Abstract
The plant hormone auxin mediates developmental patterning by a mechanism that is based on active transport. In the shoot apical meristem, auxin gradients are thought to be set up through a feedback loop between auxin and the activity and polar localization of its transporter, the PIN1 protein. Two distinct molecular mechanisms for the subcellular polarization of PIN1 have been proposed. For leaf positioning (phyllotaxis), an "up-the-gradient" PIN1 polarization mechanism has been proposed, whereas the formation of vascular strands is thought to proceed by "with-the-flux" PIN1 polarization. These patterning mechanisms intersect during the initiation of the midvein, which raises the question of how two different PIN1 polarization mechanisms may work together. Our detailed analysis of PIN1 polarization during midvein initiation suggests that both mechanisms for PIN1 polarization operate simultaneously. Computer simulations of the resulting dual polarization model are able to reproduce the dynamics of observed PIN1 localization. In addition, the appearance of high auxin concentration in our simulations throughout the initiation of the midvein is consistent with experimental observation and offers an explanation for a long-standing criticism of the canalization hypothesis; namely, how both high flux and high concentration can occur simultaneously in emerging veins.
MeSH Terms
Base Sequence
Biological Transport, Active
Body Patterning/drug effects
Computer Simulation
DNA Primers/genetics
DNA, Plant/genetics
Feedback, Physiological
Gene Expression Regulation, Developmental
Gene Expression Regulation, Plant
Genes, Plant
Indoleacetic Acids/metabolism,pharmacology
Lycopersicon esculentum/drug effects,genetics,growth & development,physiology
Meristem/growth & development,physiology
Models, Biological
Plant Growth Regulators/pharmacology,physiology
Plant Leaves/growth & development,physiology
Plant Proteins/genetics,physiology
Plants, Genetically Modified
Chemicals
DNA Primers
DNA, Plant
Indoleacetic Acids
Plant Growth Regulators
Plant Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Bayer Emmanuelle M
Institute of Plant Sciences, University of Bern, Bern, Switzerland.
Smith Richard S
Mandel Therese
Nakayama Naomi
Sauer Michael
Prusinkiewicz Przemyslaw
Kuhlemeier Cris
References (28)
28 references, click to expand
-
Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem.
Development. 2003 Sep;130(17):4073-83
PMID: 12874128
-
A plausible model of phyllotaxis.
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1301-6
PMID: 16432192
-
Auxin signaling in Arabidopsis leaf vascular development.
Plant Physiol. 2003 Mar;131(3):1327-39
PMID: 12644682
-
An auxin-driven polarized transport model for phyllotaxis.
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1633-8
PMID: 16415160
-
Canalization without flux sensors: a traveling-wave hypothesis.
Trends Plant Sci. 2007 Sep;12(9):384-90
PMID: 17765595
-
The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana.
Development. 1995 Dec;121(12):4171-82
PMID: 8575317
-
Local, efflux-dependent auxin gradients as a common module for plant organ formation.
Cell. 2003 Nov 26;115(5):591-602
PMID: 14651850
-
Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis.
Plant J. 2005 Dec;44(5):854-65
PMID: 16297075
-
Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem.
Plant Cell. 1998 Sep;10(9):1427-37
PMID: 9724690
-
Auxin as a positional signal in pattern formation in plants.
Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9282-6
PMID: 11607701
-
Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis.
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1627-32
PMID: 16432202
-
Control of leaf vascular patterning by polar auxin transport.
Genes Dev. 2006 Apr 15;20(8):1015-27
PMID: 16618807
-
Computer models of auxin transport: a review and commentary.
J Exp Bot. 2008;59(1):45-53
PMID: 17431022
-
Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development.
PLoS Comput Biol. 2008 Oct;4(10):e1000207
PMID: 18974825
-
Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation.
Development. 2004 Jul;131(14):3445-55
PMID: 15226260
-
Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events.
Development. 1998 Apr;125(8):1477-85
PMID: 9502728
-
Auxin influx carriers stabilize phyllotactic patterning.
Genes Dev. 2008 Mar 15;22(6):810-23
PMID: 18347099
-
Responses of plant vascular systems to auxin transport inhibition.
Development. 1999 Jul;126(13):2979-91
PMID: 10357941
-
PIN and AUX/LAX proteins: their role in auxin accumulation.
Trends Plant Sci. 2004 Dec;9(12):578-82
PMID: 15564124
-
Pattern Formation in the Arabidopsis Embryo Revealed by Position-Specific Lipid Transfer Protein Gene Expression.
Plant Cell. 1996 May;8(5):783-791
PMID: 12239400
-
Auxin regulates the initiation and radial position of plant lateral organs.
Plant Cell. 2000 Apr;12(4):507-18
PMID: 10760240
-
A system for modelling cell-cell interactions during plant morphogenesis.
Ann Bot. 2008 May;101(8):1255-65
PMID: 17921524
-
Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression.
Development. 2005 Oct;132(20):4521-31
PMID: 16192309
-
Regulation of phyllotaxis by polar auxin transport.
Nature. 2003 Nov 20;426(6964):255-60
PMID: 14628043
-
The role of local biosynthesis of auxin and cytokinin in plant development.
Curr Opin Plant Biol. 2008 Feb;11(1):16-22
PMID: 18409210
-
Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.
Curr Biol. 2005 Nov 8;15(21):1899-911
PMID: 16271866
-
Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny.
Plant Physiol. 2002 Sep;130(1):199-209
PMID: 12226500
-
The epidermis both drives and restricts plant shoot growth.
Nature. 2007 Mar 8;446(7132):199-202
PMID: 17344852