The gene
                    ENHANCER OF PINOID
                    controls cotyledon development in the
                    Arabidopsis
                    embryo

Birgit S. Treml; Sabine Winderl; Roman Radykewicz; Markus Herz; Günther Schweizer; Peter Hutzler; Erich Glawischnig; Ramón A. Torres Ruiz

doi:10.1242/dev.01969

journal article Sep 15, 2005

The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo

Birgit S. Treml Sabine Winderl Roman Radykewicz Markus Herz Günther Schweizer Peter Hutzler Erich Glawischnig Ramón A. Torres Ruiz

Development Vol. 132 No. 18 pp. 4063-4074 · The Company of Biologists

View at Publisher Save 10.1242/dev.01969

Abstract

During Arabidopsis embryo development, cotyledon primordia are generated at transition stage from precursor cells that are not derived from the embryonic shoot apical meristem (SAM). To date, it is not known which genes specifically instruct these precursor cells to elaborate cotyledons, nor is the role of auxin in cotyledon development clear. In laternemutants, the cotyledons are precisely deleted, yet the hypocotyl and root are unaffected. The laterne phenotype is caused by a combination of two mutations: one in the PINOID (PID) gene and another mutation in a novel locus designated ENHANCER OF PINOID (ENP). The expression domains of shoot apex organising genes such as SHOOT MERISTEMLESS (STM) extend along the entire apical region of laterne embryos. However, analysis of pid enp stm triple mutants shows that ectopic activity of STM does not appear to cause cotyledon obliteration. This is exclusively caused by enp in concert with pid. In pinoid embryos, reversal of polarity of the PIN1 auxin transport facilitator in the apex is only occasional, explaining irregular auxin maxima in the cotyledon tips. By contrast, polarity of PIN1:GFP is completely reversed to basal position in the epidermal layer of the laterne embryo. Consequently auxin, which is believed to be essential for organ formation, fails to accumulate in the apex. This strongly suggests that ENP specifically regulates cotyledon development through control of PIN1 polarity in concert with PID.

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References

60

[1]

Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. and Tasaka,M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell9,841-857. 10.1105/tpc.9.6.841

[2]

Aida, M., Ishida, T. and Tasaka, M. (1999). Shoot apical meristem and cotyledon formation during Arabidopsisembryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development126,1563-1570.

[3]

Barton, M. K. and Poethig, R. S. (1993). Formation of the shoot apical meristem in Arabidopsis thaliana: an anlysis of development in the wild-type and in the shoot meristemless mutant. Development119,823-831. 10.1242/dev.119.3.823

[4]

Baud, S., Bellec, Y., Miquel, M., Bellini, C., Caboche, M.,Lepiniec, L., Faure, J. D. and Rochat, C. (2004). gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. EMBO J.5, 515-520. 10.1038/sj.embor.7400124

[5]

Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. and Offringa, R. (2001). The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development128,4057-4067.

[6]

Benjamins, R., Ampudia, C. S., Hooykaas, P. J. and Offringa,R. (2003). PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol.132,1623-1630. 10.1104/pp.103.019943

[7]

Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T.,Seifertova, D., Jurgens, G. and Friml, J. (2003). Local,efflux-dependent auxin gradients as a common module for plant organ formation. Cell115,591-602. 10.1016/s0092-8674(03)00924-3

[8]

Bennett, S. R. M., Alvarez, J., Bossinger, G. and Smyth, D. R. (1995). Morphogenesis in pinoid mutants of Arabidopsis thaliana.Plant J.8, 505-520. 10.1046/j.1365-313x.1995.8040505.x

[9]

Berleth, T. and Jürgens, G. (1993). The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development118,575-587. 10.1242/dev.118.2.575

[10]

Berleth, T. and Chatfield, S. (2002). Embryogenesis: Pattern Formation from a Single Cell. In TheArabidopsis Book (ed. C. R. Somerville and E. M. Meyerowitz). Rockville, MD: American Society of Plant Biologists. doi/10.1199/tab.0051

[11]

Blilou. I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I.,Friml, J., Heidstra, R., Aida, M., Palme, K. and Scheres, B.(2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature433, 39-44. 10.1038/nature03184

[12]

Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. and Simon, R. (2000). Dependence of the stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science289,817-819. 10.1126/science.289.5479.617

[13]

Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis

Mary E. Byrne, Ross Barley, Mark Curtis et al.

Nature 10.1038/35050091

[14]

Christensen, S. K., Dagenais, N., Chory, J. and Weigel, D.(2000). Regulation of auxin response by the protein kinase PINOID.Cell100,469-478. 10.1016/s0092-8674(00)80682-0

[15]

Conway, L. J. and Poethig, R. S. (1997). Mutations of Arabidopsis thaliana that transform leaves into cotyledons. Proc. Natl. Acad. Sci. USA94,10209-10214. 10.1073/pnas.94.19.10209

[16]

Elliott, R. C., Betzner, A. S., Huttner, E., Oakes, M. P.,Tucker, W. Q., Gerentes, D., Perez, P. and Smyth, D. R.(1996). AINTEGUMENTA, an APETALA-2 like gene in Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell8, 155-168.

[17]

Erschadi, S., Haberer, G., Schöniger, M. and Torres Ruiz,R. A. (2000). Estimating genetic diversity of Arabidopsis thaliana ecotypes with Amplified Fragment Length Polymorphisms (AFLP). Theor. Appl. Genet.100,633-640.

[18]

Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H.,Hamann, T., Offringa, R. and Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis.Nature426,147-153. 10.1038/nature02085

[19]

Friml, J., Yang, X., Michniewicz, M., Weijers Quint, A., Tietz,O., Benjamins, R., Ouwerkerk, P. B. F., Ljung, K., Sandberg, G., Hooykaas, P. J. J. et al. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science306,862-865. 10.1126/science.1100618

[20]

Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M. and Aida, M. (2004). PIN-FORMED1 and PINOIDregulate boundary formation and cotyledon development in Arabidopsisembryogenesis. Development131,5021-5030.

[21]

Gälweiler, L., Guan, C., Müller, A., Wisman, E.,Mendgen, K., Yephremov, A. and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science282,2226-2230. 10.1126/science.282.5397.2226

[22]

Geldner, N., Richter, S., Vieten, A., Marquardt, S.,Torres-Ruiz, R. A., Mayer, U. and Jürgens, G. (2004). Partial loss-of-function alleles reveal a role for GNOM in post-embryonic and auxin-transport related development of Arabidopsis.Development131,389-400. 10.1242/dev.00926

[23]

Haberer, G., Erschadi, S. and Torres Ruiz, R. A.(2002). The Arabidopsis gene PEPINO/PASTICINO2is required for proliferation control of meristematic and non-meristematic cells and encodes a putative anti-phosphatatse. Dev. Genes Evol.212,542-550. 10.1007/s00427-002-0273-9

[24]

Hadfi, K., Speth, V. and Neuhaus, G. (1998). Auxin-induced developmental patterns in Brassica juncea embryos. Development125,879-887. 10.1242/dev.125.5.879

[25]

Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S.,Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C. and Machida,Y. (2002). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol.5,467-478. 10.1093/pcp/pcf077

[26]

Jürgens, G. (2001). Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J.20,3609-3616. 10.1093/emboj/20.14.3609

[27]

Kaplan, D. (1969). Seed development in Downingia. Phytomorphology19,253-278.

[28]

Kaplan, D. R. and Cooke, T. J. (1997). Fundamental concepts in the embryogenesis of dicotyledons - a morphological interpretation of embryo mutants. Plant Cell9,1903-1919.

[29]

Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. and Poethig, R. S. (2001). KANADI regulates organ polarity in Arabidopsis.Nature411,706-709. 10.1038/35079629

[30]

Klucher, K. M., Chow, H., Reiser, L. and Fischer, R. L.(1996). The AINTEGUMENTA gene of Arabidopsisrequired for ovule and female gametophyte development is related to the floral homeotic gene APETALA2.Plant Cell8, 137-153.

[31]

Kumaran, M. K., Bowman, J. L. and Sundaresan, V.(2002). YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis.Plant Cell14,2761-2770. 10.1105/tpc.004911

[32]

Ljung, K., Bhalerao, R. P. and Sandberg, G.(2001). Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J.28,465-474. 10.1046/j.1365-313x.2001.01173.x

[33]

The development of apical embryonic pattern in Arabidopsis

Jeff A. Long, M. Kathryn Barton

Development 10.1242/dev.125.16.3027

[34]

Long, J. A., Moan, E. I., Medford, J. I. and Barton, M. K.(1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis.Nature379,66-69. 10.1038/379066a0

[35]

Long, J. A., Woody, S., Poethig, S., Meyerowitz, E. M. and Barton, M. K. (2002). Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development129,2297-2306.

[36]

Lotan, T., Ohto, M., Yee, K. M., West, M. A. L., Lo, R., Kwong,R., Yamagishi, K., Fischer, R. L., Goldberg, R. B. and Harada, J. J.(1998). Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell93,1195-1205. 10.1016/s0092-8674(00)81463-4

[37]

Lukowitz, W., Gillmor, C. S. and Scheible, W. R.(2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol.123,795-805.

[38]

Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M.,Masson, P. and Barton, M. K. (1999). The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsisdevelopment and has overlapping functions with the ARGONAUTE gene. Development126,469-481.

[39]

Mayer, K. F. X., Schoof, H., Haecker, A., Lenhard, M.,Jürgens, G. and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsisshoot meristem. Cell95,805-815. 10.1016/s0092-8674(00)81703-1

[40]

Mayer, U., Torres Ruiz, R. A., Berleth, T., Misera, S. and Jürgens, G. (1991). Mutations affecting body organization in the Arabidopsis embryo. Nature353,402-407. 10.1038/353402a0

[41]

Mayer, U., Büttner, G. and Jürgens, G.(1993). Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the GNOM gene. Development117,149-162. 10.1242/dev.117.1.149

[42]

McConnell, J. R., Emery, J., Eshed, Y., Bao, N., Bowman, J. and Barton, M. K. (2001). Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature411,709-713. 10.1038/35079635

[43]

Meinke, D. W. (1992). A homeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science258,1647-1650. 10.1126/science.258.5088.1647

[44]

Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis

B. Moussian

The EMBO Journal 10.1093/emboj/17.6.1799

[45]

Okada, K., Ueda, J., Komaki, M. K., Bell, C. J. and Shimura,Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell3,677-684.

[46]

Reinhardt, D., Mandel, T. and Kuhlemeier, C.(2000). Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell12,507-518. 10.1105/tpc.12.4.507

[47]

Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T.,Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C.(2003). Regulation of phyllotaxis by polar auxin transport. Nature426,255-260. 10.1038/nature02081

[48]

An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root

Sabrina Sabatini, Dimitris Beis, Harald Wolkenfelt et al.

Cell 10.1016/s0092-8674(00)81535-4

[49]

Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Morita, E. H. and Okada, K. (1999). FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev.13,1079-1088. 10.1101/gad.13.9.1079

[50]

Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.-T.,Janmaat, K., Weisbeek, P. and Benfey, P. (1995). Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development, 121,53-62. 10.1242/dev.121.1.53

Showing 50 of 60 references

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Details

Published: Sep 15, 2005
Vol/Issue: 132(18)
Pages: 4063-4074

Authors

B

Birgit S. Treml

Lehrstuhl für Genetik, Technische Universität München,Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,Germany

S

Sabine Winderl

Lehrstuhl für Genetik, Technische Universität München,Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,Germany

R

Roman Radykewicz

Lehrstuhl für Genetik, Technische Universität München,Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,Germany

M

Markus Herz

Bayerische Landesanstalt für Landwirtschaft, Institut für Pflanzenbau und -züchtung, IPZ 1b, Am Gereuth 2, 85354 Freising,Germany

G

Günther Schweizer

Bayerische Landesanstalt für Landwirtschaft, Institut für Pflanzenbau und -züchtung, IPZ 1b, Am Gereuth 2, 85354 Freising,Germany

P

Peter Hutzler

Institut für Pathologie, GSF-Forschungszentrum für Umwelt und Gesundheit GmbH, 85764 Neuherberg, Germany

E

Erich Glawischnig

Lehrstuhl für Genetik, Technische Universität München,Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,Germany

R

Ramón A. Torres Ruiz

Lehrstuhl für Genetik, Technische Universität München,Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,Germany

Cite This Article

Birgit S. Treml, Sabine Winderl, Roman Radykewicz, et al. (2005). The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development, 132(18), 4063-4074. https://doi.org/10.1242/dev.01969

The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo

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