DOI: 10.1242/dev.122.11.3433. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking

Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking

10.1242/dev.122.11.3433

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT In Antirrhinum majus, petal and stamen organ identity is controlled by two MADS-box transcription factors, DEFICIENS and GLOBOSA. Mutations in either of these genes result in the replacement of petals by sepaloid organs and stamens by carpelloid organs. Somatically stable def and glo periclinal chimeras, generated by transposon excision events, were used to study the non-cell-autonomous functions of these two MADS-box proteins. Two morphologically distinct types of chimeras were analysed using genetic, morphological and molecular techniques. Restoration of DEF expression in the L1 cell layer results in the reestablishment of DEF and GLO functions in L1-derived cells only; inner layer cells retain their mutant sepaloid features. Nevertheless, this activity is sufficient to allow the expansion of petal lobes, highlighting the role of DEF in the stimulation of cell proliferation and/or cell shape and elongation when expressed in the L1 layer. Establishment of DEF or GLO expression in L2 and L3 cell layers is accompanied by the recovery of petaloid identity of the epidermal cells but it is insufficient to allow petal lobe expansion. We show by in situ immunolocalisation that the non-cell-autonomy is due to direct trafficking of DEF and GLO proteins from the inner layer to the epidermal cells. At least for DEF, this movement appears to be polar since DEF acts cell-autonomously when expressed in the L1 cell layer. Furthermore, the petaloid revertant sectors observed on second whorl mutant organs and the mutant margins of petals of L2L3 chimeras suggest that DEF and GLO intradermal movement is limited. This restriction may reflect the difference in the regulation of primary plasmodesmata connecting cells from the same layer and secondary plasmodesmata connecting cells from different layers. We propose that control of intradermal trafficking of DEF and GLO could play a role in maintaining of the boundaries of their expression domains.

Bibliography

Perbal, M.-C., Haughn, G., Saedler, H., & Schwarz-Sommer, Z. (1996). Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development, 122(11), 3433â3441.

Authors 4

Marie-Christine Perbal (first)
George Haughn (additional)
Heinz Saedler (additional)
Zsuzsanna Schwarz-Sommer (additional)

References 25 Referenced 178

10.1006/dbio.1996.0048 / Dev. Biol / Cellular interactions mediated by the homeotic PISTILLATA gene determine cell fate in the Arabidopsis flower by Bouhidel (1996)
10.1101/gad.4.9.1483 / Genes Dev / Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus by Carpenter (1990)
10.1242/dev.121.1.19 / Development / Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers by Carpenter (1995)
10.1002/j.1537-2197.1953.tb06463.x / Am. J. Bot / Periclinal cytochimeras and the origin of tissues in stem and leaf of peach by Dermen (1953)
10.1101/gad.8.13.1548 / Genes Dev / Function and regulation of the Arabidopsis floral homeotic gene Pistillata by Goto (1994)
10.1242/dev.121.1.27 / Development / Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems by Hantke (1995)
10.2307/3869769 / Plant Cell / Determination and cell interactions in reproductive meristems by Huala (1993)
10.1002/j.1460-2075.1992.tb05168.x / EMBO J / Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus by Huijser (1992)
10.1016/0092-8674(92)90144-2 / Cell / The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens by Jack (1992)
10.1126/science.270.5244.1980 / Science / Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata by Lucas (1995)
10.1111/j.1469-8137.1993.tb03897.x / New Phytol / Plasmodesmata and the supracellular nature of plants by Lucas (1993)
10.1007/BF00039385 / Plant Mol. Biol. (in press) / Plasmodesmatal cell-to-cell transport of proteins and nucleic acids by Mezitt (1996)
10.1038/378199a0 / Nature / Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries by Sakai (1995)
10.1002/j.1537-2197.1944.tb08063.x / Am. J. Bot / Periclinal chimeras in Datura in relation to development and structure (A) of the style and stigma (B) of calyx and corolla by Satina (1944)
10.1002/j.1537-2197.1940.tb13952.x / Am. J. Bot / Demonstration of the three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras by Satina (1940)
10.1002/j.1460-2075.1992.tb05048.x / EMBO J / Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development by Schwarz-Sommer (1992)
10.1002/j.1460-2075.1990.tb08152.x / EMBO J / Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors by Sommer (1990)
10.1242/dev.113.Supplement_1.169 / Development / Properties of deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus by Sommer (1991)
{'key': '2025021323493690200_DEVELOP_122_11_3433C19', 'first-page': '131', 'article-title': 'Ontogeny of the primary body in chimeral forms of higher plants', 'volume-title': 'The Clonal Basis of Development', 'author': 'Stewart', 'year': '1978'} / The Clonal Basis of Development / Ontogeny of the primary body in chimeral forms of higher plants by Stewart (1978)
10.1016/0092-8674(89)90895-7 / Cell / Developmental programming of the shoot meristem by Sussex (1989)
{'key': '2025021323493690200_DEVELOP_122_11_3433C21', 'first-page': '1089', 'article-title': 'The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras', 'volume': '4', 'author': 'Szymkowiak', 'year': '1992', 'journal-title': 'Plant Cell'} / Plant Cell / The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras by Szymkowiak (1992)
10.1046/j.1365-313X.1993.04010001.x / Plant J / Effect of lateral suppressor on petal initiation in tomato by Szymkowiak (1993)
10.1002/j.1460-2075.1992.tb05574.x / EMBO J / GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis by Tröbner (1992)
10.1016/S0960-9822(95)00282-X / Curr. Biol / Cell lineage patterns and homeotic gene activity during Antirrhinum flower development by Vincent (1995)
10.1242/dev.121.9.2861 / Development / Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature- sensitive mutant by Zachgo (1995)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:29 p.m.)
Deposited	6 months, 2 weeks ago (Feb. 13, 2025, 6:50 p.m.)
Indexed	3 weeks, 4 days ago (Aug. 5, 2025, 9 a.m.)
Issued	28 years, 9 months ago (Nov. 1, 1996)
Published	28 years, 9 months ago (Nov. 1, 1996)
Published Online	28 years, 9 months ago (Nov. 1, 1996)
Published Print	28 years, 9 months ago (Nov. 1, 1996)

Funders 0

None

BibTeX

@article{Perbal_1996, title={Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking}, volume={122}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.122.11.3433}, DOI={10.1242/dev.122.11.3433}, number={11}, journal={Development}, publisher={The Company of Biologists}, author={Perbal, Marie-Christine and Haughn, George and Saedler, Heinz and Schwarz-Sommer, Zsuzsanna}, year={1996}, month=nov, pages={3433–3441} }

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