Skip to main content
SpringerLink
Log in

Evolutionary Aspects of Auxin Signalling

  • Chapter
  • First Online:
Auxin and Its Role in Plant Development

Abstract

Auxin is one of the first phytohormones to be discovered in plants. It plays a key role in plant growth and development and in the evolution of land plants. The presence of auxin has been reported from microalgae to higher seed plants. However, tracing the origin of auxin response and of the associated proteins has proven to be more difficult. This chapter will summarize recent molecular developments on the origin of auxin metabolism, transport and signalling in green, red and brown algae, mosses and spikemosses.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Abe H, Uchiyama M, Sato R (1972) Isolation and identification of native auxins in marine algae. Agric Biol Chem 36(12):2259–2260

    CAS  Google Scholar 

  • Abel S, Theologis A (2010) Odyssey of auxin. Cold Spring Harb Perspect Biol 2:a004572. doi:10.1101/cshperspect.a004572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arteca RN (1995) Plant growth substances: principles and applications. Chapman & Hall, USA

    Google Scholar 

  • Ashton NW, Grimsley NH, Cove DJ (1979) Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144(5):427–435. doi:10.1007/bf00380118

    CAS  PubMed  Google Scholar 

  • Bainbridge K, Guyomarc’h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22(6):810–823. doi:10.1101/gad.462608

    CAS  PubMed Central  PubMed  Google Scholar 

  • Band LR, King JR (2012) Multiscale modelling of auxin transport in the plant-root elongation zone. J Math Biol 65(4):743–785. doi:10.1007/s00285-011-0472-y

    CAS  PubMed  Google Scholar 

  • Banks JA (2009) Selaginella and 400 million years of separation. Annu Rev Plant Biol 60:223–238. doi:10.1146/annurev.arplant.59.032607.092851

    CAS  PubMed  Google Scholar 

  • Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, de Pamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LGG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga SI, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riaño-Pachón DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sørensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theißen G, Ulvskov P, Wakazuki S, Weng JK, Willats WWGT, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loqué D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332(6032):960–963. doi:10.1126/science.1203810

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barbez E, Kubeš M, Rolčík J, Beziat C, Pěnčík A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zažímalová E, Petrášek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485(7396):119–122. doi:10.1038/nature11001

    CAS  PubMed  Google Scholar 

  • Basu S (2002) Early embryo development in fucus distichus is auxin sensitive. Plant Physiol 130(1):292–302. doi:10.1104/pp. 004747

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bateman RM, DiMichele WA (1994) Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Biol Rev 69(3):345–417. doi:10.1111/j.1469-185X.1994.tb01276.x

    Google Scholar 

  • Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103(7):999–1004. doi:10.1093/aob/mcp044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465. doi:10.1146/annurev.arplant.58.032806.103805

    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(5):591–602. doi:10.1016/S0092-8674(03)00924-3

    CAS  PubMed  Google Scholar 

  • Bennett T, Scheres B (2010) Chapter Three – Root development—two meristems for the price of one? In: Marja CPT (ed) Current topics in developmental biology, vol 91. Academic Press, USA, pp 67–102. doi:10.1016/S0070-2153(10)91003-X

  • 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 (New York, NY) 273(5277):948–950. doi:10.1126/science.273.5277.948

    CAS  Google Scholar 

  • Bierfreund NM, Reski R, Decker EL (2003) Use of an inducible reporter gene system for the analysis of auxin distribution in the moss Physcomitrella patens. Plant Cell Rep 21(12):1143–1152. doi:10.1007/s00299-003-0646-1

    CAS  PubMed  Google Scholar 

  • Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147. doi:10.1105/tpc.106.040782

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bogaert KA, Arun A, Coelho SM, Clerck O (2013) Brown algae as a model for plant organogenesis. Methods Mol Biol 959:97–125. doi:10.1007/978-1-62703-221-6_6

    PubMed  Google Scholar 

  • Boot KJ, Libbenga KR, Hille SC, Offringa R, van Duijn B (2012) Polar auxin transport: an early invention. J Exp Bot 63(11):4213–4218. doi:10.1093/jxb/ers106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bosco CD, Dovzhenko A, Liu X, Woerner N, Rensch T, Eismann M, Eimer S, Hegermann J, Paponov IA, Ruperti B, Heberle-Bors E, Touraev A, Cohen JD, Palme K (2012) The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis. Plant J 71(5):860–870. doi:10.1111/j.1365-313X.2012.05037.x

    Google Scholar 

  • Boysen Jensen P, Nielsen N (1925) Studien über die hormonalen Beziehungen zwischen Spitze und Basis der Avenacoleoptile. Planta 1(3):321–331. doi:10.1007/bf02039223

    Google Scholar 

  • Bradley PM (1991) Plant hormones do have a role in controlling growth and development of algae. J Phycol 27(3):317–321. doi:10.1111/j.0022-3646.1991.00317.x

    CAS  Google Scholar 

  • Braun N, Wyrzykowska J, Muller P, David K, Couch D, Perrot-Rechenmann C, Fleming AJ (2008) Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell 20(10):2746–2762. doi:10.1105/tpc.108.059048

    CAS  PubMed Central  PubMed  Google Scholar 

  • Calderon Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L, Sheard LB, Tan X, Parry G, Mao H, Zheng N, Napier R, Kepinski S, Estelle M (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8(5):477–485. doi:10.1038/nchembio.926

    CAS  PubMed  Google Scholar 

  • Calderon-Villalobos LI, Tan X, Zheng N, Estelle M (2010) Auxin perception—structural insights. Cold Spring Harb Perspect Biol 2(7):a005546. doi:10.1101/cshperspect.a005546

    PubMed Central  PubMed  Google Scholar 

  • Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci U S A 95(25):15112–15117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen X, Naramoto S, Robert S, Tejos R, Lofke C, Lin D, Yang Z, Friml J (2012) ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr Biol 22(14):1326–1332. doi:10.1016/j.cub.2012.05.020

    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. doi:10.1101/gad.1415106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho M, Cho HT (2012) The function of ABCB transporters in auxin transport. Plant Signal Behav 8(2):e22990. doi:10.4161/psb.22990

    PubMed Central  PubMed  Google Scholar 

  • Christie JM, Murphy AS (2013) Shoot phototropism in higher plants: new light through old concepts. Am J Bot 100(1):35–46. doi:10.3732/ajb.1200340

    CAS  PubMed  Google Scholar 

  • Ciesielski T (1871) Untersuchungen über die Abwärtskrümmung der Wurzel. [s.n.], Breslau

    Google Scholar 

  • Cock JM, SterckL RP, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collén J, Corre E, Silva CD, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CMM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper FC, Lang D, Bail AL, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collén P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Ségurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, Dassow PV, Yamagishi T, de Peer YV, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621

    CAS  PubMed  Google Scholar 

  • Conrad H, Saltman P, Eppley R (1959) Effects of auxin and gibberellic acid on growth of ulothrix. Nature 184(4685):556–557. doi:10.1038/184556a0

    CAS  PubMed  Google Scholar 

  • Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49(3–4):319–338. doi:10.1023/A:1015242627321

    CAS  PubMed  Google Scholar 

  • Darwin C (1880) The power of movement in plants. John Murray, London

    Google Scholar 

  • Davies P (2010) The plant hormones: their nature, occurrence, and functions. In: Davies P (ed) Plant hormones. Springer, Netherlands, pp 1–15. doi:10.1007/978-1-4020-2686-7_1

    Google Scholar 

  • de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14(3):267–277. doi:10.1094/MPMI.2001.14.3.267

    PubMed  Google Scholar 

  • De Meutter J, Tytgat T, Prinsen E, Gheysen G, Van Onckelen H (2005) Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Commun Agric Appl Biol Sci 70(1):51–60

    PubMed  Google Scholar 

  • de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C, Traas J (2006) Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci U S A 103(5):1627–1632. doi:10.1073/pnas.0510130103

    PubMed Central  PubMed  Google Scholar 

  • De Smet I, Lau S, Mayer U, Jürgens G (2010) Embryogenesis – the humble beginnings of plant life. Plant J 61(6):959–970. doi:10.1111/j.1365-313X.2010.04143.x

    PubMed  Google Scholar 

  • De Smet I, Voβ U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jürgens G, Beeckman T (2011) Unraveling the evolution of auxin signaling. Plant Physiol 155(1):209–221, doi:pp.110.168161 [pii]

    PubMed Central  PubMed  Google Scholar 

  • Decker EL, Frank W, Sarnighausen E, Reski R (2006) Moss systems biology en route: phytohormones in Physcomitrella development. Plant Biol (Stuttg) 8(3):397–405. doi:10.1055/s-2006-923952

    CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435(7041):441–445. doi:10.1038/nature03543

    CAS  PubMed  Google Scholar 

  • Ding Z, Wang B, Moreno I, Dupláková N, Simon S, Carraro N, Reemmer J, Pěnčík A, Chen X, Tejos R, Skůpa P, Pollmann S, Mravec J, Petrášek J, Zažímalová E, Honys D, Rolčík J, Murphy A, Orellana A, Geisler M, Friml J (2012) ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat Commun 3:941. doi:10.1038/ncomms1941

    PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eklund DM, Thelander M, Landberg K, Ståldal V, Nilsson A, Johansson M, Valsecchi I, Pederson ERA, Kowalczyk M, Ljung K, Ronne H, Sundberg E (2010) Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens. Development 137(8):1275–1284. doi:10.1242/dev.039594

    CAS  PubMed  Google Scholar 

  • Evans LV, Trewavas AJ (1991) Is algal development controlled by plant growth substances? J Phycol 27(3):322–326. doi:10.1111/j.0022-3646.1991.00322.x

    CAS  Google Scholar 

  • Feller C, Gabriel JP, Mazza C, Yerly F (2013) Pattern formation in auxin flux. J Math Biol 23:23. doi:10.1007/s00285-013-0655-9

    Google Scholar 

  • Feraru E, Vosolsobě S, Feraru MI, Petrášek J, Kleine-Vehn J (2012) Evolution and structural diversification of PILS putative auxin carriers in plants. Front Plant Sci 3:227. doi:10.3389/fpls.2012.00227

    PubMed Central  PubMed  Google Scholar 

  • Finet C, Jaillais Y (2012) Auxology: when auxin meets plant evo-devo. Dev Biol 369(1):19–31. doi:10.1016/j.ydbio.2012.05.039S0012-1606(12)00309-0

    CAS  PubMed  Google Scholar 

  • Finet C, Timme RE, Delwiche CF, Marlétaz F (2010) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20(24):2217–2222. doi:10.1016/j.cub.2010.11.035

    CAS  PubMed  Google Scholar 

  • Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002a) AtPIN4 mediates sink-driven auxin gradients and root patterning in arabidopsis. Cell 108(5):661–673. doi:10.1016/S0092-8674(02)00656-6

    CAS  PubMed  Google Scholar 

  • Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002b) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415(6873):806–809. doi:10.1038/415806a

    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(6963):147–153. doi:10.1038/nature02085

    CAS  PubMed  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421(6924):740–743. doi:10.1038/nature01387

    CAS  PubMed  Google Scholar 

  • Fujita T, Hasebe M (2009) Convergences and divergences in polar auxin transport and shoot development in land plant evolution. Plant Signal Behav 4(4):313–315. doi:10.4161/psb.4.4.8090

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M (2008) Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evol Dev 10(2):176–186. doi:10.1111/j.1525-142X.2008.00225.x

    CAS  PubMed  Google Scholar 

  • Gagne JM, Downes BP, Shiu S-H, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci 99(17):11519–11524. doi:10.1073/pnas.162339999

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282(5397):2226–2230. doi:10.1126/science.282.5397.2226

    PubMed  Google Scholar 

  • Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580(4):1094–1102. doi:10.1016/j.febslet.2005.11.054

    CAS  PubMed  Google Scholar 

  • Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci 97(9):4535–4540. doi:10.1073/pnas.97.9.4535

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gruen HE (1959) Auxins and fungi. Annu Rev Plant Physiol Plant Mol Biol 10:405–440. doi:10.1146/annurev.pp. 10.060159.002201

    CAS  Google Scholar 

  • Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29(16):2700–2714. doi:10.1038/emboj.2010.181

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ha CM, Jun JH, Fletcher JC (2010) Chapter Four – Shoot apical meristem form and function. In: Marja CPT (ed) Current topics in developmental biology, vol 91. Academic Press, USA, pp 103–140. doi:10.1016/S0070-2153(10)91004-1

  • Haagen-Smit A, Dandliker W, Wittwer S, Murneek A (1946) Isolation of 3-indoleacetic acid from immature corn kernels. Am J Bot 33:118–120. doi:10.2307/2437327

    CAS  Google Scholar 

  • Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53(6):965–975. doi:10.1093/pcp/pcs035

    CAS  PubMed  Google Scholar 

  • Hayashi K-I, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H (2008) Small-molecule agonists and antagonists of F-box protein–substrate interactions in auxin perception and signaling. Proc Natl Acad Sci 105(14):5632–5637. doi:10.1073/pnas.0711146105

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heisler MG, Jönsson H (2006) Modeling auxin transport and plant development. J Plant Growth Regul 25(4):302–312. doi:10.1007/s00344-006-0066-x

    CAS  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15(21):1899–1911. doi:10.1016/j.cub.2005.09.052

    CAS  PubMed  Google Scholar 

  • Hochholdinger F, Wulff D, Reuter K, Park WJ, Feix G (2000) Tissue-specific expression of AUX1 in maize roots. J Plant Physiol 157(3):315–319. doi:10.1016/S0176-1617(00)80053-X

    CAS  Google Scholar 

  • Hošek P, Kubeš M, Laňková M, Dobrev PI, Klima P, Kohoutová M, Petrášek J, Hoyerová K, Jiřina M, Zažímalová E (2012) Auxin transport at cellular level: new insights supported by mathematical modelling. J Exp Bot 63(10):3815–3827. doi:10.1093/jxb/ers074

    PubMed Central  PubMed  Google Scholar 

  • Ichimura H, Yamaki T (1975) Indole-3-acetic acid in chick embryos. Dev Growth Differ 17(3):275–279. doi:10.1111/j.1440-169X.1975.00275.x

    CAS  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. doi:10.1038/ncb1879

    CAS  PubMed  Google Scholar 

  • Isenbarger TA, Carr CE, Johnson SS, Finney M, Church GM, Gilbert W, Zuber MT, Ruvkun G (2008) The most conserved genome segments for life detection on earth and other planets. Orig Life Evol Biosph 38(6):517–533. doi:10.1007/s11084-008-9148-z

    CAS  PubMed  Google Scholar 

  • Jacobs WP (1950) Auxin effects in bryopsis. Biol Bull 99(2):369–370

    CAS  PubMed  Google Scholar 

  • Jacobs WP, Falkenstein K, Hamilton RH (1985) Nature and amount of auxin in algae: IAA from extracts of Caulerpa paspaloides (Siphonales). Plant Physiol 78(4):844–848. doi:10.1104/pp. 78.4.844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jang G, Dolan L (2011) Auxin promotes the transition from chloronema to caulonema in moss protonema by positively regulating PpRSL1and PpRSL2 in Physcomitrella patens. New Phytol 192(2):319–327. doi:10.1111/j.1469-8137.2011.03805.x

    CAS  PubMed  Google Scholar 

  • Johri MM, Desai S (1973) Auxin regulation of caulonema formation in moss protonema. Nat New Biol 245:1. doi:10.1038/newbio245223a0

    Google Scholar 

  • Jones AM, Herman EM (1993) KDEL-containing auxin-binding protein is secreted to the plasma membrane and cell wall. Plant Physiol 101(2):595–606. doi:10.1104/pp. 101.2.595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84. doi:10.1038/ncb1815

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A 103:1633–1638. doi:10.1073/pnas.0509839103

    PubMed Central  PubMed  Google Scholar 

  • Kai K, Horita J, Wakasa K, Miyagawa H (2007) Three oxidative metabolites of indole-3-acetic acid from Arabidopsis thaliana. Phytochemistry 68(12):1651–1663. doi:10.1016/j.phytochem.2007.04.030

    CAS  PubMed  Google Scholar 

  • Kamimoto Y, Terasaka K, Hamamoto M, Takanashi K, Fukuda S, Shitan N, Sugiyama A, Suzuki H, Shibata D, Wang B, Pollmann S, Geisler M, Yazaki K (2012) Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol 53(12):2090–2100. doi:10.1093/pcp/pcs149

    CAS  PubMed  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294(5550):2351–2353. doi:10.1126/science.1065156

    CAS  PubMed  Google Scholar 

  • Kenrick P, Wellman CH, Schneider H, Edgecombe GD (2012) A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic. Philos Trans R Soc Lond B Biol Sci 367(1588):519–536. doi:10.1098/rstb.2011.0271

    PubMed Central  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435(7041):446–451. doi:10.1038/nature03542

    CAS  PubMed  Google Scholar 

  • Koepfli JB, Thimann KV, Went FW (1938) Phytohormones: structure and physiological activity. I. J Biol Chem 122(3):763–780

    CAS  Google Scholar 

  • Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10(12):249, doi:gb-2009-10-12-249 [pii]10.1186/gb-2009-10-12-249

    PubMed Central  PubMed  Google Scholar 

  • Kubeš M, Yang H, Richter GL, Cheng Y, Mlodzinska E, Wang X, Blakeslee JJ, Carraro N, Petrášek J, Zažímalová E, Hoyerová K, Peer WA, Murphy AS (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J 69(4):640–654. doi:10.1111/j.1365-313X.2011.04818.x

    PubMed  Google Scholar 

  • Lau S, Jurgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20(7):1738–1746. doi:10.1105/tpc.108.060418

    CAS  PubMed Central  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(4):182–188. doi:10.1016/j.tplants.2009.01.004

    CAS  PubMed  Google Scholar 

  • Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153(1):128–144. doi:10.1104/pp. 109.149708

    PubMed Central  PubMed  Google Scholar 

  • Lehmann T, Hoffmann M, Hentrich M, Pollmann S (2010) Indole-3-acetamide-dependent auxin biosynthesis: a widely distributed way of indole-3-acetic acid production? Eur J Cell Biol 89(12):895–905, doi:S0171-9335(10)00135-4 [pii]

    CAS  PubMed  Google Scholar 

  • Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91(10):1535–1556. doi:10.3732/ajb.91.10.1535

    PubMed  Google Scholar 

  • Leyser O (2011) Auxin, self-organisation, and the colonial nature of plants. Curr Biol 21(9):R331–R337, doi:S0960-9822(11)00222-3 [pii]

    CAS  PubMed  Google Scholar 

  • Litwack G (2005) Plant hormones. Elsevier Academic Press Inc, USA

    Google Scholar 

  • Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140(5):943–950. doi:10.1242/dev.086363

    CAS  PubMed  Google Scholar 

  • Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312(5779):1520–1523. doi:10.1126/science.1123841

    CAS  PubMed  Google Scholar 

  • Ludwig-Mueller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62(6):1757–1773. doi:10.1093/jxb/erq412

    CAS  Google Scholar 

  • Ludwig-Muller J, Julke S, Bierfreund NM, Decker EL, Reski R (2009) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181(2):323–338. doi:10.1111/j.1469-8137.2008.02677.x

    PubMed  Google Scholar 

  • 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(14):2175–2187. doi:10.1101/gad.12.14.2175

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63(8):2853–2872. doi:10.1093/jxb/ers091

    CAS  PubMed  Google Scholar 

  • Maraschin Fdos S, Memelink J, Offringa R (2009) Auxin-induced, SCF(TIR1)-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59(1):100–109. doi:10.1111/j.1365-313X.2009.03854.x

    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. doi:10.1105/tpc.010354

    CAS  PubMed Central  PubMed  Google Scholar 

  • Merks RM, Van de Peer Y, Inze D, Beemster GT (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390. doi:10.1016/j.tplants.2007.08.004

    CAS  PubMed  Google Scholar 

  • Mjolsness E (2006) The growth and development of some recent plant models: a viewpoint. J Plant Growth Regul 25(4):270–277. doi:10.1007/s00344-006-0069-7

    CAS  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80. doi:10.1146/annurev.cellbio.23.090506.123214

    CAS  PubMed  Google Scholar 

  • Monroe-Augustus M, Zolman BK, Bartel B (2003) IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15(12):2979–2991. doi:10.1105/tpc.017046

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, Skupa P, Chand S, Benkova E, Zazimalova E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354. doi:10.1242/dev.021071

    CAS  PubMed  Google Scholar 

  • Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459(7250):1136–1140. doi:10.1038/nature08066

    CAS  PubMed  Google Scholar 

  • Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17(23):6903–6911. doi:10.1093/emboj/17.23.6903

    CAS  PubMed Central  PubMed  Google Scholar 

  • Napier RM (2005) TIRs of joy: new receptors for auxin. Bioessays 27(12):1213–1217. doi:10.1002/bies.20329

    CAS  PubMed  Google Scholar 

  • Newell AC, Shipman PD, Sun Z (2008) Phyllotaxis: cooperation and competition between mechanical and biochemical processes. J Theor Biol 251(3):421–439. doi:10.1016/j.jtbi.2007.11.036

    CAS  PubMed  Google Scholar 

  • Niklas KJ, Kutschera U (2009) The evolutionary development of plant body plans. Funct Plant Biol 36(8):682–695. doi:10.1071/fp09107

    Google Scholar 

  • Nishiyama T, Fujita T, Shin IT, Seki M, Nishide H, Uchiyama I, Kamiya A, Carninci P, Hayashizaki Y, Shinozaki K, Kohara Y, Hasebe M (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci U S A 100(13):8007–8012. doi:10.1073/pnas.0932694100

    CAS  PubMed Central  PubMed  Google Scholar 

  • Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2(1):a001594. doi:10.1101/cshperspect.a001594

    PubMed Central  PubMed  Google Scholar 

  • Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72(3):523–536. doi:10.1111/j.1365-313X.2012.05085.x

    PubMed  Google Scholar 

  • Novoselova ES, Mironova VV, Omelyanchuk NA, Kazantsev FV, Likhoshvai VA (2013) Mathematical modeling of auxin transport in protoxylem and protophloem of Arabidopsis thaliana root tips. J Bioinform Comput Biol 11(1):6. doi:10.1142/S0219720013400106

    Google Scholar 

  • Orbovik V, Poff KL (1993) Growth distribution during Phototropism of Arabidopsis thaliana seedlings. Plant Physiology 103(1):157–163. doi:10.1104/pp. 103.1.157

    Google Scholar 

  • Östin A, Kowalyczk M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118(1):285–296. doi:10.1104/pp. 118.1.285

    PubMed Central  PubMed  Google Scholar 

  • Overbeek JV (1940) Auxin in marine algae. Plant Physiol 15(2):291–299. doi:10.1104/pp. 15.2.291

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324(5935):1684–1689, doi:1167324 [pii] 10.1126/science.1167324

    CAS  PubMed  Google Scholar 

  • Panigrahi KC, Panigrahy M, Vervliet-Scheebaum M, Lang D, Reski R, Johri MM (2009) Auxin-binding proteins without KDEL sequence in the moss Funaria hygrometrica. Plant Cell Rep 28(11):1747–1758. doi:10.1007/s00299-009-0775-2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paponov IA, Teale WD, Trebar M, Blilou K, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10(4):170–177. doi:10.1016/j.tplants.2005.02.009

    CAS  PubMed  Google Scholar 

  • Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol Biol 9:126, doi:1471-2148-9-126 [pii] 10.1186/1471-2148-9-126

    PubMed Central  PubMed  Google Scholar 

  • Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282(13):10036–10046. doi:10.1074/jbc.M610524200

    CAS  PubMed  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42(3):207–220. doi:10.1139/m96-032

    CAS  PubMed  Google Scholar 

  • Pattison RJ, Catala C (2012) Evaluating auxin distribution in tomato (Solanum lycopersicum) through an analysis of the PIN and AUX/LAX gene families. Plant J 70(4):585–598. doi:10.1111/j.1365-313X.2011.04895.x

    CAS  PubMed  Google Scholar 

  • Péret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol 144(4):1852–1862. doi:10.1104/pp. 107.101337

    PubMed Central  PubMed  Google Scholar 

  • 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 14:399–408. doi:10.1016/j.tplants.2009.05.002

    PubMed  Google Scholar 

  • Péret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, Yang H, Reemmer J, Venison E, Howells C, Perez-Amador MA, Yun J, Alonso J, Beemster GT, Laplaze L, Murphy A, Bennett MJ, Nielsen E, Swarup R (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24(7):2874–2885. doi:10.1105/tpc.112.097766

    PubMed Central  PubMed  Google Scholar 

  • Peris CIL, Rademacher EH, Weijers D (2010) Green beginnings – pattern formation in the early plant embryo. In: Timmermans MCP (ed) Plant development, vol 91, Current topics in developmental biology. Elsevier Academic, San Diego, pp 1–27. doi:10.1016/s0070-2153(10)91001-6

    Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136(16):2675–2688. doi:10.1242/dev.030353

    PubMed  Google Scholar 

  • Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918. doi:10.1126/science.1123542

    CAS  PubMed  Google Scholar 

  • Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci U S A 110(3):1107–1112. doi:10.1073/pnas.1213497110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Lond B Biol Sci 367(1588):508–518. doi:10.1098/rstb.2011.0252

    CAS  PubMed Central  PubMed  Google Scholar 

  • Poli DB, Jacobs M, Cooke TJ (2003) Auxin regulation of axial growth in bryophyte sporophytes: its potential significance for the evolution of early land plants. Am J Bot 90(10):1405–1415. doi:10.3732/ajb.90.10.1405

    CAS  PubMed  Google Scholar 

  • Porter WL, Thimann KV (1965) Molecular requirements for auxin action-I. Halogenated indoles and indoleacetic acid. Phytochemistry 4(2):229–243. doi:10.1016/S0031-9422(00)86169-5

    CAS  Google Scholar 

  • Prigge MJ, Lavy M, Ashton NW, Estelle M (2010) Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr Biol 20(21):1907–1912. doi:10.1016/j.cub.2010.08.050

    CAS  PubMed  Google Scholar 

  • Reinhardt D (2005) Regulation of phyllotaxis. Int J Dev Biol 49(5–6):539–546, doi:041922dr [pii] 10.1387/ijdb.041922dr

    CAS  PubMed  Google Scholar 

  • Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260. doi:10.1038/nature02081

    CAS  PubMed  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69, doi:1150646 [pii] 10.1126/science.1150646

    CAS  PubMed  Google Scholar 

  • Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zazimalova E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143(1):111–121. doi:10.1016/j.cell.2010.09.027

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ross J, Reid J (2010) Evolution of growth-promoting plant hormones. Funct Plant Biol 37:10. doi:10.1071/FP10063

    Google Scholar 

  • Ruiz Rosquete M, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5(4):772–786. doi:10.1093/mp/ssr109

    CAS  Google Scholar 

  • Ruiz-Trillo I, Burger G, Holland PWH, King N, Lang BF, Roger AJ, Gray MW (2007) The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 23(3):113–118. doi:10.1016/j.tig.2007.01.005

    CAS  PubMed  Google Scholar 

  • Sakakibara K (2003) Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130(20):4835–4846. doi:10.1242/dev.00644

    CAS  PubMed  Google Scholar 

  • Sanderson M, Thorne J, Wikstrom N, Bremer K (2004) Molecular evidence on plant divergence times. Am J Bot 91(10):1656–1665. doi:10.3732/ajb.91.10.1656

    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(20):2902–2911. doi:10.1101/gad.390806

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sawchuk MG, Edgar A, Scarpella E (2013) Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet 9(2):e1003294. doi:10.1371/journal.pgen.1003294

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scarpella E, Helariutta Y (2010) Chapter Eight – Vascular pattern formation in plants. In: Marja CPT (ed) Current topics in developmental biology, vol 91. Academic Press, USA, pp 221–265. doi:10.1016/S0070-2153(10)91008-9

  • Shipman PD, Newell AC (2005) Polygonal planforms and phyllotaxis on plants. J Theor Biol 236(2):154–197. doi:10.1016/j.jtbi.2005.03.007

    CAS  PubMed  Google Scholar 

  • Simon S, Petrášek J (2011) Why plants need more than one type of auxin. Plant Sci 180(3):454–460. doi:10.1016/j.plantsci.2010.12.007

    CAS  PubMed  Google Scholar 

  • Simon A, Glockner G, Felder M, Melkonian M, Becker B (2006) EST analysis of the scaly green flagellate Mesostigma viride (Streptophyta): implications for the evolution of green plants (Viridiplantae). BMC Plant Biol 6(1):2. doi:10.1186/1471-2229-6-2

    PubMed Central  PubMed  Google Scholar 

  • Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103:1301–1306. doi:10.1073/pnas.0510457103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31(4):425–448. doi:10.1111/j.1574-6976.2007.00072.x

    CAS  PubMed  Google Scholar 

  • Stark P (1921) Studien iiber traumatotrope und haptotrope Reizleitungsvorgange mit besonderer Berücksichtigung der Reizübertragung auf fremde Arten und Gattungen. Jahr biicher fiir wissenschaftliche Botanik 60:67

    Google Scholar 

  • Stepanova AN (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191. doi:10.1016/j.cell.2008.01.047

    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. doi:10.1105/tpc.105.033365

    CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  • Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci 106(13):5430–5435. doi:10.1073/pnas.0811226106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sun H, Basu S, Brady SR, Luciano RL, Muday GK (2004) Interactions between auxin transport and the actin cytoskeleton in developmental polarity of Fucus distichus embryos in response to light and gravity. Plant Physiol 135(1):266–278. doi:10.1104/pp. 103.034900

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653. doi:10.1101/gad.210501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954. doi:10.1038/ncb1754

    CAS  PubMed  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319(5868):1384–1386. doi:10.1126/science.1151461

    CAS  PubMed  Google Scholar 

  • Sztein AE, Cohen JD, Cooke TJ (2000) Evolutionary patterns in the auxin metabolism of green plants. Int J Plant Sci 161(6):849–859. doi:10.1086/317566

    CAS  Google Scholar 

  • Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446(7136):640–645. doi:10.1038/nature05731

    CAS  PubMed  Google Scholar 

  • Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176. doi:10.1016/j.cell.2008.01.049

    CAS  PubMed Central  PubMed  Google Scholar 

  • Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, Yazaki K (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17(11):2922–2939. doi:10.1105/tpc.105.035816

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thimann KV (1969) The auxins. In: Wilkins MB (ed) The physiology of plant growth and development. McGraw-Hill, New York, p 345

    Google Scholar 

  • Thimann KV, Skoog F (1933) Studies on the growth hormone of plants: III. The inhibiting action of the growth substance on bud development. Proc Natl Acad Sci 19(7):714–716

    CAS  PubMed Central  PubMed  Google Scholar 

  • Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS (2009) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57(1):27–44. doi:10.1111/j.1365-313X.2008.03668.x

    CAS  PubMed  Google Scholar 

  • Tivendale ND, Davies NW, Molesworth PP, Davidson SE, Smith JA, Lowe EK, Reid JB, Ross JJ (2010) Reassessing the role of N-hydroxytryptamine in auxin biosynthesis. Plant Physiol 154(4):1957–1965. doi:10.1104/pp. 110.165803

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tromas A, Paponov I, Perrot-Rechenmann C (2010) AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends Plant Sci 15(8):436–446. doi:10.1016/j.tplants.2010.05.001

    CAS  PubMed  Google Scholar 

  • Tsavkelova E, Cherdyntseva T, Klimova S, Shestakov A, Botina S, Netrusov A (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188(6):655–664. doi:10.1007/s00203-007-0286-x

    CAS  PubMed  Google Scholar 

  • Turmel M (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23(6):1324–1338. doi:10.1093/molbev/msk018

    CAS  PubMed  Google Scholar 

  • Ugartechea-Chirino Y, Swarup R, Swarup K, Peret B, Whitworth M, Bennett M, Bougourd S (2009) The AUX1 LAX family of auxin influx carriers is required for the establishment of embryonic root cell organization in Arabidopsis thaliana. Ann Bot 105(2):277–289. doi:10.1093/aob/mcp287

    PubMed Central  PubMed  Google Scholar 

  • Utsuno K, Shikanai T, Yamada Y, Hashimoto T (1998) AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol 39(10):1111–1118

    CAS  PubMed  Google Scholar 

  • Van den Hoek C, Mann D, Jahns HM (1996) Algae: an introduction to phycology. Cambridge University Press, Cambridge

    Google Scholar 

  • Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu Ü, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EP, Yazaki K, Theodoulou FL (2008) Plant ABC proteins – a unified nomenclature and updated inventory. Trends Plant Sci 13(4):151–159. doi:10.1016/j.tplants.2008.02.001

    CAS  PubMed  Google Scholar 

  • Viaene T, Delwiche CF, Rensing SA, Friml J (2013) Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci 18(1):5–10, doi:S1360-1385(12)00194-X [pii]10.1016/j.tplants.2012.08.009

    CAS  PubMed  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12(4):160–168. doi:10.1016/j.tplants.2007.03.006

    CAS  PubMed  Google Scholar 

  • Wabnik K, Kleine-Vehn J, Govaerts W, Friml J (2011) Prototype cell-to-cell auxin transport mechanism by intracellular auxin compartmentalization. Trends Plant Sci 16(9):468–475. doi:10.1016/j.tplants.2011.05.002S1360-1385(11)00100-2

    CAS  PubMed  Google Scholar 

  • Went FW (1927) Wuchsstoff und wachstum. J.H. de Bussy, Amsterdam

    Google Scholar 

  • Went F, Thimann K (1937) Phytohormones. Macmillan, New York, NY

    Google Scholar 

  • Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11(1):104. doi:10.1186/1471-2148-11-104

    PubMed Central  PubMed  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95(5):707–735. doi:10.1093/aob/mci083

    CAS  PubMed  Google Scholar 

  • Yang H, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59(1):179–191. doi:10.1111/j.1365-313X.2009.03856.x

    CAS  PubMed  Google Scholar 

  • Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16(11):1123–1127. doi:10.1016/j.cub.2006.04.029

    CAS  PubMed  Google Scholar 

  • Yokoya NS, West JA, Luchi AE (2004) Effects of plant growth regulators on callus formation, growth and regeneration in axenic tissue cultures of Gracilaria tenuistipitata and Gracilaria perplexa (Gracilariales, Rhodophyta). Phycol Res 52(3):244–254. doi:10.1111/j.1440-183.2004.00349.x

    CAS  Google Scholar 

  • Yokoya NS, Stirk WA, van Staden J, Novák O, Turečková V, Pěnčík A, Strnad M (2010) Endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. J Phycol 46(6):1198–1205. doi:10.1111/j.1529-8817.2010.00898.x

    CAS  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21(5):809–818. doi:10.1093/molbev/msh075

    CAS  PubMed  Google Scholar 

  • Zažímalová E, Křeček P, Skůpa P, Hoyerová K, Petrášek J (2007) Polar transport of the plant hormone auxin – the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64(13):1621–1637. doi:10.1007/s00018-007-6566-4

    PubMed  Google Scholar 

  • Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2(3):a001552. doi:10.1101/cshperspect.a001552

    PubMed Central  PubMed  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. doi:10.1146/annurev-arplant-042809-112308

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5(2):334–338. doi:10.1093/mp/ssr104

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmerman PW, Wilcoxon F (1935) Several chemical growth substances which cause initiation of root and other responses in plants. Contrib Boyce Thompson Inst 7:209–229

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK

    Priya Ramakrishna & Ive De Smet

  2. Centre for Plant Integrative Biology, University of Nottingham, Nottingham, LE12 5RD, UK

    Ive De Smet

Authors
  1. Priya Ramakrishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ive De Smet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ive De Smet .

Editor information

Editors and Affiliations

  1. Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany AS CR, Prague 6, Czech Republic

    Eva Zažímalová

  2. Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany AS CR, Prague 6, Czech Republic

    Jan Petrášek

  3. Hormonal Cross-talk Group, Institute of Science and Technology (IST), Austria, Klosterneuburg, Austria

    Eva Benková

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Ramakrishna, P., De Smet, I. (2014). Evolutionary Aspects of Auxin Signalling. In: Zažímalová, E., Petrášek, J., Benková, E. (eds) Auxin and Its Role in Plant Development. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1526-8_13

Download citation

Publish with us

Policies and ethics

Search

Navigation