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

Development (Cambridge)

Volumn 140, Issue 22, 2013, Pages 4544-4553

  Lituiev, Dmytro S ^a   Krohn, Nádia G ^b   Müller, Bruno ^a   Jackson, David ^c   Hellriegel, Barbara ^a   Dresselhaus, Thomas ^b   Grossniklaus, Ueli ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Arabidopsis; Auxin; Female gametophyte; Gradient; Maize; Modelling

Indexed keywords

AUXIN;

ARABIDOPSIS THALIANA; ARTICLE; CELL FATE; CELL VACUOLE; DEGRADATION; EXPERIMENTAL MODEL; FEMALE GAMETOPHYTE; MAIZE; MATHEMATICAL MODEL; MICROSCOPY; OVULE; PLANT CELL; PRIORITY JOURNAL; SIMULATION; SPOROPHYTE; SYNCYTIUM; SYNTHESIS; THEORETICAL MODEL;

ARABIDOPSIS; AUXIN; FEMALE GAMETOPHYTE; GRADIENT; MAIZE; MODELLING;

ANGIOSPERMS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; BODY PATTERNING; CELL LINEAGE; CELL POLARITY; COMPUTER SIMULATION; DIFFUSION; INDOLEACETIC ACIDS; MODELS, BIOLOGICAL; OVULE; VACUOLES; ZEA MAYS;

EID: 84887167952     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.098301     Document Type: Article

References (55)

1. Alon, U. (2007). An Introduction to Systems Biology: Design Principles of Biological Circuits, pp. 15. Boca Raton, FL: Chapman & Hall/CRC.
2. Bent, A. (2006). Arabidopsis thaliana floral dip transformation method. Methods Mol. Biol. 343, 87-103.
3. Chavarría-Krauser, A. and Ptashnyk, M. (2010). Homogenization of long-range auxin transport in plant tissues. Nonlinear Anal. Real World Appl. 11, 4524-4532.
4. Christensen, C. A., King, E. J., Jordan, J. R. and Drews, G. N. (1997). Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10, 49-64.
5. Ceccato, L., Masiero, S., Sinha Roy, D., Bencivenga, S., Roig-Villanova, I., Ditengou, F.A., Palme, K., Simon, R., and Colombo, L. (2013). Maternal control of PIN1 is required for female gametophyte development in Arabidopsis. PLoS ONE 8, e66148.
6. Curtis, M. D. and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
7. Dal Bosco, C., Dovzhenko, A., Liu, X., Woerner, N., Rensch, T., Eismann, M., Eimer, S., Hegermann, J., Paponov, I. A., Ruperti, B. et al. (2012). The endoplasmic reticulum localized PIN8 is a pollen specific auxin carrier involved in intracellular auxin homeostasis. Plant J. 71, 860-870.
8. de Lachapelle, A. M. and Bergmann, S. (2010). Precision and scaling in morphogen gradient read-out. Mol. Systems Biol. 6, 351.
9. Delbarre, A., Muller, P., Imhoff, V. and Guern, J. (1996). 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 198, 532-541.
10. Desfeux, C., Clough, S. J. and Bent, A. F. (2000). Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol. 123, 895-904.
11. Escobar-Restrepo, J.-M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.-C. and Grossniklaus, U. (2007). The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317, 656-660.
12. Evans, M. M. S. (2007). The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo Sac and leaf development. Plant Cell 19, 46-62.
13. Gallavotti, A., Yang, Y., Schmidt, R. J. and Jackson, D. (2008). The relationship between auxin transport and maize branching. Plant Physiol. 147, 1913-1923.
14. Gallie, D. R. (2002). The 5'-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res. 30, 3401-3411.
15. Garnett, P., Steinacher, A., Stepney, S., Clayton, R. and Leyser, O. (2010). Computer simulation: the imaginary friend of auxin transport biology. BioEssays 32, 828-835.
16. Geisler, M., Blakeslee, J. J., Bouchard, R., Lee, O. R., Vincenzetti, V., Bandyopadhyay, A., Titapiwatanakun, B., Peer, W. A., Bailly, A., Richards, E. L. et al. (2005). Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179-194.
17. Gregor, T., Bialek, W., de Ruyter van Steveninck, R. R., Tank, D. W. and Wieschaus, E. F. (2005). Diffusion and scaling during early embryonic pattern formation. Proc. Natl. Acad. Sci. USA 102, 18403-18407.
18. Grieneisen, V. A., Xu, J., Maree, A. F. M., Hogeweg, P. and Scheres, B. (2007). Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008-1013.
19. Gross-Hardt, R., Kägi, C., Baumann, N., Moore, J. M., Baskar, R., Gagliano, W. B., Jürgens, G. and Grossniklaus, U. (2007). LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol. 5, e47.
20. Guilfoyle, T. J. and Hagen, G. (2007). Auxin response factors. Curr. Opin. Plant Biol. 10, 453-460.
21. Gutknecht, J. and Walter, A. (1980). Transport of auxin (indoleacetic acid) through lipid bilayer membranes. J. Membr. Biol. 56, 65-72.
22. He, F., Saunders, T. E., Wen, Y., Cheung, D., Jiao, R., Rein ten Wolde, P., Howard, M. and Ma, J. (2010). Shaping a morphogen gradient for positional precision. Biophys. J. 99, 697-707.
23. Huang, B. Q. and Sheridan, W. F. (1994). Female gametophyte development in maize: microtubular organization and embryo sac polarity. Plant Cell 6, 845-861.
24. Johnston, A. J., Kirioukhova, O., Barrell, P. J., Rutten, T., Moore, J. M., Baskar, R., Grossniklaus, U. and Gruissem, W. (2010). Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle. PLoS Genet. 6, e1000988.
25. Krohn, N. G., Lausser, A., Juranić, M. and Dresselhaus, T. (2012). Egg cell signaling by the secreted peptide ZmEAL1 controls antipodal cell fate. Dev. Cell 23, 219-225.
26. Lander, A. D., Lo, W.-C., Nie, Q. and Wan, F. Y. (2009). The measure of success: constraints, objectives, and tradeoffs in morphogen-mediated patterning. Cold Spring Harb. Perspect. Biol. 1, a002022.
27. Liu, J., Mehdi, S., Topping, J., Tarkowski, P. and Lindsey, K. (2010). Modelling and experimental analysis of hormonal crosstalk in Arabidopsis. Mol. Syst. Biol. 6, 373.
28. Ljung, K., Ostin, A., Lioussanne, L. and Sandberg, G. (2001). Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. Plant Physiol. 125, 464-475.
29. Marchant, A., Kargul, J., May, S. T., Muller, P., Delbarre, A., Perrot-Rechenmann, C. and Bennett, M. J. (1999). AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 18, 2066-2073.
30. Moll, C., von Lyncker, L., Zimmermann, S., Kägi, C., Baumann, N., Twell, D., Grossniklaus, U. and Gross-Hardt, R. (2008). CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56, 913-921.
31. Mori, Y., Jilkine, A. and Edelstein-Keshet, L. (2008). Wave-pinning and cell polarity from a bistable reaction-diffusion system. Biophys. J. 94, 3684-3697.
32. Ottenschläger, I., Wolff, P., Wolverton, C., Bhalerao, R. P., Sandberg, G., Ishikawa, H., Evans, M. and Palme, K. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 100, 2987-2991.
33. Pagnussat, G. C., Yu, H.-J. and Sundaresan, V. (2007). 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 19, 3578-3592.
34. Pagnussat, G. C., Alandete-Saez, M., Bowman, J. L. and Sundaresan, V. (2009). Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324, 1684-1689.
35. Petrásek, J. and Friml, J. (2009). Auxin transport routes in plant development. Development 136, 2675-2688.
36. Ramos, J. A., Zenser, N., Leyser, O. and Callis, J. (2001). Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13, 2349-2360.
37. Rapparini, F., Tam, Y. Y. Y., Cohen, J. D. and Slovin, J. P. (2002). Indole-3-acetic acid metabolism in Lemna gibba undergoes dynamic changes in response to growth temperature. Plant Physiol. 128, 1410-1416.
38. Rotman, N., Durbarry, A., Wardle, A., Yang, W. C., Chaboud, A., Faure, J. E., Berger, F. and Twell, D. (2005). A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol. 15, 244-248.
39. Sbalzarini, I. F., Mezzacasa, A., Helenius, A. and Koumoutsakos, P. (2005). Effects of organelle shape on fluorescence recovery after photobleaching. Biophys. J. 89, 1482-1492.
40. Schmid, M. W., Schmidt, A., Klostermeier, U. C., Barann, M., Rosenstiel, P. and Grossniklaus, U. (2012). A powerful method for transcriptional profiling of specific cell types in eukaryotes: laser-assisted microdissection and RNA sequencing. PLoS ONE 7, e29685.
41. Schneitz, K., Hülskamp, M. and Pruitt, R. E. (1995). Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J. 7, 731-749.
42. Sequeira, L. and Mineo, L. (1966). Partial purification and kinetics of indoleacetic acid oxidase from tobacco roots. Plant Physiol. 41, 1200-1208.
43. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N. G., Palmer, A. E. and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
44. Srilunchang, K. O., Krohn, N. G. and Dresselhaus, T. (2010). DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 137, 333-345.
45. Sundaresan, V. and Alandete-Saez, M. (2010). Pattern formation in miniature: the female gametophyte of flowering plants. Development 137, 179-189.
46. Swarup, R. and Péret, B. (2012). AUX/LAX family of auxin influx carriers - an overview. Front. Plant Sci. 3, 225.
47. Swarup, K., Benková, E., Swarup, R., Casimiro, I., Péret, B., Yang, Y., Parry, G., Nielsen, E., De Smet, I., Vanneste, S. et al. (2008). The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946-954.
48. Tucker, M. R., Okada, T., Johnson, S. D., Takaiwa, F. and Koltunow, A. M. G. (2012). Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium. J. Exp. Bot. 63, 3229-3241.
49. Ulmasov, T., Murfett, J., Hagen, G. and Guilfoyle, T. J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963-1971.
50. Vernoux, T., Brunoud, G., Farcot, E., Morin, V., Van den Daele, H., Legrand, J., Oliva, M., Das, P., Larrieu, A., Wells, D. et al. (2011). The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7, 508.
51. Weijers, D., Schlereth, A., Ehrismann, J. S., Schwank, G., Kientz, M. and Jürgens, G. (2006). Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265-270.
52. Xiang, C., Han, P., Lutziger, I., Wang, K. and Oliver, D. J. (1999). A mini binary vector series for plant transformation. Plant Mol. Biol. 40, 711-717.
53. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J.G., Wu, M.J., Perrot-Rechenmann, C., Friml, J., Jones, A.M., and Yang, Z. (2010). Cell surface-and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110.
54. Yanagisawa, S. and Sheen, J. (1998). Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10, 75-89.
55. Yang, Y., Hammes, U. Z., Taylor, C. G., Schachtman, D. P. and Nielsen, E. (2006). High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123-1127.