Abstract
Plants have a unique capacity for continuous postembryonic development linked to the existence of permanent stem cell niches, located in specialized tissues called meristems. The activity of the shoot apical meristem (SAM), which is located at the tip of stems and branches, allows for the continuous production of all aerial organs that will develop as lateral shoots, leaves, or flowers. As it defines the number, type, and position of lateral primordia, the SAM is at the basis of plant architecture and its activity can be modulated by both internal and environmental cues. Successive initiations of new organ primordia occur in the meristem following very precise spatiotemporal patterns, called phyllotaxis. The maintenance of the meristem over time is thus expected to require precise spatiotemporal control of cell fate to allow for the continuous emergence of new primordia at precise positions and the maintenance of the stem cell niche. Signaling initiated by the plant hormone auxin plays a central role in the control of cell identities during organogenesis and in the dynamics of phyllotaxis. We first describe the structure and function of the SAM, focusing on the model species Arabidopsis thaliana. We then discuss the central role played by auxin in the coordination of cellular behaviors and cell identities in the SAM, and thus in providing the primary instructions for phyllotaxis and for elaborating the shoot architecture. Finally, we illustrate how the gene network downstream of auxin and mechanical properties of tissues participate in controlling morphogenesis and phyllotaxis dynamics.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63(63):615–636
Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9(6):841–857. doi:10.1105/tpc.9.6.841
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
Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341(1):95–113. doi:10.1016/j.ydbio.2009.11.029
Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23(3):373–384. doi:10.1101/gad.497009, 23/3/373 [pii]
Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128(20):4057–4067
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
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(5277):948–950
Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19(6):1795–1808. doi:10.1105/tpc.106.047159
Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5(3):110–115
Bowman JL, Floyd SK (2008) Patterning and polarity in seed plant shoots. Annu Rev Plant Biol 59:67–88. doi:10.1146/annurev.arplant.57.032905.105356
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289(5479):617–619
Brand U, Grunewald M, Hobe M, Simon R (2002) Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiol 129(2):565–575. doi:10.1104/pp. 001867
Brandt R, Salla-Martret M, Bou-Torrent J, Musielak T, Stahl M, Lanz C, Ott F, Schmid M, Greb T, Schwarz M, Choi SB, Barton MK, Reinhart BJ, Liu T, Quint M, Palauqui JC, Martinez-Garcia JF, Wenkel S (2012) Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J 72(1):31–42. doi:10.1111/j.1365-313X.2012.05049.x
Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482(7383):103–106. doi:10.1038/nature10791
Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408(6815):967–971. doi:10.1038/35050091
Chandler JW (2012) Floral meristem initiation and emergence in plants. Cell Mol Life Sci 69(22):3807–3818. doi:10.1007/s00018-012-0999-0
Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285. doi:10.1146/annurev-genet-102108-134148
Chehab EW, Eich E, Braam J (2009) Thigmomorphogenesis: a complex plant response to mechano-stimulation. J Exp Bot 60(1):43–56. doi:10.1093/jxb/ern315
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
Cheng YF, Dai XH, Zhao YD (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20(13):1790–1799. doi:10.1101/Gad.1415106
Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19(8):2430–2439. doi:10.1105/tpc.107.053009
Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100(4):469–478
Cosgrove D (1986) Biophysical control of plant cell growth. Annu Rev Plant Physiol 37:377–405. doi:10.1146/annurev.pp. 37.060186.002113
D’Arcy Thompson W (1917) On growth and form. Cambridge University Press, Cambridge
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, 0510130103 [pii]
Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R, Laux T, Palme K (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105(48):18818–18823. doi:10.1073/pnas.0807814105
Douady S, Couder Y (1992) Phyllotaxis as a physical self-organized growth-process. Phys Rev Lett 68(13):2098–2101. doi:10.1103/PhysRevLett.68.2098
Douady S, Couder Y (1996a) Phyllotaxis as a dynamical self organizing process.1. The spiral modes resulting from time-periodic iterations. J Theor Biol 178(3):255–274. doi:10.1006/jtbi.1996.0024
Douady S, Couder Y (1996b) Phyllotaxis as a dynamical self organizing process. 2. The spontaneous formation of a periodicity and the coexistence of spiral and whorled patterns. J Theor Biol 178(3):275–294. doi:10.1006/jtbi.1996.0025
Douady S, Couder Y (1996c) Phyllotaxis as a dynamical self organizing process. 3. The simulation of the transient regimes of ontogeny. J Theor Biol 178(3):295–312. doi:10.1006/jtbi.1996.0026
Dumais J, Steele CR (2000) New evidence for the role of mechanical forces in the shoot apical meristem. J Plant Growth Regul 19(1):7–18
Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10(6):967–979
Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689. doi:10.1016/j.cell.2006.06.044
Farge E (2003) Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr Biol 13(16):1365–1377
Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283(5409):1911–1914
Friml J (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biol 89(2–3):231–235. doi:10.1016/j.ejcb.2009.11.003
Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306(5697):862–865. doi:10.1126/science.1100618
Gallois JL, Woodward C, Reddy GV, Sablowski R (2002) Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129(13):3207–3217
Galweiler L, Guan C, Muller 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
Green PB (1999) Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. Am J Bot 86(8):1059–1076
Guenot B, Bayer E, Kierzkowski D, Smith RS, Mandel T, Zadnikova P, Benkova E, Kuhlemeier C (2012) Pin1-independent leaf initiation in Arabidopsis. Plant Physiol 159(4):1501–1510. doi:10.1104/pp. 112.200402
Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322(5908):1650–1655. doi:10.1126/science.1165594, 322/5908/1650 [pii]
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, S0960-9822(05)01213-3 [pii]
Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jonsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8(10):e1000516. doi:10.1371/journal.pbio.1000516
Hernandez LF, Green PB (1993) Transductions for the expression of structural pattern: analysis in sunflower. Plant Cell 5(12):1725–1738. doi:10.1105/tpc.5.12.1725
Hofmeister W (1868) Allgemeine Morphologie des Gewächse. Handbuch des physiologischeb Botanik, vol 1. Engelmann, Leipzig
Husbands A, Bell EM, Shuai B, Smith HM, Springer PS (2007) LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins. Nucleic Acids Res 35(19):6663–6671. doi:10.1093/nar/gkm775
Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103(5):1633–1638. doi:10.1073/pnas.0509839103, 0509839103 [pii]
Kierzkowski D, Nakayama N, Routier-Kierzkowska AL, Weber A, Bayer E, Schorderet M, Reinhardt D, Kuhlemeier C, Smith RS (2012) Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335(6072):1096–1099. doi:10.1126/science.1213100
Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313(5788):845–848. doi:10.1126/science.1128439
Krizek B (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150(4):1916–1929. doi:10.1104/pp.109.141119
Kutschera U, Niklas KJ (2007) The epidermal-growth-control theory of stem elongation: an old and a new perspective. J Plant Physiol 164(11):1395–1409. doi:10.1016/j.jplph.2007.08.002
Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129(13):3195–3206
Li W, Zhou Y, Liu X, Yu P, Cohen JD, Meyerowitz EM (2013) LEAFY Controls Auxin Response Pathways in Floral Primordium Formation. Sci Signal 6(270):ra23. doi:10.1126/scisignal.2003937
Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28(4):465–474
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379(6560):66–69. doi:10.1038/379066a0
Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao YD, Hayashi K, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108(45):18512–18517. doi:10.1073/pnas.1108434108
Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95(6):805–815
Mitchison GJ (1980) A model for vein formation in higher plants. Proc R Soc Lond Biol Sci 207:79–109
Mitchison GJ (1981) The polar transport of auxin and vein patterns in plants. Philos Trans R Soc B 295
Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97(2):942–947
Moyroud E, Minguet EG, Ott F, Yant L, Pose D, Monniaux M, Blanchet S, Bastien O, Thevenon E, Weigel D, Schmid M, Parcy F (2011) Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor. Plant Cell 23(4):1293–1306. doi:10.1105/tpc.111.083329
Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10(4):e1001299. doi:10.1371/journal.pbio.1001299
Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S, Boudaoud A, Kuhlemeier C (2012) Mechanical regulation of auxin-mediated growth. Curr Biol 22(16):1468–1476. doi:10.1016/j.cub.2012.06.050
Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM (2011) Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr Biol 21(5):345–352. doi:10.1016/j.cub.2011.01.039
Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319(5861):294. doi:10.1126/science.1150083
Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3(7):677–684. doi:10.1105/tpc.3.7.677
Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435(7046):1251–1256. doi:10.1038/nature03633
Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395(6702):561–566. doi:10.1038/26903
Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Hofte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21(20):1720–1726. doi:10.1016/j.cub.2011.08.057
Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16(7):1898–1911. doi:10.1105/tpc.021501
Peret 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
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, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312(5775):914–918. doi:10.1126/science.1123542
Phelps-Durr TL, Thomas J, Vahab P, Timmermans MC (2005) Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17(11):2886–2898. doi:10.1105/tpc.105.035477
Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Fleming A (2001) Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc Natl Acad Sci USA 98(20):11812–11817. doi:10.1073/pnas.191380498
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 USA 110(3):1107–1112. doi:10.1073/pnas.1213497110
Prasad K, Grigg SP, Barkoulas M, Yadav RK, Sanchez-Perez GF, Pinon V, Blilou I, Hofhuis H, Dhonukshe P, Galinha C, Mahonen AP, Muller WH, Raman S, Verkleij AJ, Snel B, Reddy GV, Tsiantis M, Scheres B (2011) Arabidopsis PLETHORA transcription factors control phyllotaxis. Curr Biol 21(13):1123–1128. doi:10.1016/j.cub.2011.05.009
Proseus TE, Ortega JK, Boyer JS (1999) Separating growth from elastic deformation during cell enlargement. Plant Physiol 119(2):775–784
Rast MI, Simon R (2012) Arabidopsis JAGGED LATERAL ORGANS acts with ASYMMETRIC LEAVES2 to coordinate KNOX and PIN expression in shoot and root meristems. Plant Cell 24(7):2917–2933. doi:10.1105/tpc.112.099978
Raven JA (1975) Transport of indoleacetic-acid in plant-cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol 74(2):163–172. doi:10.1111/j.1469-8137.1975.tb02602.x
Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12(4):507–518
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(6964):255–260. doi:10.1038/nature02081, nature02081 [pii]
Richards FJ (1948) The geometry of phyllotaxis and its origin. Symp Soc Exp Biol 2:217–245
Richter GL, Monshausen GB, Krol A, Gilroy S (2009) Mechanical stimuli modulate lateral root organogenesis. Plant Physiol 151(4):1855–1866. doi:10.1104/pp. 109.142448
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
Rolland-Lagan AG, Prusinkiewicz P (2005) Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J 44(5):854–865. doi:10.1111/j.1365-313X.2005.02581.x
Sachs T (1969) Polarity and induction of organized vascular tissues. Ann Bot Lond 33(130):263
Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446(7132):199–202. doi:10.1038/Nature05618
Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20(8):1015–1027. doi:10.1101/gad.1402406
Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100(6):635–644
Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93(10):1415–1425. doi:10.3732/ajb.93.10.1415
Schoute JC (1913) Beitrage zur Blattstellunglehre. I. Die Theorie. Recueil de Travaux Botaniques Neerlandais 10:153–339
Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129(2):747–761. doi:10.1104/pp. 010926
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(5):1301–1306. doi:10.1073/pnas.0510457103, 0510457103 [pii]
Snow M, Snow R (1932) Experiments on phyllotaxis I—the effect of isolating a pininordium. Philos Trans R Soc Lond B 221:1–43. doi:10.1098/rstb.1932.0001
Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4(10):e1000207. doi:10.1371/journal.pcbi.1000207
Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128(7):1127–1135
Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykret D, Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A, Kwiatkowska D, Hamant O (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149(2):439–451. doi:10.1016/j.cell.2012.02.048
van Berkel K, de Boer RJ, Scheres B, Ten Tusscher K (2013) Polar auxin transport: models and mechanisms. Development 140(11):2253–2268. doi:10.1242/dev.079111
Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127(23):5157–5165
Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, Guedon Y, Armitage L, Picard F, Guyomarc'h S, Cellier C, Parry G, Koumproglou R, Doonan JH, Estelle M, Godin C, Kepinski S, Bennett M, De Veylder L, Traas J (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7:508. doi:10.1038/msb.2011.39
Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132(20):4521–4531. doi:10.1242/dev.02027
Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15(7):1563–1577
Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinohl V, Merks RMH, Govaerts W, Friml J (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:447. doi:10.1038/Msb.2010.103
Wardlaw CW (1949) Phyllotaxis and organogenesis in ferns. Nature 164(4161):167–169. doi:10.1038/164167a0
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843–859
Winter CM, Austin RS, Blanvillain-Baufume S, Reback MA, Monniaux M, Wu MF, Sang Y, Yamaguchi A, Yamaguchi N, Parker JE, Parcy F, Jensen ST, Li H, Wagner D (2011) LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell 20(4):430–443. doi:10.1016/j.devcel.2011.03.019
Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312(5775):883. doi:10.1126/science.1121356
Won C, Shen XL, Mashiguchi K, Zheng ZY, Dai XH, Cheng YF, Kasahara H, Kamiya Y, Chory J, Zhao YD (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci USA 108(45):18518–18523. doi:10.1073/pnas.1108436108
Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143(1):99–110. doi:10.1016/j.cell.2010.09.003
Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25(19):2025–2030. doi:10.1101/gad.17258511
Yamaguchi N, Wu MF, Winter CM, Berns MC, Nole-Wilson S, Yamaguchi A, Coupland G, Krizek BA, Wagner D (2013) A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 24(3):271–282. doi:10.1016/j.devcel.2012.12.017
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
Acknowledgments
We thank Olivier Hamant for critical reading of the manuscript and Geraldine Brunoud for providing pictures. The work in the authors’ laboratory is supported by ANR and HFSP grants.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag Wien
About this chapter
Cite this chapter
Landrein, B., Vernoux, T. (2014). Auxin, Chief Architect of the Shoot Apex. 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_10
Download citation
DOI: https://doi.org/10.1007/978-3-7091-1526-8_10
Published:
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-1525-1
Online ISBN: 978-3-7091-1526-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)