Skip to main content
SpringerLink
Log in
SpringerLink
Log in

Insights into Pivotal Role of Phytohormonal Cross Talk in Tailoring Underground Plant Root System Architecture

  • Chapter
  • First Online:
Root Biology

Part of the book series: Soil Biology ((SOILBIOL,volume 52))

  • 2078 Accesses

Abstract

Root architecture development is a fundamental component of plant growth, facilitating plant with firm anchorage in the ground, adequate acquisition of water and nutrients, as well as their responses to abiotic and biotic signals in various ecological niches. Physiological and molecular research in the field of root biology has substantiated that root organogenesis is governed by the intricate role of “plant growth regulators—phytohormones.” Typically, master regulator—auxin—plays a crucial role at various developmental processes; however other hormones also interact either synergistically or antagonistically with auxin to trigger cascades of events leading to appropriate root morphogenesis. Studies on phytohormonal regulation of root architecture development principally focus on analysis of gene mutations modulating hormone synthesis and catabolism and those encoding for receptors and signaling elements along with analysis of the feedback regulation of hormonal pathways. Hormonal regulation of root architecture operates through a web of interacting responses rather than through linear conduit, where one hormone may be positively regulating one step but downregulating the other step. This chapter is designed to highlight the significance of complicated interplay among the phytohormones in regulating downstream events coupled with root architecture development at three important steps: primary root (PR) development, lateral root (LR) development, and root hair (RH) growth.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
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

  • Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane- 1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 270:19093–19099

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193

    Article  CAS  PubMed  Google Scholar 

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, Ecker JR (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci 100:2992–2997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio GA et al (2013) PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol 161:931–941

    Article  CAS  PubMed  Google Scholar 

  • Band LR, Wells DM, Larrieu A, Sun J, Middleton AM, French AP et al (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. PNAS 109(12):4668–4673

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Beemster GT, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belin C, Megies C, Hauserova E, Lopez-Molina L (2009) Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21:2253–2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser M-T, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70

    CAS  PubMed  Google Scholar 

  • Benfey PN, Bennett M, Schiefelbein J (2010) Getting to the root of plant biology: impact of the Arabidopsis. Plant J 61:992–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465

    Article  CAS  PubMed  Google Scholar 

  • Benjamins R, Quint AB, 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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Berger F, Hung C-Y, Dolan L, Schiefelbein J (1998) Control of cell division in the root epidermis of Arabidopsis thaliana. Dev Biol 194:235–245

    Article  CAS  PubMed  Google Scholar 

  • Berova M, Zlatev Z (2000) Physiological response and yield of paclobutrazol treated tomato plants (Lycopersicon esculentum Mill.). Plant Growth Regul 30:117–123

    Google Scholar 

  • Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant J 29:325–332

    Article  CAS  PubMed  Google Scholar 

  • Bianco MD, Kepinski S (2011) Context, specificity, and self-organization in auxin response. Cold Spring Harb Perspect Biol 3:a001578

    PubMed  PubMed Central  Google Scholar 

  • Bianco MD, Giustini L, Sabatini S (2013) Spatiotemporal changes in the role of cytokinin during root development. New Phytol 199:324–338

    Article  PubMed  CAS  Google Scholar 

  • Bielach A, Duclercq J, Marhavy P, Benkova E (2012) Genetic approach towards the identification of auxin–cytokinin crosstalk components involved in root development. Philos Trans R Soc B 367:1469–1478

    Article  CAS  Google Scholar 

  • Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Philip NB (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960

    Article  CAS  PubMed  Google Scholar 

  • Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benkova E, Mahonen AP, Helariutta Y (2011a) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21:917–926

    Article  CAS  PubMed  Google Scholar 

  • Bishopp A, Lehesranta S, Vaten V, Help H, El-Showk E, Scheres B, Helariutta K, Mahonen AP, Sakakibara H, Helariutta Y (2011b) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  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 signalling and lateral root development in Arabidopsis. Plant J 34:67–75

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6(1):18–28

    Article  CAS  PubMed  Google Scholar 

  • Brugiere N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299

    Article  CAS  PubMed  Google Scholar 

  • Cao XF, Linstead P, Berger F, Kieber J, Dolan L (1999) Differential sensitivity of epidermal cells is involved in the establishment of cell pattern in the Arabidopsis root. Physiol Plant 106:311–317

    Article  CAS  PubMed  Google Scholar 

  • Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO et al (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci 111:2379–2384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cary AJ, Liu W, Howell SH (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 107:1075–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casson SA, Lindsey K (2003) Genes and signalling in root development. New Phytol 158:11–38

    Article  CAS  Google Scholar 

  • Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K (2002) The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14:1705–1721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chapman EJ, Estelle M (2009) Cytokinin and auxin intersection in root meristems. Genome Biol 10:210

    Article  PubMed Central  CAS  Google Scholar 

  • Chen H, Xiong L (2009) The short-rooted vitamin B6-deficient mutant pdx1 has impaired local auxin biosynthesis. Planta 229:1303–1310

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL, Hussey PJ (2006) The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058–3072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett MJ, Hwang D, De Smet I, Hwang I (2014) A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat Cell Biol 16:66–76

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Lee Y, Kim SY, Lee Y, Hwang J (2012) Arabidopsis ROP interactive CRIB motif-containing protein 1 (RIC1) positively regulates auxin signalling and negatively regulates abscisic acid (ABA) signalling during root development. Plant Cell Environ 36(5):945–955

    Article  PubMed  CAS  Google Scholar 

  • Chung Y, Maharjan PM, Lee O, Fujioka S, Jang S, Kim B, Takatsuto S, Tsujimoto M, Kim H, Cho S, Park T, Cho H, Hwang I, Choe S (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J 66:564–578

    Article  CAS  PubMed  Google Scholar 

  • Clark NM, de Luis Balaguer MA, Sozzani R (2014) Experimental data and computational modeling link auxin gradient and development in the Arabidopsis root. Front Plant Sci 5:328

    Article  PubMed  PubMed Central  Google Scholar 

  • Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) TORNADO1 and TORNADO2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development 127:3385–3394

    CAS  PubMed  Google Scholar 

  • Cohen M, Prandi C, Occhiato EG, Tabasso S, Wininger S, Resnick N, Steinberger Y, Koltai H, Kapulnik Y (2013) Structure-function relations of strigolactone analogs: activity as plant hormones and plant interactions. Mol Plant 6:141–152

    Article  CAS  PubMed  Google Scholar 

  • Couee I, Hummel I, Sulmon C, Gouesbet G, Amrani AE (2004) Involvement of polyamines in root development. Plant Cell Tiss Org Cult 76:1–10

    Article  CAS  Google Scholar 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  CAS  PubMed  Google Scholar 

  • Dai Y, Wang H, Li B, Huang J, Liu X, Zhou Y, Mou Z, Li J (2006) Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 18:308–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D et al (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20:1697–1706

    Article  PubMed  CAS  Google Scholar 

  • De Smet I (2012) Lateral root initiation: one step at a time. New Phytol 193:867–873

    Article  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

    Article  PubMed  Google Scholar 

  • De Smet I, Vanneste S, Inze D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887

    Article  CAS  PubMed  Google Scholar 

  • De Smet I, Tetsumura T, De Rybel B, Frey N, Laplaze L, Casimiro I et al (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D et al (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, White PJ, Bengough AG, Dupuy L, Parizot B, Casimiro I et al (2012) Analyzing lateral root development: how to move forward. Plant Cell 24:15–20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Del Bianco M, Kepinski S (2011) Context, specificity and self-organization in auxin response. Cold Spring Harb Perspect Biol 3:a001578

    PubMed  PubMed Central  Google Scholar 

  • Del Bianco M, Giustini L, Sabatini S (2013) Spatiotemporal changes in the role of cytokinin during root development. New Phytol 199:324–338

    Article  PubMed  CAS  Google Scholar 

  • Delbarre A, Muller P, Guern J (1998) Short-lived and phosphorylated proteins contribute to carrier-mediated efflux, but not to influx, of auxin in suspension-cultured tobacco cells. Plant Physiol 116:833–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Della Rovere F, Fattorini L, D’Angeli D, Veloccia A, Falasca G, Altamura MM (2013) Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of Arabidopsis. Ann Bot 112:1395–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root meristem size by controlling cell differentiation. Curr Biol 17:678–682

    Article  CAS  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Article  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:365–373

    Article  CAS  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 

  • Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J et al (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. PNAS 105:4489–4494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy J, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    Article  PubMed  Google Scholar 

  • Doerner P, Jorgensen J-E, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380:520–523

    Article  CAS  PubMed  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organization of the Arabidopsis thaliana root. Development 119:71–84

    CAS  PubMed  Google Scholar 

  • Dolan L, Duckett C, Grienon C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relations and patterning in the root epidermis of Arabidopsis. Development 120:2465–2474

    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

    Article  CAS  PubMed  Google Scholar 

  • Echevarria-Machado I, MRM E-G, Larque-Saavedra A (2007) Responses of transformed Catharanthus roseus roots to femtomolar concentrations of salicylic acid. Plant Physiol Biochem 45:501–507

    Article  CAS  PubMed  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  CAS  PubMed  Google Scholar 

  • Esau K (1977) Anatomy of seed plants. John Wiley & Sons, New York

    Google Scholar 

  • Fabregas N, Li N, Boeren S, Nash TE, Goshe MB, Clouse SD, de Vries S, Cano-Delgado AI (2013) The BRASSINOSTEROID INSENSITIVE1-LIKE3 signalosome complex regulates Arabidopsis root development. Plant Cell 25:3377–3388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frigerio M, Alabadi D, Perez-Gomez J, Gracia-Cacel L, Phillips AL, Hedden P, Blazquez MA (2006) Transcriptional regulation of gibberellins metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jurgens G, Palme K (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 in Arabidopsis. Plant J 29:153–168

    Article  CAS  PubMed  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Garay-Arroyo A, Sanchez MD, Garcia-PonceB AE, Alvarezuylla ER (2012) Hormone symphony during root growth and development. Dev Dyn 241:1867–1885

    Article  CAS  PubMed  Google Scholar 

  • Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166:509–517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giehl RF, Gruber BD, von Wiren N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Carranza ZH, Elliott KA, Roberts JA (2007) Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana. J Exp Bot 58:3719–3730

    Article  CAS  PubMed  Google Scholar 

  • Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busova VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639

    Article  CAS  PubMed  Google Scholar 

  • Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M, Palme K, Bennett MJ, Scheres B (2002) Cell polarity signalling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr Biol 12:329–334

    Article  CAS  PubMed  Google Scholar 

  • Grieneisen VA, Xu J, Maree AFM, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013

    Article  CAS  PubMed  Google Scholar 

  • Grossi JA, Moraes PJ, Tinoco SA, Barbosa JG, Finger FL, Cecon PR (2005) Effects of paclobutrazol on growth and fruiting characteristics of Pitanga ornamental pepper. Acta Hortic (683):333–336

    Google Scholar 

  • Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Rashotte AM (2012) Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep 31:801–812

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Singh M, Laxmi A (2015) Interaction between glucose and brassinosteroid during the regulation of lateral root development in Arabidopsis. Plant Physiol 168:307–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamann T, Mayer U, Jurgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395

    CAS  PubMed  Google Scholar 

  • Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15:301–312

    Article  CAS  PubMed  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11:70–74

    Article  CAS  PubMed  Google Scholar 

  • Hummel I, Couee I, EI Amrani A, Martin-Tanguy J, Hennion F (2002) Involvement of polyamines in root development at low temperature in the subantarctic cruciferous species Pringlea antiscorbutica. J Exp Bot 53:1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Hung C-Y, Lin Y, Zhang M, Pollock S, Marks MD, Schiefelbein J (1998) A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol 117:73–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M (2009) Local auxin biosynthesis modulates gradient directed planar polarity in Arabidopsis. Nat Cell Biol 11:731–738

    Article  CAS  PubMed  Google Scholar 

  • Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386

    Article  CAS  PubMed  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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jang SJ, Choi YJ, Park KY (2002) Effects of polyamines on shoot and root development in Arabidopsis seedlings and carnation cultures. Plant Biol J 45:230–236

    Article  CAS  Google Scholar 

  • Jung JKH, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapulnik Y, Koltai H (2014) Strigolactone involvement in root development, response to abiotic stress, and interactions with the biotic soil environment. Plant Physiol 166:560–569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C et al (2011a) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216

    Article  CAS  PubMed  Google Scholar 

  • Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H (2011b) Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J Exp Bot 62:2915–2924

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Park PJ, Hwang HJ, Lee SY, Oh MH, Kim SG (2006) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci Biotechnol Biochem 70:768–773

    Article  CAS  PubMed  Google Scholar 

  • Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130:5769–5777

    Article  CAS  PubMed  Google Scholar 

  • Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa Y (2007) RING-H2 type ubiquitin ligase EL5 is involved in root development through the maintenance of cell viability in rice. Plant J 51:92–104

    Article  CAS  PubMed  Google Scholar 

  • Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549

    Article  CAS  PubMed  Google Scholar 

  • Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S et al (2010) Strigolactones effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136

    Article  CAS  Google Scholar 

  • Krupinski P, Jonsson H (2010) Modeling auxin-regulated development. Cold Spring Harb Perspect Biol 2:a001560

    Article  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–655

    Article  CAS  PubMed  Google Scholar 

  • Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152–3169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R et al (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900

    Article  CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792

    Article  CAS  PubMed  Google Scholar 

  • Lau S, Shao N, Bock R, Jurgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188

    Article  CAS  PubMed  Google Scholar 

  • Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up- and down-regulated and uncoupled from differentiation. Plant Physiol 125(2):519–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473–483

    Article  CAS  PubMed  Google Scholar 

  • Lee JS, Wang S, Sritubtim S, Chen JG, Ellis BE (2009) Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J 57:975–985

    Article  CAS  PubMed  Google Scholar 

  • Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485–3495

    Article  CAS  PubMed  Google Scholar 

  • Lewis DR, Olex AL, Lundy SR, Turkett WH, Fetrow JS, Muday GK (2013) A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell 25:3329–3346

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant. Dev Biol 304:297–307

    Article  CAS  PubMed  Google Scholar 

  • Lindsay D, Sawhney V, Bonham-Smith P (2006) Cytokinin-induced changes in CLAVATA1 and WUSCHEL expression temporally coincide with altered floral development in Arabidopsis. Plant Sci 170:1111–1117

    Article  CAS  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Xu ZH, Luo D, Xue HW (2003) Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J 36:189–202

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci 110:15485–15490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Rowe J, Lindsey K (2014) Hormonal cross talk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116

    PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Lucas M, Godin C, Jay-Allemand C, Laplaze L (2007) Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J Exp Bot 59:56–66

    Google Scholar 

  • Maharjan PM, Schulz B, Choe S (2011) BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis. J Plant Biol 54:126–134

    Article  CAS  Google Scholar 

  • Mähönen H, Törmäkangas M, Pischke S, Helariutta K (2006) Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol 16:1116–1122

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklöf 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(3):589–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32:149–158

    Article  PubMed  CAS  Google Scholar 

  • Masucci JD, Schiefelbein JW (1994) The rdh6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-and-ethylene associated process. Plant Physiol 106:1335–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8:1505–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci U S A 105:20027–20031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes AFS, Cidade LC, Otoni WC, Soares-Filho WS, Costa WGC (2011) Role of auxins, polyamines and ethylene in root formation and growth in sweet orange. Biol Plant 55:375–378

    Article  CAS  Google Scholar 

  • Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I et al (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyl transferases and tRNA isopentenyl transferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:16598–16603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monzon GC, Pinedo M, Lamattina L, Canal L (2012) Sunflower root growth regulation: the role of jasmonic acid and its relation with auxins. Plant Growth Regul 66:129–136

    Article  CAS  Google Scholar 

  • Moore S, Zhang X, Mudge A, Rowe JH, Topping JF, Liu J, Lindsey K (2015) Spatiotemporal modelling of hormonal crosstalk explains the level and patterning of hormones and gene expression in Arabidopsis thaliana wild-type and mutant roots. New Phytol 207:1110–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moubayidin L, Perilli S, Dello Ioio R et al (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20:1138–1143

    Article  CAS  PubMed  Google Scholar 

  • Moubayidin L, Di Mambro R, Sozzani R, Pacifici E, Salvi E, Terpstra I et al (2013) Spatial coordination between stem cell activity and cell differentiation in the root meristem. Dev Cell 26:405–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mravec J, Petrasek J, Li N, Boeren S, Karlova R, Kitakura S et al (2011) Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr Biol 21:1055–1060

    Article  CAS  PubMed  Google Scholar 

  • Mu Y, Zou M, Sun X, HeB, Xu X, Liu Y, Zhang L, Chi1 W (2017) BASIC PENTACYSTEINE proteins repress ABSCISIC ACID INSENSITIVE4 expression via direct recruitment of the Polycomb-Repressive Complex 2 in Arabidopsis root development. Plant Cell Physiol 58(3):607–621

    Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Nieuwland J, Maughan S, Dewitte W, Scofield S, Sanz L, Murray JA (2009) The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region. Proc Natl Acad Sci 106:22528–22533

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pacifici E, Polverari L, Sabatini S (2015) Plant hormone cross-talk: the pivot of root growth. J Exp Bot 66:1113–1121

    Article  CAS  PubMed  Google Scholar 

  • Palavan-Unsal N (1987) Polyamine metabolism in the roots of Phaseolus vulgaris. Interaction of inhibitors of polyamine biosynthesis with putrescine in growth and polyamine biosynthesis. Plant Cell Physiol 28:565–572

    CAS  Google Scholar 

  • Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H et al (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202:1184–1196

    Article  CAS  PubMed  Google Scholar 

  • Parizot B, Laplaze L, Ricaud L, Boucheron-Dubuisson E, Bayle V, Bonke M et al (2008) Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol 146:140–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett MJ (2001) Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J 25:399–406

    Article  CAS  PubMed  Google Scholar 

  • Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408

    Article  CAS  PubMed  Google Scholar 

  • Peret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L (2014) Root architecture responses: In search of phosphate. Plant Physiol 166:1713–1723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perilli S, Moubayidin L, Sabatini S (2013) Molecular basis of Cytokinin action during Root development. In: Beeckman T (ed) Plant Roots-The Hidden Half, CRC Press, pp 1–12

    Google Scholar 

  • Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T et al (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21(6):1659–1668

    Article  CAS  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. In: Merchant SS (ed) Annual Review of Plant Biology. Palo Alto, CA: Annual Reviews, pp 563–590

    Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560

    Article  CAS  PubMed  Google Scholar 

  • Rahman A, Amakawa T, Goto N, Tsurumi S (2001) Auxin is a positive regulator for ethylene-mediated response in the growth of Arabidopsis roots. Plant Cell Physiol 42:301–307

    Article  CAS  PubMed  Google Scholar 

  • Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  CAS  Google Scholar 

  • Raya-Gonzalez J, Pelagio-Flores R, Lopez-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358

    Article  CAS  PubMed  Google Scholar 

  • Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosquete MR, von Wangenheim D, Marhavy P, Barbez E, Stelzer EH, Benkova E, Maizel A, Kleine-Vehn J (2013) An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr Biol 23:817–822

    Article  CAS  PubMed  Google Scholar 

  • Rowe JH, Topping JF, Liu J, Lindsey K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734

    Article  CAS  PubMed  Google Scholar 

  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beechman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruzicka K, Simaskova M, Duclercq J, Petrasek J, Zazimalova E, Simon S, Friml J, Van Montagu MCE, Benkova E (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci U S A 106:4284–4289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini S, Sharma I, Kaur N, Pati PK (2013) Auxin: A master regulator in plant root development. Plant Cell Rep 32:741–757

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Mark Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakkajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    Article  CAS  PubMed  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scacchi E, Salinas P, Gujas B, Santuari L, Krogan N, Ragni L, Berleth T, Hardtke CS (2010) Spatio-temporal sequence of cross regulatory events in root meristem growth. Proc Natl Acad Sci U S A 107:22734–22739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120:2475–2487

    CAS  Google Scholar 

  • Scheres B, Di Laurenzio L, Willemsen V, Hauser M-T, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121:53–62

    CAS  Google Scholar 

  • Schiefelbein JW (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol 124:1525–1531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwager KM, Calderon-Villalobos LI, Dohmann EM, Willige BC, Knierer S, Nill C, Schwechheimer C (2007) Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development. Plant Cell 19:1163–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sena G, Wang X, Liu HY, Hofhuis H, Birnbaum KD (2009) Organ regeneration does not require a functional stem cell niche in plants. Nature 457:1150–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shani E, Weinstain R, Zhang Y, Castillejo C, Kaiserli E, Chory J, Tsien RY, Estelle M (2013) Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci USA 110:4834–4839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222

    Article  CAS  PubMed  Google Scholar 

  • Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H, Kato H, Matsuoka M (2008) Structural basis for gibberellins recognition by its receptor GID1. Nature 456:520–523

    Article  CAS  PubMed  Google Scholar 

  • Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverstone AL, Chang C, Krol E, Sun TP (1997) Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. The Plant J 12:9–19

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Gupta A, Laxmi A (2014) Glucose control of root growth direction in Arabidopsis thaliana. J Exp Bot 65:2981–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MA, Davies PJ (1985) Separation and quantification of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol 78:89–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JA, Benfey PN (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:128–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spalding EP, Wu G, Lewis DR (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  PubMed  PubMed Central  CAS  Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localisation of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    Article  CAS  PubMed  Google Scholar 

  • Strader LC, Bartel B (2008) A new path to auxin. Nat Chem Biol 4:337–339

    Article  CAS  PubMed  Google Scholar 

  • Strader LC, Bartel B (2009) The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Street IH, Aman S, Zubo Y, Ramzan A, Wang X, Shakeel SN, Kieber JJ, Schaller GE (2015) Ethylene inhibits cell proliferation of the Arabidopsis Root Meristem. Plant Physiol 169:338–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Swarup R, Kramer EM, Perry P, Knox K, Leyser HM, Haseloff J, Beemster GT, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7:1057–1065

    Article  CAS  PubMed  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennet MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A (2007) ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48:263–277

    Article  CAS  PubMed  Google Scholar 

  • Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  CAS  PubMed  Google Scholar 

  • Thole JM, Beisner ER, Liu J, Venkova SV, Strader LC (2014) Abscisic acid regulates root elongation through the activities of auxin and ethylene in Arabidopsis thaliana G3-Genes Genomes. Genetics 4:1259–1274

    CAS  Google Scholar 

  • Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P (2009) Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms. PLoS Genet 5:e1000328

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian Q, Nagpal P, Reed JW (2003) Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J 36:643–651

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) Aux/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR, Symonova O et al (2013) 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc Natl Acad Sci USA 110:E1695–E1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Topping JF, Lindsey K (1997) Promoter trap markers differentiate structural and positional components of polar development in Arabidopsis. Plant Cell 9:1713–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J (2006) A map of KNAT gene expression in the Arabidopsis root. Plant Mol Biol 60:1–20

    Article  CAS  PubMed  Google Scholar 

  • Tsurumi S, Wada S (1980) Transport of shoot- and cotyledon-applied indole-3-acetic acid to Vicia faba root. Plant Cell Physiol 21:803–816

    Article  CAS  Google Scholar 

  • Ubeda-Tomas S, Beemster GTS, Bennett MJ (2012) Hormonal regulation of root growth: integrating local activities into global behaviour. Trends Plant Sci 17:326–331

    Article  CAS  PubMed  Google Scholar 

  • van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287–289

    Article  PubMed  CAS  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  CAS  PubMed  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, Inzé 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vellosillo T, Martinez M, Lopez MA, Vicente J, Cascon T, Dolan L, Hamberg M, Castresana C (2007) Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defence responses through a specific signalling cascade. Plant Cell 19:831–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verstraeten I, Schotte S, Geelen D (2014) Hypocotyl adventitious root organogenesis differs from lateral root development. Front Plant Sci 5:495

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieten A, Vanneste S, Wisniewska J, Benkova 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

    Article  CAS  PubMed  Google Scholar 

  • Voegele A, Linkies A, Muller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLININSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62:5131–5147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinohl V, Merks RMH, Govaerts W, Friml J (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005a) Control of root cap formation by Micro RNA targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005b) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID INSENSITIVE1 receptor kinase. Plant Cell 17:1685–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JR, Hu H, Wang GH, Li J, Chen JY, Wu P (2009) Expression of PIN Genes in Rice (Oryza sativa L.): tissue specificity and regulation by hormones. Mol Plant 2:823–831

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Hua D, He J, Duan Y, Chen Z, Hong X, Gong Z (2011) Auxin Response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7:e1002172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson G (2004) Effect of transplanting and paclobutrazol on root growth of ’Green Column’ black maple and ’Summit’ green ash. J Environ Hortic 22:209–212

    Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Onckelen HV, Schmuelling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Wu G, 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. Plant Cell 19:1826–1837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    CAS  PubMed  Google Scholar 

  • Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M (2009) The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol 151:168–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Hao Q, Li W, Yan C, Yan N, Yin P (2014) Identification and characterization of ABA receptors in Oryza sativa. PLoS One 9(4):e95246

    Article  Google Scholar 

  • Zazımalova E, Murphy AS, Yang H, Hoyerova K, Hosek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2:a001552

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Xiong Y, DeFraia C, Schmelz E, Mou Z (2008) The Arabidopsis MAP kinase kinase 7. A crosstalk point between auxin signaling and defense responses? Plant Signal Behav 3:272–274

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Swarup R, Bennett M, Schaller GE, Kieber JJ (2013) Cytokinin induces cell division in the quiescent center of the Arabidopsis root apical meristem. Curr Biol 23:1979–1989

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Xing L, Wang X, Hou Y-J, Gao J, Wang P et al (2014) The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci Signal 7:ra53. https://doi.org/10.1126/scisignal.2005051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. Both authors have equally contributed.

Authors and Affiliations

  1. Department of Botany, SGTB Khalsa College, University of Delhi, Delhi, India

    Priyanka Singla & Surinder Kaur

Authors
  1. Priyanka Singla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Surinder Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Botany, Swami Shraddhanand College, University of Delhi, Delhi, India

    Bhoopander Giri

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ram Prasad

  3. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Singla, P., Kaur, S. (2018). Insights into Pivotal Role of Phytohormonal Cross Talk in Tailoring Underground Plant Root System Architecture. In: Giri, B., Prasad, R., Varma, A. (eds) Root Biology. Soil Biology, vol 52. Springer, Cham. https://doi.org/10.1007/978-3-319-75910-4_1

Download citation

Publish with us

Policies and ethics

Search

Navigation