Plant Cell Reports

, Volume 32, Issue 6, pp 741–757 | Cite as

Auxin: a master regulator in plant root development

  • Shivani Saini
  • Isha Sharma
  • Navdeep Kaur
  • Pratap Kumar PatiEmail author


The demand for increased crop productivity and the predicted challenges related to plant survival under adverse environmental conditions have renewed the interest in research in root biology. Various physiological and genetic studies have provided ample evidence in support of the role of plant growth regulators in root development. The biosynthesis and transport of auxin and its signaling play a crucial role in controlling root growth and development. The univocal role of auxin in root development has established it as a master regulator. Other plant hormones, such as cytokinins, brassinosteroids, ethylene, abscisic acid, gibberellins, jasmonic acid, polyamines and strigolactones interact either synergistically or antagonistically with auxin to trigger cascades of events leading to root morphogenesis and development. In recent years, the availability of biological resources, development of modern tools and experimental approaches have led to the advancement of knowledge in root development. Research in the areas of hormone signal perception, understanding network of events involved in hormone action and the transport of plant hormones has added a new dimension to root biology. The present review highlights some of the important conceptual developments in the interplay of auxin and other plant hormones and associated downstream events affecting root development.


Auxin Root development Plant hormones Crosstalk Signaling Transport 


  1. Abel S, Nguyen MD, Chow W, Theologis A (1995) ASC4, a primary indoleacetic acid responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 270:19093–19099PubMedCrossRefGoogle Scholar
  2. 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 119:109–120PubMedCrossRefGoogle Scholar
  3. 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 USA 100:2992–2997PubMedCrossRefGoogle Scholar
  4. 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 134:1624–1631PubMedCrossRefGoogle Scholar
  5. Benfey PN, Bennett M, Schiefelbein J (2010) Getting to the root of plant biology: impact of the Arabidopsis. Plant J 61:992–1000PubMedCrossRefGoogle Scholar
  6. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465PubMedCrossRefGoogle Scholar
  7. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950PubMedCrossRefGoogle Scholar
  8. Berova M, Zlatev Z (2000) Physiological response and yield of paclobutrazol treated tomato plants (Lycopersicon esculentum Mill.). Plant Growth Regul 30:117–123CrossRefGoogle Scholar
  9. Bielach A, Duclercq J, Marhavý P, Benková E (2012) Genetic approach towards the identification of auxin–cytokinin crosstalk components involved in root development. Phil Trans R Soc B 367:1469–1478PubMedCrossRefGoogle Scholar
  10. Biondi S, Diaz T, Iglesias I, Gamberini G, Bagni N (1990) Polyamines and ethylene in relation to adventitious root formation in Prunus avium shoot cultures. Physiol Plant 78:474–483CrossRefGoogle Scholar
  11. Bishopp A, Benkova E, Helariutta Y (2011) Sending mixed messages: auxin–cytokinin crosstalk in roots. Curr Opin Plant Biol 14:10–16PubMedCrossRefGoogle Scholar
  12. 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 433:39–44PubMedCrossRefGoogle Scholar
  13. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  14. 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 34:67–75PubMedCrossRefGoogle Scholar
  15. Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis thaliana. Plant Physiol 140:1384–1396PubMedCrossRefGoogle Scholar
  16. 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 224:288–299PubMedCrossRefGoogle Scholar
  17. 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 8:165–171PubMedCrossRefGoogle Scholar
  18. Chandler JW (2009) Local auxin production: a small contribution to a big field. BioEssays 31:60–70PubMedCrossRefGoogle Scholar
  19. Chapman EJ, Estelle M (2009) Cytokinin and auxin intersection in root meristems. Genome Biol 10:210. doi: 10.1186/gb-2009-10-2-210 CrossRefGoogle Scholar
  20. 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 and Environment, pp 1–11. doi: 10.1111/pce.12028
  21. Choudhary SP, Yu JQ, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Benefits of brassinosteroid crosstalk. Trends Plant Sci 17:594–605PubMedCrossRefGoogle Scholar
  22. Chung Y et al (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J 66:564–578PubMedCrossRefGoogle Scholar
  23. Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–60PubMedCrossRefGoogle Scholar
  24. Coudert Y, Pe′rin C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226PubMedCrossRefGoogle Scholar
  25. Couee I, Hummel I, Sulmon C, Gouesbet G, Amrani AE (2004) Involvement of polyamines in root development. Plant Cell, Tissue Organ Cult 76:1–10CrossRefGoogle Scholar
  26. 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 18:308–320PubMedCrossRefGoogle Scholar
  27. Davies PJ (2010) Plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones. Springer, Netherlands, pp 1–15CrossRefGoogle Scholar
  28. De Dorlodot S, Forster B, Page`s L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481PubMedCrossRefGoogle Scholar
  29. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555PubMedCrossRefGoogle Scholar
  30. De Smet I, White PJ, Bengough AG, Dupuy L, Parizot B, Casimiro I, Heidstra R, Laskowski M, Lepetit M, Hochholdinge F, Draye X, Zhang H, Broadley MR, Peret B, Hammond JP, Fukaki H, Mooney S, Lynch JP, Nacry P, Schurr U, Laplaze L, Benfey P, Beeckman T, Bennett M (2012) Analyzing lateral root development: how to move forward. Plant Cell 24:15–20PubMedCrossRefGoogle Scholar
  31. 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 17:678–682PubMedCrossRefGoogle Scholar
  32. 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 322:1380–1384PubMedCrossRefGoogle Scholar
  33. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445PubMedCrossRefGoogle Scholar
  34. Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J, Paciorek T, Petrasek J, Seifertova′ D, Tejos R, Meisel LA, Zazımalova′ E, Gadella TWJ, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. PNAS 105:4489–4494PubMedCrossRefGoogle Scholar
  35. Dill A, Sun T (2001) Synergistic derepression of gibberellins signalling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785PubMedGoogle Scholar
  36. Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85PubMedCrossRefGoogle Scholar
  37. Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706PubMedCrossRefGoogle Scholar
  38. Fowler MR, Kirby MJ, Scott NW, Slater A, Elliott MC (1996) Polyamine metabolism and gene regulation during the transition of autonomous sugar beet cell in suspension culture from quiescence to division. Physiol Plant 98:439–446CrossRefGoogle Scholar
  39. 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 142:553–563PubMedCrossRefGoogle Scholar
  40. Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellins response. Nature 421:740–743PubMedCrossRefGoogle Scholar
  41. 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 29:153–168PubMedCrossRefGoogle Scholar
  42. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transportby AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  43. Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102PubMedCrossRefGoogle Scholar
  44. Gou J, Strauss SH, Tsai CJ, Kai F, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639PubMedCrossRefGoogle Scholar
  45. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276PubMedCrossRefGoogle Scholar
  46. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460PubMedCrossRefGoogle Scholar
  47. Guilfoyle T, Hagen G, Ulmasov T, Murfett J (1998a) How does auxins turn on genes? Plant Physiol 118:341–347PubMedCrossRefGoogle Scholar
  48. Guilfoyle TJ, Ulmasov T, Hagen G (1998b) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54:619–627PubMedCrossRefGoogle Scholar
  49. Gupta S, Rashotte AM (2012) Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep 31:801–812PubMedCrossRefGoogle Scholar
  50. Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic Acid homeostasis. Plant cell 24:2515–2527PubMedCrossRefGoogle Scholar
  51. 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 138:839–848PubMedCrossRefGoogle Scholar
  52. Hacham Y et al (2012) BRI1 activity in the root meristem involves post-transcriptional regulation of PIN auxin efflux carriers. Plant Signal Behav 7:68–70PubMedCrossRefGoogle Scholar
  53. Haecker A, Groß-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668PubMedCrossRefGoogle Scholar
  54. Hardtke CS, Dorcey E, Osmont KS, Sibout R (2007) Phytohormone collaboration: zooming in on auxin–brassinosteroid interactions. Trends Cell Biol 17:485–492PubMedCrossRefGoogle Scholar
  55. Hausman JF, Kevers C, Gaspar T (1994) Auxin–polyamine interaction in the control of the rooting inductive phase of poplar shoots in vitro. Plant Sci 110:63–71CrossRefGoogle Scholar
  56. He JX, Gendron JM, Yang Y, Li J, Wang ZY (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 99:10185–10190PubMedCrossRefGoogle Scholar
  57. Heloir M, Kevers C, Hausman J, Gaspar T (1996) Changes in the concentration of auxins and polyamines during rooting of in vitro-propagated walnut shoots. Tree Physiol 16:515–519PubMedCrossRefGoogle Scholar
  58. Hennion F, Martin-Tanguy J (2000) Amines of the subantarctic crucifer Pringlea antiscorbutica are responsive to temperature conditions. Physiol Plant 109:232–243CrossRefGoogle Scholar
  59. Hummel I, Couée 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 53:1463–1473PubMedCrossRefGoogle Scholar
  60. Itoh H, Matsuoka M, Steber CM (2003) A role for the ubiquitin 26S proteasome pathway in gibberellins signalling. Trends Plant Sci 8:492–497PubMedCrossRefGoogle Scholar
  61. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene–auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347PubMedCrossRefGoogle Scholar
  62. Jang SJ, Choi YJ, Park KY (2002) Effects of polyamines on shoot and root development in Arabidopsis seedlings and carnation cultures. Plant Biol J 45:230–236CrossRefGoogle Scholar
  63. Jones B, Gunnera SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22:2956–2969PubMedCrossRefGoogle Scholar
  64. Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Sejalon-Delmas N, Combier JP, Becard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216PubMedCrossRefGoogle Scholar
  65. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451PubMedCrossRefGoogle Scholar
  66. Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399–1409PubMedCrossRefGoogle Scholar
  67. Kieber JJ, Schaller GE (2010) The Perception of Cytokinin: a story 50 years in the making. Plant Physiol 154:487–492PubMedCrossRefGoogle Scholar
  68. 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):773Google Scholar
  69. King KE, Mortiz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159:767–776PubMedGoogle Scholar
  70. Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu rev cell bio 24:447–473CrossRefGoogle Scholar
  71. Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM independent trafficking in Arabidopsis. Plant cell 21:3839–3849PubMedCrossRefGoogle Scholar
  72. Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130:5769–5777PubMedCrossRefGoogle Scholar
  73. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549PubMedCrossRefGoogle Scholar
  74. Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bahattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136CrossRefGoogle Scholar
  75. Kovtun Y, Chiu WL, Zeng W, Sheen J (1998) Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395:716–720PubMedCrossRefGoogle Scholar
  76. Kramer EM, Bennett MJ (2006) Auxin transport: a field in flux. Trends Plant Sci 11:382–386PubMedCrossRefGoogle Scholar
  77. Kuppusamy KT, Chen AY, Nemhauser JL (2009) Steroids are required for epidermal cell fate establishment in Arabidopsis roots. Proc Natl Acad Sci USA 106:8073–8076PubMedCrossRefGoogle Scholar
  78. Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium dependent protein kinases are involved in nitric oxide- and auxininduced adventitious root formation in cucumber. J Exp Bot 57:1341–1351PubMedCrossRefGoogle Scholar
  79. Lau S, Shao N, Bock R, Jurgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188PubMedCrossRefGoogle Scholar
  80. 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 125:519–522PubMedCrossRefGoogle Scholar
  81. 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 57:975–985PubMedCrossRefGoogle Scholar
  82. Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19:1838–1850PubMedCrossRefGoogle Scholar
  83. 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 138:3485–3495PubMedCrossRefGoogle Scholar
  84. Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-Like Kinase. Science 295:1299–1301PubMedGoogle Scholar
  85. 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 17:2738–2753PubMedCrossRefGoogle Scholar
  86. Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400PubMedCrossRefGoogle Scholar
  87. 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 17:1090–1104PubMedCrossRefGoogle Scholar
  88. Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic Publishers, Dordrecht, Boston, pp 509–530Google Scholar
  89. Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187PubMedCrossRefGoogle Scholar
  90. Maharjan PM, Schulz B, Choe S (2011) BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis. J Plant Biol 54:126–134CrossRefGoogle Scholar
  91. Mano Y, Nemoto K (2012) The pathway of a auxin biosynthesis in plants. J Exp Bot. doi: 10.1093jxb/ers091 PubMedGoogle Scholar
  92. 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 17:3007–3018PubMedCrossRefGoogle Scholar
  93. 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 8:1505–1517PubMedGoogle Scholar
  94. 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 55:375–378CrossRefGoogle Scholar
  95. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056PubMedCrossRefGoogle Scholar
  96. Mochaitis K, Estelle M (2008) Auxin receptors and plant development: a new signalling paradigm. Annu Rev Cell Dev Biol 24:55–80CrossRefGoogle Scholar
  97. 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 15:2979–2991PubMedCrossRefGoogle Scholar
  98. 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 66:129–136CrossRefGoogle Scholar
  99. Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid and auxin signalling in root growth. Nature 443:458–461PubMedCrossRefGoogle Scholar
  100. Mravec J, Petrásek J, Li N, Boeren S, Karlova R, Kitakura S, Parezová M, Naramoto S, Nodzynski T, Dhonukshe P, Bednarek SY, Zazímalová E, De Vries S, Friml J (2011) Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr Biol 21:1055–1060PubMedCrossRefGoogle Scholar
  101. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195PubMedCrossRefGoogle Scholar
  102. Muller B (2011) Generic signal-specific responses: cytokinin and context-dependent cellular responses. J Exp Bot 62:3273–3288PubMedCrossRefGoogle Scholar
  103. Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463PubMedCrossRefGoogle Scholar
  104. Naija S, Elloumi N, Ammar S, Kevers C, Dommes J (2009) Involvement of polyamines in the adventitious rooting of micropropagated shoots of the apple rootstock MM106. J In Vitro Cell Dev Biol Plant 45:83–91CrossRefGoogle Scholar
  105. 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 45:193–205PubMedCrossRefGoogle Scholar
  106. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187PubMedCrossRefGoogle Scholar
  107. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15PubMedCrossRefGoogle Scholar
  108. Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2:a001594PubMedCrossRefGoogle Scholar
  109. O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982PubMedCrossRefGoogle Scholar
  110. Okushima Y, Fukaki H, Onoda M, Teologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct avtivation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130PubMedCrossRefGoogle Scholar
  111. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113PubMedCrossRefGoogle Scholar
  112. Ouyang J, Shao X, Li J (2000) Indole-3-glycerol phosphate, a branchpoint of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant J 24:327–333PubMedCrossRefGoogle Scholar
  113. Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2(6):a001537PubMedCrossRefGoogle Scholar
  114. 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 28:565–572Google Scholar
  115. Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177PubMedCrossRefGoogle Scholar
  116. Pati PK, Sharma M, Nagar PK (2010) The Role of Polyamines during Rhizogenesis. In: Advances in Plant Physiol- An Int. Treatise Series Vol 12: Edited by A. Hemantaranjan, Scientific Pub., India. pp 390–414Google Scholar
  117. Péret 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 14:399–408PubMedCrossRefGoogle Scholar
  118. Perilli S, Moubayidin L, Sabatini S (2010) The molecular basis of cytokinin function. Curr Opin Plant Biol 13:21–26PubMedCrossRefGoogle Scholar
  119. Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94:1462–1466PubMedCrossRefGoogle Scholar
  120. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560PubMedCrossRefGoogle Scholar
  121. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE gene. Plant J 18:111–119PubMedCrossRefGoogle Scholar
  122. Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, Dupont-Gillian CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733PubMedCrossRefGoogle Scholar
  123. Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453PubMedCrossRefGoogle Scholar
  124. 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 42:301–307PubMedCrossRefGoogle Scholar
  125. Ramos JA, Zener N, Leyser O, Callis J (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13:2349–2360PubMedGoogle Scholar
  126. Riefler M, Novak O, Strnad M, Schmullinga T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, cytokinin metabolism. Plant Cell 18:40–54PubMedCrossRefGoogle Scholar
  127. Rock CD, Sun X (2005) Crosstalk between ABA and auxin signalling pathways in roots of Arabidopsis thaliana (L.) Heynh. Planta 222:98–106PubMedCrossRefGoogle Scholar
  128. Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12:198–207PubMedCrossRefGoogle Scholar
  129. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester HJ (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734PubMedCrossRefGoogle Scholar
  130. 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 19:2197–2212PubMedCrossRefGoogle Scholar
  131. Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521PubMedCrossRefGoogle Scholar
  132. Santner A, Mark Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078PubMedCrossRefGoogle Scholar
  133. 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 456:520–523PubMedCrossRefGoogle Scholar
  134. 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 22:3560–3573PubMedCrossRefGoogle Scholar
  135. Silverstone AL, Chang CW, Krol E, Sun TP (1997) Developmental regulation of the gibberellins biosynthetic gene GAI1 in Arabidopsis thaliana. Plant J 12:9–19PubMedCrossRefGoogle Scholar
  136. Slade WO, Ray WK, Patricia M, Williams PM, Winkel BSJ, Helm RF (2012) Effects of exogenous auxin and ethylene on the Arabidopsis root proteome. Phytochemistry 84:18–23PubMedCrossRefGoogle Scholar
  137. Smith MA, Davies PJ (1985) Separation and quantification of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol 78:89–91PubMedCrossRefGoogle Scholar
  138. 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 17:2230–2242PubMedCrossRefGoogle Scholar
  139. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185PubMedCrossRefGoogle Scholar
  140. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Doležal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191PubMedCrossRefGoogle Scholar
  141. Strader LC, Bartel B (2008) A new path to auxin. Nat Chem Biol 4:337–339PubMedCrossRefGoogle Scholar
  142. 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 21:1495–1511PubMedCrossRefGoogle Scholar
  143. 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 15:2648–2653PubMedCrossRefGoogle Scholar
  144. Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49:411–426PubMedCrossRefGoogle Scholar
  145. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennet MJ (2007) Ethlene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196PubMedCrossRefGoogle Scholar
  146. Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and deetiolation in Arabidopsis. Cell 85:171–182PubMedCrossRefGoogle Scholar
  147. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386PubMedCrossRefGoogle Scholar
  148. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138:1117–1125PubMedCrossRefGoogle Scholar
  149. Tassoni A, Van Buuren M, Franceschetti M, Fornalè S, Bagni N (2000) Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiol Biochem 38:383–393CrossRefGoogle Scholar
  150. 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 7:847–859PubMedCrossRefGoogle Scholar
  151. Tian Q, Nagpal P, Reed JW (2003) Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J 36:643–651PubMedCrossRefGoogle Scholar
  152. 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 13:2809–2822PubMedGoogle Scholar
  153. To JP, Kieber JJ (2008) Cytokinin signalling: two-components and more. Trends Plant Sci 13:85–92PubMedCrossRefGoogle Scholar
  154. 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 signalling. Plant Cell 16:658–671PubMedCrossRefGoogle Scholar
  155. Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628PubMedCrossRefGoogle Scholar
  156. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698PubMedCrossRefGoogle Scholar
  157. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016PubMedCrossRefGoogle Scholar
  158. 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 19:831–846PubMedCrossRefGoogle Scholar
  159. Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin transport-mediated development. Trends Plant Sci 12:160–168PubMedCrossRefGoogle Scholar
  160. Voegele A, Linkies A, Muller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Expt Bot 62:5131–5147CrossRefGoogle Scholar
  161. Walker L, Estelle M (1998) Molecular mechanisms of auxin action. Curr Opin Plant Biol 1:434–439PubMedCrossRefGoogle Scholar
  162. Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID INSENSITIVE1 receptor kinase. Plant Cell 17:1685–1703PubMedCrossRefGoogle Scholar
  163. 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 2:823–831PubMedCrossRefGoogle Scholar
  164. 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:e1002172PubMedCrossRefGoogle Scholar
  165. Watson MB, Emory KK, Piatak RM, Malmberg RL (1998) Arginine decarboxylase (polyamine synthesis) mutants of Arabidopsis thaliana exhibit altered root growth. Plant J 13:231–239PubMedCrossRefGoogle Scholar
  166. Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538PubMedCrossRefGoogle Scholar
  167. 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 23:2184–2195PubMedCrossRefGoogle Scholar
  168. Wilson AK, Pickett BF, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383PubMedCrossRefGoogle Scholar
  169. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735PubMedCrossRefGoogle Scholar
  170. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117PubMedCrossRefGoogle Scholar
  171. Yang YK, Lee SY, Park WT, Park NI, Park SU (2010) Exogenous auxins and polyamines enhance growth and rosmarinic acid production in hairy root cultures of Nepeta cataria L. Plant Omics 3:190–193Google Scholar
  172. Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600PubMedCrossRefGoogle Scholar
  173. Zazímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P (2010) Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2:a001552PubMedCrossRefGoogle Scholar
  174. Zener N, Ellsmore A, Leasure C, Callis J (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci USA 98:11795–11800CrossRefGoogle Scholar
  175. Zhang R, Wang B, Ouyang J, Li J, Wang Y (2008a) Arabidopsis indole synthase, a homolog of tryptophan synthase alpha, is an enzyme involved in the Trp-independent indole-containing metabolite biosynthesis. J Integr Plant Biol 50:1070–1077PubMedCrossRefGoogle Scholar
  176. Zhang X, Xiong Y, DeFraia C, Schmelz E, Mou Z (2008b) The Arabidopsis MAP kinase kinase 7. A crosstalk point between auxin signaling and defense responses? Plant Signal Behav 3:272–274PubMedCrossRefGoogle Scholar
  177. Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112Google Scholar
  178. Zhao Y, Hu Y, Dai M, Huang L, Zhou DX (2009) The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21:736–748PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Shivani Saini
    • 1
  • Isha Sharma
    • 1
  • Navdeep Kaur
    • 1
  • Pratap Kumar Pati
    • 1
    Email author
  1. 1.Department of BiotechnologyGuru Nanak Dev UniversityAmritsarIndia

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