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Hormone interactions during lateral root formation

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Abstract

Lateral root (LR) formation, the production of new roots from parent roots, is a hormone- and environmentally-regulated developmental process in higher plants. Physiological and genetic studies using Arabidopsis thaliana and other plant species have revealed the roles of several plant hormones in LR formation, particularly the role of auxin in LR initiation and primordium development, resulting in much progress toward understanding the mechanisms of auxin-mediated LR formation. However, hormone interactions during LR formation have been relatively underexamined. Recent studies have shown that the plant hormones, cytokinin and abscisic acid negatively regulate LR formation whereas brassinosteroids positively regulate LR formation. On the other hand, ethylene has positive and negative roles during LR formation. This review summarizes recent findings on hormone-regulated LR formation in higher plants, focusing on auxin as a trigger and on the other hormones in LR formation, and discusses the possible interactions among plant hormones in this developmental process.

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References

  • Ahringer J (2000) NuRD and SIN3. Trends Genet 16:351–356. doi:10.1016/S0168-9525(00)02066-7

    PubMed  CAS  Google Scholar 

  • 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. Ann Bot (Lond) 97:883–893. doi:10.1093/aob/mcl027

    CAS  Google Scholar 

  • Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134:1624–1631. doi:10.1104/pp.103.036897

    PubMed  CAS  Google Scholar 

  • Barlow PW, Volkmann D, Baluska F (2004) Polarity in roots. In: Lindsey K (ed) Polarity in plants. Blackwell Publishing, Oxford, pp 192–241

    Google Scholar 

  • Beeckman T, Burssens S, Inzé D (2001) The peri-cell-cycle in Arabidopsis. J Exp Bot 52:403–411

    PubMed  CAS  Google Scholar 

  • Benková 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. doi:10.1016/S0092-8674(03)00924-3

    PubMed  Google Scholar 

  • Bhalerao RP, Eklöf J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332. doi:10.1046/j.0960-7412.2001.01217.x

    PubMed  CAS  Google Scholar 

  • Blakely LM, Blakely RM, Colowit PM, Elliott DS (1988) Experimental studies on lateral root formation in radish seedling roots. II. Analysis of the dose-response to exogenous auxin. Plant Physiol 87:414–419

    PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44. doi:10.1038/nature03184

    PubMed  CAS  Google Scholar 

  • Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34:67–75. doi:10.1046/j.1365-313X.2003.01707.x

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171. doi:10.1016/S1360-1385(03)00051-7

    PubMed  CAS  Google Scholar 

  • Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9:2131–2142. doi:10.1101/gad.9.17.2131

    PubMed  CAS  Google Scholar 

  • Charlton WA (1996) Lateral root initiation. In: Waisel Y, Eshel A, Kfkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 149–173

    Google Scholar 

  • Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–60. doi:10.1104/pp.121.1.53

    PubMed  CAS  Google Scholar 

  • De Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang H (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555. doi:10.1046/j.1365-313X.2003.01652.x

    PubMed  Google Scholar 

  • De Smet I, Vanneste S, Inzé D, Beeckman T (2006a) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887. doi:10.1007/s11103-005-4547-2

    PubMed  CAS  Google Scholar 

  • De Smet I, Zhang H, Inzé D, Beeckman T (2006b) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439. doi:10.1016/j.tplants.2006.07.003

    PubMed  Google Scholar 

  • De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690. doi:10.1242/dev.02753

    PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:4441–4445. doi:10.1038/nature03543

    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. doi:10.1016/j.devcel.2005.05.014

    PubMed  CAS  Google Scholar 

  • Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M, Marchant A, Mills S, Sandberg G, Bennett MJ, Estelle M (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220. doi:10.1126/science.1122847

    PubMed  CAS  Google Scholar 

  • DiDonato RJ, Arbuckle E, Buker S, Sheets J, Tobar J, Totong R, Grisafi P, Fink GR, Celenza JL (2004) Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. Plant J 37:340–353. doi:10.1046/j.1365-313X.2003.01964.x

    PubMed  CAS  Google Scholar 

  • Dong L, Wang L, Zhang Y, Zhang Y, Deng X, Xue Y (2006) An auxin-inducible F-box protein CEGENDUO negatively regulates auxin-mediated lateral root formation in Arabidopsis. Plant Mol Biol 60:599–615. doi:10.1007/s11103-005-5257-5

    PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Doerner PW, Colon-Carmon A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol 124:1648–1657. doi:10.1104/pp.124.4.1648

    PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Rost TL, Colon-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214:30–36

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Gambetta GA, Hernandez-Barrera A, Shishkova S, Gonzalez I (2006) Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Ann Bot (Lond) 7:903–915. doi:10.1093/aob/mcj604

    Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794. doi:10.1073/pnas.0712307105

    PubMed  CAS  Google Scholar 

  • Ferguson BJ, Ross JJ, Reid JB (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol 138:2396–2405. doi:10.1104/pp.105.062414

    PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743. doi:10.1038/nature01387

    PubMed  CAS  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168. doi:10.1046/j.0960-7412.2001.01201.x

    PubMed  CAS  Google Scholar 

  • Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44:382–395. doi:10.1111/j.1365-313X.2005.02537.x

    PubMed  CAS  Google Scholar 

  • Fukaki H, Taniguchi N, Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J 48:380–389. doi:10.1111/j.1365-313X.2006.02882.x

    PubMed  CAS  Google Scholar 

  • Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137. doi:10.1016/S0074-7696(07)56004-3

    PubMed  CAS  Google Scholar 

  • Geisler M, Murphy AS (2005) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102. doi:10.1016/j.febslet.2005.11.054

    PubMed  Google Scholar 

  • 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 transport-related, post-embryonic development of Arabidopsis. Development 131:389–400. doi:10.1242/dev.00926

    PubMed  CAS  Google Scholar 

  • 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 Dev 15:1985–1997. doi:10.1101/gad.905201

    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. doi:10.1105/tpc.106.043778

    PubMed  CAS  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. Plant Cell 17:1376–1386. doi:10.1105/tpc.105.030841

    PubMed  CAS  Google Scholar 

  • Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351. doi:10.1105/tpc.004960

    PubMed  CAS  Google Scholar 

  • 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. Proc Natl Acad Sci USA 101:5146–5151. doi:10.1073/pnas.0308702101

    PubMed  CAS  Google Scholar 

  • Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168. doi:10.1105/tpc.107.050674

    PubMed  CAS  Google Scholar 

  • Hobbie L, Estelle M (1995) The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J 7:211–220. doi:10.1046/j.1365-313X.1995.7020211.x

    PubMed  CAS  Google Scholar 

  • Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087. doi:10.1105/tpc.106.045674

    PubMed  CAS  Google Scholar 

  • Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396. doi:10.1105/tpc.105.030981

    PubMed  CAS  Google Scholar 

  • Ivanchenko MG, Coffeen WC, Lomax TL, Dubrovsky JG (2006) Mutations in the Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation from proliferative cell division in the pericycle. Plant J 46:436–447. doi:10.1111/j.1365-313X.2006.02702.x

    PubMed  CAS  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347. doi:10.1111/j.1365-313X.2008.03528.x

    PubMed  CAS  Google Scholar 

  • Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478. doi:10.1093/pcp/pcf077

    PubMed  CAS  Google Scholar 

  • Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miège C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:1057–1070. doi:10.1016/j.cell.2007.08.040

    PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis TIR1 protein is an auxin receptor. Nature 435:446–451. doi:10.1038/nature03542

    PubMed  CAS  Google Scholar 

  • Kuderová A, Urbánková I, Válková M, Malbeck J, Brzobohaty B, Némethová D, Hejátko J (2008) Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant Cell Physiol 49:570–582. doi:10.1093/pcp/pcn029

    PubMed  Google Scholar 

  • Kurup S, Runions J, Köhler U, Laplaze L, Hodge S, Haseloff J (2005) Marking cell lineages in living tissues. Plant J 42:444–453. doi:10.1111/j.1365-313X.2005.02386.x

    PubMed  CAS  Google Scholar 

  • Laplaze L, Benková E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900. doi:10.1105/tpc.107.055863

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Li L, Xu J, Xu ZH, Xue HW (2005) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17:2738–2753. doi:10.1105/tpc.105.034397

    PubMed  CAS  Google Scholar 

  • Li X, Mo X, Shou H, Wu P (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol 47:1112–1123. doi:10.1093/pcp/pcj082

    PubMed  CAS  Google Scholar 

  • Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56. doi:10.1111/j.1365-313X.2005.02434.x

    PubMed  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287. doi:10.1016/S1369-5266(03)00035-9

    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. doi:10.1111/j.1365-313X.2004.02038.x

    PubMed  CAS  Google Scholar 

  • Lucas M, Godin C, Jay-Allemand C, Laplaze L (2008) Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J Exp Bot 59:55–66. doi:10.1093/jxb/erm171

    PubMed  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77. doi:10.1111/j.1365-3040.2005.01306.x

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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. Plant Cell 14:589–597. doi:10.1105/tpc.010354

    PubMed  CAS  Google Scholar 

  • Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17:3007–3018. doi:10.1105/tpc.105.035451

    PubMed  CAS  Google Scholar 

  • Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15:2979–2991. doi:10.1105/tpc.017046

    PubMed  CAS  Google Scholar 

  • Morris DA, Friml J, Zazímalová E (2004) The transport of auxins. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!, 3rd edn. Kluwer Academic Publishers, Dordrecht, pp 437–470

    Google Scholar 

  • Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097. doi:10.1038/nature06943

    PubMed  Google Scholar 

  • Nakamoto D, Ikeura A, Asami T, Yamamoto KT (2006) Inhibition of brassinosteroid biosynthesis by either a dwarf4 mutation or a brassinosteroid biosynthesis inhibitor rescues defects in tropic responses of hypocotyls in the arabidopsis mutant nonphototropic hypocotyl 4. Plant Physiol 141:456–464. doi:10.1104/pp.105.076273

    PubMed  CAS  Google Scholar 

  • Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853. doi:10.1104/pp.103.030031

    PubMed  CAS  Google Scholar 

  • Nakamura A, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S (2006) Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type. Plant J 45:193–205. doi:10.1111/j.1365-313X.2005.02582.x

    PubMed  CAS  Google Scholar 

  • Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187. doi:10.1111/j.1365-313X.2008.03495.x

    PubMed  CAS  Google Scholar 

  • Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614. doi:10.1111/j.1469-8137.2008.02472.x

    PubMed  CAS  Google Scholar 

  • Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006. doi:10.1111/j.1365-313X.2004.02266.x

    PubMed  CAS  Google Scholar 

  • Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044. doi:10.1073/pnas.0402504101

    PubMed  Google Scholar 

  • Oh K, Ivanchenko MG, White TJ, Lomax TL (2006) The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signaling. Planta 224:133–144. doi:10.1007/s00425-005-0202-z

    PubMed  CAS  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. doi:10.1105/tpc.104.028316

    PubMed  CAS  Google Scholar 

  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. doi:10.1105/tpc.106.047761

    PubMed  CAS  Google Scholar 

  • Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113. doi:10.1146/annurev.arplant.58.032806.104006

    PubMed  CAS  Google Scholar 

  • Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256. doi:10.1038/nature03633

    PubMed  CAS  Google Scholar 

  • Rani Debi B, Taketa S, Ichii M (2005) Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). J Plant Physiol 162:507–515. doi:10.1016/j.jplph.2004.08.007

    PubMed  Google Scholar 

  • Reed RC, Brady SR, Muday GR (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol 118:1369–1378. doi:10.1104/pp.118.4.1369

    PubMed  CAS  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54. doi:10.1105/tpc.105.037796

    PubMed  CAS  Google Scholar 

  • Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480

    PubMed  CAS  Google Scholar 

  • 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. Plant Cell 9:745–757

    PubMed  CAS  Google Scholar 

  • 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 Lett 579:5399–5406. doi:10.1016/j.febslet.2005.08.061

    PubMed  CAS  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453. doi:10.1105/tpc.107.050963

    PubMed  CAS  Google Scholar 

  • Shuai B, Reynaga-Pena CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761. doi:10.1104/pp.010926

    PubMed  CAS  Google Scholar 

  • Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662. doi:10.1046/j.1365-313x.2001.01185.x

    PubMed  CAS  Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Gälweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318. doi:10.1126/science.286.5438.316

    PubMed  CAS  Google Scholar 

  • Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242. doi:10.1105/tpc.105.033365

    PubMed  CAS  Google Scholar 

  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185. doi:10.1105/tpc.107.052068

    PubMed  CAS  Google Scholar 

  • Strader LC, Monroe-Augustus M, Bartel B (2008) The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation. BMC Plant Biol 8:41. doi:10.1186/1471-2229-8-41

    PubMed  Google Scholar 

  • Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954. doi:10.1038/ncb1754

    PubMed  CAS  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 31:1384–1386. doi:10.1126/science.1151461

    Google Scholar 

  • Taramino G, Sauer M, Stauffer JL Jr, Multani D, Niu X, Sakai H, Hochholdinger F (2007) The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J 50:649–659. doi:10.1111/j.1365-313X.2007.03075.x

    PubMed  CAS  Google Scholar 

  • Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393. doi:10.1105/tpc.018630

    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. doi:10.1105/tpc.105.035816

    PubMed  CAS  Google Scholar 

  • Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721

    PubMed  CAS  Google Scholar 

  • To JP, Haberer G, Ferreira FJ, Deruère J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16:658–671. doi:10.1105/tpc.018978

    PubMed  CAS  Google Scholar 

  • Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49:1025–1038. doi:10.1093/pcp/pcn079

    PubMed  CAS  Google Scholar 

  • Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inze D, Fukaki H, Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17:3035–3050. doi:10.1105/tpc.105.035493

    PubMed  CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492. doi:10.1073/pnas.171304098

    PubMed  CAS  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550. doi:10.1105/tpc.014928

    PubMed  CAS  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed J (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130. doi:10.1111/j.1365-313X.2005.02432.x

    PubMed  CAS  Google Scholar 

  • Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383. doi:10.1007/BF00633843

    PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (Lond) 95:707–735. doi:10.1093/aob/mci083

    CAS  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036. doi:10.1101/gad.852200

    PubMed  CAS  Google Scholar 

  • Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419:167–170. doi:10.1038/nature00998

    PubMed  CAS  Google Scholar 

  • Yamamoto M, Yamamoto KT (1999) Effects of natural and synthetic auxins on the gravitropic growth habit of roots in two auxin-resistant mutants of Arabidopsis, axr1 and axr4: evidence for defects in the auxin influx mechanism of axr4. J Plant Res 112:391–396. doi:10.1007/PL00013892

    PubMed  CAS  Google Scholar 

  • Yang X, Lee S, So JH, Dharmasiri S, Dharmasiri N, Ge L, Jensen C, Hangarter R, Hobbie L, Estelle M (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J 40:772–782. doi:10.1111/j.1365-313X.2004.02254.x

    PubMed  CAS  Google Scholar 

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Acknowledgments

We wish to thank Joseph G. Dubrovsky, Yoko Okushima, the anonymous reviewer and editor for helpful comments on this manuscript. The work of our group was supported in part by a Grant-in-Aid to H.F. for Scientific Research on Priority Areas (19060006) from The Ministry of Education, Culture, Sports, Science and Technology, Japan.

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  1. Department of Biology, Graduate School of Science, Kobe University, 1-1, Rokkodai, Kobe, 657-8501, Japan

    Hidehiro Fukaki

  2. Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-0101, Japan

    Masao Tasaka

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  1. Hidehiro Fukaki
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  2. Masao Tasaka
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Correspondence to Hidehiro Fukaki.

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Fukaki, H., Tasaka, M. Hormone interactions during lateral root formation. Plant Mol Biol 69, 437–449 (2009). https://doi.org/10.1007/s11103-008-9417-2

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