Frey NFD, Laplaze L , et al . (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134, 681–690.
CrossRef | PubMed | open url image1

Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK , et al . (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312, 1218–1220.
CrossRef | PubMed | open url image1

Dhonukshe P, Grigoriev I, Fischere R, Tominaga M, Robinson DG , et al . (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proceedings of the National Academy of Sciences of the United States of America 105, 4489–4494.
CrossRef | PubMed | open url image1

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 and Soil 212, 153–162.
CrossRef | open url image1

Dubrovsky JG, Doerner PW, Colon-Carmona A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiology 124, 1648–1657.
CrossRef | PubMed | open url image1

Dullaart J, Duba LI (1970) Presence of gibberellin-like substances and their possible role in auxin bioproduction in root nodules and roots of Lupinus luteus L. Acta Botanica Neerlandica 19, 877–883. open url image1

Fang YW, Hirsch AM (1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiology 116, 53–68.
CrossRef | PubMed | open url image1

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.  Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 47, 203–206. open url image1

Ferguson BJ, Reid JB (2005) Cochleata: getting to the root of legume nodules. Plant & Cell Physiology 46, 1583–1589.
CrossRef | PubMed | open url image1

Ferguson BJ, Ross JJ, Reid JB (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiology 138, 2396–2405.
CrossRef | PubMed | open url image1

Fernández-López M , Goormachtig S , Gao M , D’Haeze W , Van Montagu M , Holsters M (1998) Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrata. Proceedings of the National Academy of Sciences of the United States of America 95 12724 12728

Foucher F, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Molecular Biology 43, 773–786.
CrossRef | PubMed | open url image1

Friml J (2003) Auxin transport – shaping the plant. Current Opinion in Plant Biology 6, 7–12.
CrossRef | CAS | PubMed | open url image1

Friml J, Yang X, Michniewicz M, Weijers D, Quint A , et al . (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862–865.
CrossRef | PubMed | open url image1

Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. International Review of Cytology – a Survey of Cell Biology 256, 111–137. open url image1

Furuya M, Garlston AW, Stowe BB (1962) Isolation from peas of co-factors and inhibitors of indolyl-3-acetic acid oxidase. Nature 193, 456–457.
CrossRef | PubMed | open url image1

Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V , et al . (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal 44, 179–194.
CrossRef | PubMed | open url image1

Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Müller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230.
CrossRef | PubMed | open url image1

Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jürgens G (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin trans port-related, post-embryonic development of Arabidopsis. Development 131, 389–400.
CrossRef | PubMed | open url image1

Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D , et al . (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proceedings of the National Academy of Sciences of the United States of America 105, 4928–4932.
CrossRef | PubMed | open url image1

Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes & Development 15, 1985–1997.
CrossRef | PubMed | open url image1

Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E , et al . (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316, 1307–1312.
CrossRef | PubMed | open url image1

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.  The Plant Cell 18, 2680–2693.
CrossRef | PubMed | open url image1

Goormachtig S, Capoen W, Holsters M (2004) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends in Plant Science 9, 518–522.
CrossRef | PubMed | open url image1

Grambow HJ, Langenbeck-Schwich B (1983) The relationship between oxidase activity, peroxidase activity, hydrogen peroxide, and phenolic compounds in the degradation of indole-3-acetic acid in vitro. Planta 157, 132–137.
CrossRef | open url image1

Gresshoff PM (1993) Molecular genetic analysis of nodulation genes in soybean. In ‘Plant breeding reviews, Vol. 11’. (Ed. J Janick) pp. 274–318. (John Wiley & Sons Inc.: New York)

Gualtieri G, Bisseling T (2000) The evolution of nodulation. Plant Molecular Biology 42, 181–194.
CrossRef | PubMed | open url image1

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. Canadian Journal of Botany – Revue Canadienne de Botanique 80, 695–720.
CrossRef | open url image1

Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15, 1899–1911.
CrossRef | PubMed | open url image1

Himanen K, Boucheron E, Vanneste S, Engler JD, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. The Plant Cell 14, 2339–2351.
CrossRef | PubMed | open url image1

Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, van Montagu M, Inzé D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proceedings of the National Academy of Sciences of the United States of America 101, 5146–5151.
CrossRef | PubMed | open url image1

Hirsch AM (1992) Developmental biology of legume nodulation. New Phytologist 122, 211–237.
CrossRef | open url image1

Hirsch AM, Fang YW (1994) Plant hormones and nodulation – what’s the connection. Plant Molecular Biology 26, 5–9.
CrossRef | PubMed | open url image1

Hirsch AM, LaRue T (1997) Is the legume nodule a modified root, stem or an organ sui generis? Critical Reviews in Plant Sciences 16, 361–392.
CrossRef | open url image1

Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proceedings of the National Academy of Sciences of the United States of America 86, 1244–1248.
CrossRef | PubMed | open url image1

Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia–legume symbiosis so special? Plant Physiology 127, 1484–1492.
CrossRef | PubMed | open url image1

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. Journal of Plant Growth Regulation 25, 156–165.
CrossRef | open url image1

Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241, 346–349.
CrossRef | PubMed | open url image1

Jones AM (1998) Auxin transport: down and out and up again. Science 282, 2201–2202.
CrossRef | CAS | PubMed | open url image1

Kefford NP, Brockwell J, Zwar JA (1960) The symbiotic synthesis of auxin by legumes and nodule bacteria and its role in nodule development. Australian Journal of Biological Sciences 13, 456–467. open url image1

Kim HB, Lee H, Oh CJ, Lee NH, An CS (2007) Expression of EuNOD-ARP1 encoding auxin-repressed protein homolog is upregulated by auxin and localized to the fixation zone in root nodules of Elaeagnus umbellata.  Molecules and Cells 23, 115–121.
PubMed |
open url image1

Kinkema M, Scott PT, Gresshoff PM (2006) Legume nodulation: successful symbiosis through short- and long-distance signalling. Functional Plant Biology 33, 707–721.
CrossRef | open url image1

Kondorosi E, Redondo-Nieto M, Kondorosi A (2005) Ubiquitin-mediated proteolysis. To be in the right place at the right moment during nodule development. Plant Physiology 137, 1197–1204.
CrossRef | CAS | PubMed | open url image1

Laplaze L, Benkovà E, Casimiro I, Maes L, Vanneste S , et al . (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. The Plant Cell 19, 3889–3900.
CrossRef | PubMed | open url image1

Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two-stage process. Development 121, 3303–3310.
PubMed |
open url image1

Liang Y, Harris JM (2005) Response of root branching to abscisic acid is correlated with nodule formation both in legumes and nonlegumes. American Journal of Botany 92, 1675–1683.
CrossRef | open url image1

Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant. Developmental Biology 304, 297–307.
CrossRef | PubMed | open url image1

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.
CrossRef | open url image1

Lievens S, Goormachtig S, Den Herder J, Capoen W, Mathis R, Hedden P, Holsters M (2005) Gibberellins are involved in nodulation of Sesbania rostrata.  Plant Physiology 139, 1366–1379.
CrossRef | PubMed | open url image1

Ligero F, Lluch C, Olivares J (1986) Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti.  Journal of Plant Physiology 125, 361–365. open url image1

Ligero F, Lluch C, Olivares J (1987) Evolution of ethylene from roots and nodulation rate of alfalfa (Medicago sativa L.) plants inoculated with Rhizobium meliloti as affected by the presence of nitrate. Journal of Plant Physiology 129, 461–467. open url image1

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 Molecular Biology 49, 249–272.
CrossRef | PubMed | open url image1

Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Nonmanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. The Plant Cell 17, 1090–1104.
CrossRef | PubMed | open url image1

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. The Plant Journal 38, 203–214.
CrossRef | PubMed | open url image1

Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana.  Development 124, 33–44.
PubMed |
open url image1

Marchant A, Bhalerao R, Casimiro I, Eklof J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. The Plant Cell 14, 589–597.
CrossRef | PubMed | open url image1

Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biology 6, e68.
CrossRef | PubMed | open url image1

Mathesius U (2001) Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. Journal of Experimental Botany 52, 419–426.
CAS | PubMed |
open url image1

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. Molecular Plant-Microbe Interactions 11, 1223–1232.
CrossRef | open url image1

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. The Plant Journal 14, 23–34.
CrossRef | PubMed | open url image1

Mathesius U, Charon C, Rolfe BG, Kondorosi A, Crespi M (2000a) Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Molecular Plant-Microbe Interactions 13, 617–628.
CrossRef | PubMed | open url image1

Mathesius U, Weinman JJ, Rolfe BG, Djordjevic MA (2000b) Rhizobia can induce nodules in white clover by ‘hijacking’ mature cortical cells activated during lateral root development. Molecular Plant-Microbe Interactions 13, 170–182.
CrossRef | PubMed | open url image1

Mitchell EK, Davies PJ (1975) Evidence for three different systems of movement of indoleacetic-acid in intact roots of Phaseolus coccineus.  Physiologia Plantarum 33, 290–294.
CrossRef | open url image1

Morris AC, Djordjevic MA (2006) The Rhizobium leguminosarum biovar trifolii ANU794 induces novel developmental responses on the subterranean clover cultivar Woogenellup. Molecular Plant-Microbe Interactions 19, 471–479.
CrossRef | PubMed | open url image1

Morris ME, Zhang SZ (2006) Flavonoid-drug interactions: effects of flavonoids on ABC transporters. Life Sciences 78, 2116–2130.
CrossRef | PubMed | open url image1

Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends in Plant Science 6, 535–542.
CrossRef | PubMed | open url image1

Muday GK, Haworth P (1994) Tomato root-growth, gravitropism, and lateral development – correlation with auxin transport. Plant Physiology and Biochemistry 32, 193–203.
PubMed |
open url image1

Murphy A, Taiz L (1999) Naphthylphthalamic acid is enzymatically hydrolyzed at the hypocotyl-root transition zone and other tissues of Arabidopsis thaliana seedlings. Plant Physiology and Biochemistry 37, 413–430.
CrossRef | open url image1

Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211, 315–324.
CrossRef | PubMed | open url image1

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 Physiology 128, 935–950.
CrossRef | PubMed | open url image1

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.
CrossRef | PubMed | open url image1

Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. The Plant Cell 13, 2441–2454.
CrossRef | PubMed | open url image1

van Noorden GE (2006) The role of auxin in the regulation of nodule numbers in Medicago truncatula. PhD thesis. Australian National University, Canberra, Australia.

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 Physiology 144, 1115–1131.
CrossRef | PubMed | open url image1

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 Physiology 140, 1494–1506.
CrossRef | PubMed | open url image1

Nutman PS (1948) Physiological studies on nodule formation. I. The relation between nodulation and lateral root formation in red clover. Annals of Botany 12, 81–96. open url image1

Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD , et al . (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251–1256.
CrossRef | PubMed | open url image1

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 Molecular Biology 52, 1169–1180.
CrossRef | PubMed | open url image1

Parry G, Estelle M (2006) Auxin receptors: a new role for F-box proteins. Current Opinion in Cell Biology 18, 152–156.
CrossRef | PubMed | open url image1

Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? The Plant Cell 8, 1899–1913.
CrossRef | PubMed | open url image1

Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends in Plant Science 12, 556–563.
CrossRef | PubMed | open url image1

Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiology 126, 536–548.
CrossRef | PubMed | open url image1

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.  The Plant Cell 16, 1898–1911.
CrossRef | open url image1

Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.
CrossRef | PubMed | open url image1

Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula.  Plant Physiology 131, 998–1008.
CrossRef | PubMed | open url image1

Penmetsa RV, Uribe P, Anderson J, Lichtenzveig J, Gish J-C , et al . (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. The Plant Journal 55, 580–595.
CrossRef | PubMed | open url image1

Peret B, Swarup R, Jansen L, Devos G, Auguy F , et al . (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca.  Plant Physiology 144, 1852–1862.
CrossRef | PubMed | open url image1

Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M , et al . (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918.
CrossRef | PubMed | open url image1

Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biology 7, 21.
CrossRef | PubMed | open url image1

Prayitno J, Imin N, Rolfe BG, Mathesius U (2006a) Identification of ethylene-mediated protein changes during nodulation in Medicago truncatula using proteome analysis. Journal of Proteome Research 5, 3084–3095.
CrossRef | PubMed | open url image1

Prayitno J, Rolfe BG, Mathesius U (2006b) The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiology 142, 168–180.
CrossRef | PubMed | open url image1

Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany 52, 381–401.
PubMed |
open url image1

Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
CrossRef | PubMed | open url image1

Rolfe BG, Gresshoff PM (1988) Genetic analysis of legume nodule initiation. Annual Review of Plant Physiology and Plant Molecular Biology 39, 297–319. open url image1

Ross JJ, O’Neill DP, Smith JJ, Kerckhoffs LHJ, Elliott RC (2000) Evidence that auxin promotes gibberellin A(1) biosynthesis in pea. The Plant Journal 21, 547–552.
CrossRef | PubMed | open url image1

Roudier F, Fedorova E, Lebris M, Lecomte P, Gyorgyey J, Vaubert D, Horvath G, Abad P, Kondorosi A, Kondorosi E (2003) The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplication-associated developmental programs. Plant Physiology 131, 1091–1103.
CrossRef | PubMed | open url image1

Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. The Plant Cell 9, 745–757.
CrossRef | PubMed | open url image1

Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T , et al . (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472.
CrossRef | PubMed | open url image1

Sachs T (1981) The control of the patterned differentiation of vascular tissues. Advances in Botanical Research 9, 151–262.
CrossRef |
open url image1

Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Duchtig P, Mancuso S, Martinoia E, Geisler M (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Letters 579, 5399–5406.
CrossRef | PubMed | open url image1

Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822.
CrossRef | PubMed | open url image1

Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299, 109–112.
CrossRef | PubMed | open url image1

Sergeeva E, Liaimer A, Bergman B (2002) Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215, 229–238.
CrossRef | PubMed | open url image1

Smit P , Bisseling T (2008) Genetics: a way to unravel molecular mechanisms controlling the rhizobial-legume symbiosis. In ‘Nitrogen-fixing leguminous symbioses’. (Eds MJ Dilworth, EK James, JI Sprent, WE Newton) pp. 191–206. (Springer-Verlag: Dordrecht, The Netherlands)

Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen-fixation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 92, 2647–2651.
CrossRef | PubMed | open url image1

Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews 31, 425–448.
CrossRef | PubMed | open url image1

Spaink HP (2004) Specific recognition of bacteria by plant LysM domain receptor kinases. Trends in Microbiology 12, 201–204.
CrossRef | CAS | PubMed | open url image1

Sprent JI (1989) Which steps are essential for the formation of functional legume nodules? New Phytologist 111, 129–153.
CrossRef | open url image1

Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174, 11–25.
CrossRef | CAS | PubMed | open url image1

Sprent JI (2008) Evolution and diversity of legume symbiosis. In ‘Nitrogen-fixing leguminous symbioses’. (Eds MJ Dilworth, EK james, JI Sprent, WE Newton) pp. 1–21. (Springer-Verlag: Dordrecht, The Netherlands)

Sprent JI, James EK (2008) Legume–rhizobial symbiosis: an anorexic model? New Phytologist 179, 3–5.
CrossRef | PubMed | open url image1

Sprent JI , Sprent P (1990) ‘Nitrogen fixing organisms.’ (Chapman and Hall: London)

Stenlid G (1976) Effects of flavonoids on the polar transport of auxins. Physiologia Plantarum 38, 262–266.
CrossRef | CAS | open url image1

Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. The Plant Cell 19, 2169–2185.
CrossRef | PubMed | open url image1

Streeter J (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Critical Reviews in Plant Sciences 7, 1–23.
CAS |
open url image1

Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum.  The Plant Journal 48, 261–273.
CrossRef | PubMed | open url image1

Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends in Plant Science 12, 282–285.
CrossRef | PubMed | open url image1

Sun JH, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. The Plant Journal 46, 961–970.
CrossRef | PubMed | open url image1

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 & Development 15, 2648–2653.
CrossRef | PubMed | open url image1

Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Current Opinion in Plant Biology 8, 317–323.
CrossRef | PubMed | open url image1

Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews. Molecular Cell Biology 7, 847–859.
CrossRef | PubMed | open url image1

Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A , et al . (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. The Plant Cell 17, 2922–2939.
CrossRef | PubMed | open url image1

Theunis M, Kobayashi H, Broughton WJ, Prinsen E (2004) Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Molecular Plant-Microbe Interactions 17, 1153–1161.
CrossRef | PubMed | open url image1

Thimann KV (1936) On the physiology of the formation of nodules on legume roots. Proceedings of the National Academy of Sciences of the United States of America 22, 511–514.
CrossRef | CAS | PubMed | open url image1

Timmers ACJ, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium–Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126, 3617–3628.
PubMed |
open url image1

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.
CrossRef | PubMed | open url image1

Trinick MJ (1979) Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii plants. Canadian Journal of Microbiology 25, 565–578.
CAS | PubMed |
open url image1

Tsurumi S, Ohwaki Y (1978) Transport of C-14-labeled indoleacetic acid in Vicia root segments. Plant & Cell Physiology 19, 1195–1206. open url image1

Vanneste S, De Rybel B, Beemster GTS, Ljung K, De Smet I , et al . (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana.  The Plant Cell 17, 3035–3050.
CrossRef | PubMed | open url image1

Vieten A, Vanneste S, Wisniewska J, Benkovà E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin dependent cross-regulation of PIN expression. Development 132, 4521–4531.
CrossRef | PubMed | open url image1

Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends in Plant Science 12, 160–168.
CrossRef | PubMed | open url image1

Walch-Liu P, Ivanov II, Filleur S, Gan YB, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Annals of Botany 97, 875–881.
CrossRef | PubMed | open url image1

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. The Plant Cell 18, 1617–1629.
CrossRef | PubMed | open url image1

Wheeler CT, Crozier A, Sandberg G (1984) The biosynthesis of indole-3-acetic acid by Frankia. Plant and Soil 78, 99–104.
CrossRef | open url image1

Wightman F, Schneider EA, Thimann KV (1980) Hormonal factors controlling the initiation and development of lateral roots. II. Effects of exogenous growth factors on lateral root formation in pea roots. Physiologia Plantarum 49, 304–314.
CrossRef | open url image1

Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485–493.
CrossRef | CAS | PubMed | open url image1

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.
CrossRef | PubMed | open url image1

Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Annals of Botany 95, 707–735.
CrossRef | PubMed | open url image1

Wopereis J, Pajuelo E, Dazzo FB, Jiang QY, Gresshoff PM, de Bruijn FJ, Stougaard J, Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal 23, 97–114.
CrossRef | PubMed | open url image1

Wu CW, Dickstein R, Cary AJ, Norris JH (1996) The auxin transport inhibitor N-(1-naphthyl)phthalamic acid elicits pseudonodules on non-nodulating mutants of white sweetclover. Plant Physiology 110, 501–510.
PubMed |
open url image1

Wu GS, Lewis DR, Spalding EP (2007) Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. The Plant Cell 19, 1826–1837.
CrossRef | PubMed | open url image1

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. Current Microbiology 32, 67–71.
CrossRef | open url image1

Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Current Biology 16, 1123–1127.
CrossRef | PubMed | open url image1

Zhang XC, Wu XL, Findley S, Wan JR, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiology 144, 623–636.
CrossRef | PubMed | open url image1







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