Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte

Dmytro S. Lituiev; Nádia G. Krohn; Bruno Müller; Barbara Hellriegel; Thomas Dresselhaus; Ueli Grossniklaus

doi:10.1242/dev.098301

journal article Nov 15, 2013

Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte

Dmytro S. Lituiev Nádia G. Krohn Bruno Müller Barbara Hellriegel Thomas Dresselhaus

Ueli Grossniklaus

Development Vol. 140 No. 22 pp. 4544-4553 · The Company of Biologists

View at Publisher Save 10.1242/dev.098301

Abstract

The plant life cycle alternates between a diploid sporophytic and a haploid gametophytic generation. The female gametophyte (FG) of flowering plants is typically formed through three syncytial mitoses, followed by cellularisation that forms seven cells belonging to four cell types. The specification of cell fates in the FG has been suggested to depend on positional information provided by an intrinsic auxin concentration gradient. The goal of this study was to develop mathematical models that explain the formation of this gradient in a syncytium. Two factors were proposed to contribute to the maintenance of the auxin gradient in Arabidopsis FGs: polar influx at early stages and localised auxin synthesis at later stages. However, no gradient could be generated using classical, one-dimensional theoretical models under these assumptions. Thus, we tested other hypotheses, including spatial confinement by the large central vacuole, background efflux and localised degradation, and investigated the robustness of cell specification under different parameters and assumptions. None of the models led to the generation of an auxin gradient that was steep enough to allow sufficiently robust patterning. This led us to re-examine the response to an auxin gradient in developing FGs using various auxin reporters, including a novel degron-based reporter system. In agreement with the predictions of our models, auxin responses were not detectable within the FG of Arabidopsis or maize, suggesting that the effects of manipulating auxin production and response on cell fate determination might be indirect.

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References

55

[1]

Alon (2007)

[2]

Bent "Arabidopsis thaliana floral dip transformation method" Methods Mol. Biol. (2006)

[3]

Chavarría-Krauser "Homogenization of long-range auxin transport in plant tissues" Nonlinear Anal. Real World Appl. (2010) 10.1016/j.nonrwa.2008.12.003

[4]

Christensen "Megagametogenesis in Arabidopsis wild type and the Gf mutant" Sex. Plant Reprod. (1997) 10.1007/s004970050067

[5]

Ceccato "Maternal control of PIN1 is required for female gametophyte development in Arabidopsis" PLoS ONE (2013) 10.1371/journal.pone.0066148

[6]

Curtis "A gateway cloning vector set for high-throughput functional analysis of genes in planta" Plant Physiol. (2003) 10.1104/pp.103.027979

[7]

Dal Bosco "The endoplasmic reticulum localized PIN8 is a pollen specific auxin carrier involved in intracellular auxin homeostasis" Plant J. (2012) 10.1111/j.1365-313x.2012.05037.x

[8]

de Lachapelle "Precision and scaling in morphogen gradient read-out" Mol. Systems Biol. (2010) 10.1038/msb.2010.7

[9]

Delbarre "Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells" Planta (1996) 10.1007/bf00262639

[10]

Desfeux "Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method" Plant Physiol (2000) 10.1104/pp.123.3.895

[11]

The FERONIA Receptor-like Kinase Mediates Male-Female Interactions During Pollen Tube Reception

Juan-Miguel Escobar-Restrepo, Norbert Huck, Sharon Kessler et al.

Science 2007 10.1126/science.1143562

[12]

Evans "The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo Sac and leaf development" Plant Cell (2007) 10.1105/tpc.106.047506

[13]

Gallavotti "The relationship between auxin transport and maize branching" Plant Physiol. (2008) 10.1104/pp.108.121541

[14]

Gallie "The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F" Nucleic Acids Res. (2002) 10.1093/nar/gkf457

[15]

Garnett "Computer simulation: the imaginary friend of auxin transport biology" BioEssays (2010) 10.1002/bies.200900185

[16]

Geisler "Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1" Plant J. (2005) 10.1111/j.1365-313x.2005.02519.x

[17]

Gregor "Diffusion and scaling during early embryonic pattern formation" Proc. Natl. Acad. Sci. USA (2005) 10.1073/pnas.0509483102

[18]

Grieneisen "Auxin transport is sufficient to generate a maximum and gradient guiding root growth" Nature (2007) 10.1038/nature06215

[19]

Gross-Hardt "LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis" PLoS Biol. (2007) 10.1371/journal.pbio.0050047

[20]

Auxin response factors

Tom J. Guilfoyle, Gretchen Hagen

Current Opinion in Plant Biology 2007 10.1016/j.pbi.2007.08.014

[21]

Gutknecht "Transport of auxin (indoleacetic acid) through lipid bilayer membranes" J. Membr. Biol. (1980) 10.1007/bf01869353

[22]

He "Shaping a morphogen gradient for positional precision" Biophys. J. (2010) 10.1016/j.bpj.2010.04.073

[23]

Huang "Female gametophyte development in maize: microtubular organization and embryo sac polarity" Plant Cell (1994) 10.2307/3869963

[24]

Johnston "Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle" PLoS Genet. (2010) 10.1371/journal.pgen.1000988

[25]

Krohn "Egg cell signaling by the secreted peptide ZmEAL1 controls antipodal cell fate" Dev. Cell (2012) 10.1016/j.devcel.2012.05.018

[26]

Lander "The measure of success: constraints, objectives, and tradeoffs in morphogen-mediated patterning" Cold Spring Harb. Perspect. Biol. (2009) 10.1101/cshperspect.a002022

[27]

Liu "Modelling and experimental analysis of hormonal crosstalk in Arabidopsis" Mol. Syst. Biol. (2010) 10.1038/msb.2010.26

[28]

Ljung "Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings" Plant Physiol. (2001) 10.1104/pp.125.1.464

[29]

Marchant "AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues" EMBO J. (1999) 10.1093/emboj/18.8.2066

[30]

Moll "CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants" Plant J. (2008) 10.1111/j.1365-313x.2008.03650.x

[31]

Mori "Wave-pinning and cell polarity from a bistable reaction-diffusion system" Biophys. J. (2008) 10.1529/biophysj.107.120824

[32]

Ottenschläger "Gravity-regulated differential auxin transport from columella to lateral root cap cells" Proc. Natl. Acad. Sci. USA (2003) 10.1073/pnas.0437936100

[33]

Pagnussat "Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1" Plant Cell (2007) 10.1105/tpc.107.054890

[34]

Pagnussat "Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte" Science (2009) 10.1126/science.1167324

[35]

Petrásek "Auxin transport routes in plant development" Development (2009) 10.1242/dev.030353

[36]

Ramos "Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent" Plant Cell (2001) 10.1105/tpc.010244

[37]

Rapparini "Indole-3-acetic acid metabolism in Lemna gibba undergoes dynamic changes in response to growth temperature" Plant Physiol. (2002) 10.1104/pp.011005

[38]

Rotman "A novel class of MYB factors controls sperm-cell formation in plants" Curr. Biol. (2005) 10.1016/j.cub.2005.01.013

[39]

Sbalzarini "Effects of organelle shape on fluorescence recovery after photobleaching" Biophys. J. (2005) 10.1529/biophysj.104.057885

[40]

A Powerful Method for Transcriptional Profiling of Specific Cell Types in Eukaryotes: Laser-Assisted Microdissection and RNA Sequencing

Marc W. Schmid, Anja Schmidt, Ulrich C. Klostermeier et al.

PLoS ONE 2012 10.1371/journal.pone.0029685

[41]

Schneitz "Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue" Plant J. (1995) 10.1046/j.1365-313x.1995.07050731.x

[42]

Sequeira "Partial purification and kinetics of indoleacetic acid oxidase from tobacco roots" Plant Physiol. (1966) 10.1104/pp.41.7.1200

[43]

Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein

Nathan C Shaner, Robert E Campbell, Paul A Steinbach et al.

Nature Biotechnology 2004 10.1038/nbt1037

[44]

Srilunchang "DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize" Development (2010) 10.1242/dev.035964

[45]

Sundaresan "Pattern formation in miniature: the female gametophyte of flowering plants" Development (2010) 10.1242/dev.030346

[46]

Swarup "AUX/LAX family of auxin influx carriers - an overview" Front. Plant Sci. (2012) 10.3389/fpls.2012.00225

[47]

Swarup "The auxin influx carrier LAX3 promotes lateral root emergence" Nat. Cell Biol. (2008) 10.1038/ncb1754

[48]

Tucker "Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium" J. Exp. Bot. (2012) 10.1093/jxb/ers047

[49]

Ulmasov "Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements" Plant Cell (1997)

[50]

Vernoux "The auxin signalling network translates dynamic input into robust patterning at the shoot apex" Mol. Syst. Biol. (2011) 10.1038/msb.2011.39

Showing 50 of 55 references

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References

Details

Published: Nov 15, 2013
Vol/Issue: 140(22)
Pages: 4544-4553

Authors

D

Dmytro S. Lituiev

Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland.

N

Nádia G. Krohn

Cell Biology and Plant Biochemistry, Biochemie-Zentrum Regensburg, University of Regensburg, Universitätsstrasse 31, D-93053 Regensburg, Germany.

B

Bruno Müller

Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland.

B

Barbara Hellriegel

Anthropological Institute and Museum, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland.

T

Thomas Dresselhaus

Cell Biology and Plant Biochemistry, Biochemie-Zentrum Regensburg, University of Regensburg, Universitätsstrasse 31, D-93053 Regensburg, Germany.

U

Ueli Grossniklaus

Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland.

Cite This Article

Dmytro S. Lituiev, Nádia G. Krohn, Bruno Müller, et al. (2013). Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte. Development, 140(22), 4544-4553. https://doi.org/10.1242/dev.098301

Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte

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