DOI: 10.1242/dev.121.4.975. LEUNIG regulates AGAMOUS expression in Arabidopsis flowers

LEUNIG regulates AGAMOUS expression in Arabidopsis flowers

10.1242/dev.121.4.975

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT LEUNIG was identified in a genetic screen designed to isolate second-site enhancer mutations of the floral homeotic mutant apetala2-1. leunig mutations not only enhance apetala2, but by themselves cause a similar but less-pronounced homeotic transformation than apetala2 mutations. leunig flowers have sepals that are transformed toward stamens and carpels, and petals that are either staminoid or absent. In situ hybridization experiments with leunig mutants revealed altered expression pattern of the floral homeotic genes APETALA1, APETALA3, PISTIL-LATA, and AGAMOUS. Double mutants of leunig and agamous exhibited a phenotype similar to agamous single mutants, indicating that agamous is epistatic to leunig. Our analysis suggests that a key role of LEUNIG is to negatively regulate AGAMOUS expression in the first two whorls of the Arabidopsis flower.

Bibliography

Liu, Z., & Meyerowitz, E. M. (1995). LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development, 121(4), 975â991.

Authors 2

Zhongchi Liu (first)
Elliot M. Meyerowitz (additional)

References 43 Referenced 183

10.1242/dev.101.1.1 / Development / The molecular basis for metameric pattern in the Drosophila embryo by Akam (1987)
10.1046/j.1365-313X.1993.04010101.x / Plant J / Petal and stamen formation in petunia is regulated by the homeotic gene FBP1 by Angenent (1993)
{'key': '2025011513521990600_DEVELOP_121_4_975C3', 'first-page': '37', 'article-title': 'Genes directing flower development in Arabidopsis', 'volume': '1', 'author': 'Bowman', 'year': '1989', 'journal-title': 'Plant Cell'} / Plant Cell / Genes directing flower development in Arabidopsis by Bowman (1989)
10.1242/dev.112.1.1 / Development / Genetic interactions among floral homeotic genes of Arabidopsis by Bowman (1991)
10.1242/dev.114.3.599 / Development / SUPERMAN, a regulator of floral homeotic genes in Arabidopsis by Bowman (1992)
10.1242/dev.119.3.721 / Development / Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes by Bowman (1993)
10.1016/0092-8674(93)90052-R / Cell / Complementary floral homeotic phenotypes result from opposite orientation of a transposon at the plena locus of Antirrhinum by Bradley (1993)
10.1101/gad.4.9.1483 / Genes Dev / Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus by Carpenter (1990)
10.1038/353031a0 / Nature / The war of whorls: genetic interactions controlling flower development by Coen (1991)
10.1007/BF03015868 / Plant Mol. Biol. Rep / Petunia hybrida: a short description of the action of 91 genes, their origin and map location by de Vlaming (1984)
10.1016/0092-8674(91)90551-9 / Cell / Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product by Drews (1991)
{'volume-title': 'Morphology and Evolution of Vascular Plants', 'year': '1988', 'author': 'Gifford', 'key': '2025011513521990600_DEVELOP_121_4_975C12'} / Morphology and Evolution of Vascular Plants by Gifford (1988)
10.1016/0092-8674(94)90178-3 / Cell / Regulation of the Arabidopsis floral homeotic gene APETALA1 by Gustafson-Brown (1994)
10.1101/gad.8.13.1548 / Genes Dev / Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA by Goto (1994)
10.1038/329219a0 / Nature / Functional inactivation of genes by dominant negative mutations by Herskowitz (1987)
10.2307/3869458 / Plant Cell / LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development by Huala (1992)
10.1038/335025a0 / Nature / The molecular genetics of embryonic pattern formation in Drosophila by Ingham (1988)
{'key': '2025011513521990600_DEVELOP_121_4_975C18', 'first-page': '741', 'article-title': 'Function of the apetala-1 gene during Arabidopsis floral development', 'volume': '2', 'author': 'Irish', 'year': '1990', 'journal-title': 'Plant Cell'} / Plant Cell / Function of the apetala-1 gene during Arabidopsis floral development by Irish (1990)
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)
10.1016/0092-8674(94)90509-6 / Cell / Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and post-transcriptional regulation determine floral organ identity by Jack (1994)
{'key': '2025011513521990600_DEVELOP_121_4_975C21', 'first-page': '1211', 'article-title': 'Control of Arabidopsis flower and seed development by the homeotic gene APETALA2', 'volume': '6', 'author': 'Jofuku', 'year': '1994', 'journal-title': 'Plant Cell'} / Plant Cell / Control of Arabidopsis flower and seed development by the homeotic gene APETALA2 by Jofuku (1994)
10.1242/dev.104.2.195 / Development / Isolation and characterization of novel mutants of Arabidopsis thaliana defective in flower development by Komaki (1988)
10.2307/3868917 / Plant Cell / AP2 gene determines the identity of perianth organs in flowers of Arabidopsis thaliana by Kunst (1989)
10.1016/0012-1606(87)90349-6 / Dev. Biol / The argentia mutation delays normal development of photosynthetic cell-types in Zea mays by Langdale (1987)
10.2307/3869758 / Plant Cell / A seed shape mutant of Arabidopsis that is affected in integument development by Leon-Kloosterziel (1994)
10.1038/276565a0 / Nature / A gene complex controlling segmentation in Drosophila by Lewis (1978)
10.1038/360273a0 / Nature / Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 by Mandel (1992)
10.1016/0092-8674(88)90244-9 / Cell / Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element by Norman (1988)
10.1016/0022-2836(88)90358-0 / J. Mol. Biol / A Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MATa cells by Passmore (1988)
{'key': '2025011513521990600_DEVELOP_121_4_975C30', 'first-page': '163', 'article-title': 'Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants', 'volume': '6', 'author': 'Pnueli', 'year': '1994', 'journal-title': 'Plant Cell'} / Plant Cell / Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants by Pnueli (1994)
10.1016/0012-1606(90)90053-L / Dev. Biol / Control of the initiation of homeotic gene expression by the gap genes giant and tailless in Drosophila by Reinitz (1990)
10.2307/3869229 / Plant Cell / The FLO10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers by Schultz (1992)
10.1242/dev.119.3.745 / Development / Genetic analysis of the floral initiation process (FLIP) in Arabidopsis by Schultz (1993)
10.1126/science.250.4983.931 / Science / Genetic control of flower development: homeotic genes of Antirrhinum Majus by Schwarz-Sommer (1990)
{'key': '2025011513521990600_DEVELOP_121_4_975C35', 'first-page': '755', 'article-title': 'Early flower development in Arabidopsis', 'volume': '2', 'author': 'Smyth', 'year': '1990', 'journal-title': 'Plant Cell'} / Plant Cell / Early flower development in Arabidopsis by Smyth (1990)
10.2307/3869807 / Plant Cell / Genetic interaction that regulate inflorescence development in Arabidopsis by Shannon (1993)
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 (1992)
{'key': '2025011513521990600_DEVELOP_121_4_975C38', 'first-page': '843', 'article-title': 'Ectopic expression of pMADS3 in transgenic petunia blind mutant', 'volume': '5', 'author': 'Tsuchimoto', 'year': '1993', 'journal-title': 'Plant cell'} / Plant cell / Ectopic expression of pMADS3 in transgenic petunia blind mutant by Tsuchimoto (1993)
10.1101/gad.7.7a.1214 / Gene Dev / Functional analysis of petunia floral homeotic MADS box gene PMADS1 by van der Krol (1993)
10.1016/0092-8674(92)90295-N / Cell / LEAFY controls floral meristem identity in Arabidopsis by Weigel (1992)
10.1126/science.261.5129.1723 / Science / Activation of floral homeotic genes in Arabidopsis by Weigel (1993)
10.1016/0092-8674(94)90291-7 / Cell / The ABCs of floral homeotic genes by Weigel (1994)
10.1038/346035a0 / Nature / The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors by Yanofsky (1990)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:16 p.m.)
Deposited	7 months, 2 weeks ago (Jan. 15, 2025, 8:52 a.m.)
Indexed	1 week, 5 days ago (Aug. 21, 2025, 1:47 p.m.)
Issued	30 years, 5 months ago (April 1, 1995)
Published	30 years, 5 months ago (April 1, 1995)
Published Online	30 years, 5 months ago (April 1, 1995)
Published Print	30 years, 5 months ago (April 1, 1995)

Funders 0

None

BibTeX

@article{Liu_1995, title={LEUNIG regulates AGAMOUS expression in Arabidopsis flowers}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.4.975}, DOI={10.1242/dev.121.4.975}, number={4}, journal={Development}, publisher={The Company of Biologists}, author={Liu, Zhongchi and Meyerowitz, Elliot M.}, year={1995}, month=apr, pages={975–991} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>LEUNIG was identified in a genetic screen designed to isolate second-site enhancer mutations of the floral homeotic mutant apetala2-1. leunig mutations not only enhance apetala2, but by themselves cause a similar but less-pronounced homeotic transformation than apetala2 mutations. leunig flowers have sepals that are transformed toward stamens and carpels, and petals that are either staminoid or absent. In situ hybridization experiments with leunig mutants revealed altered expression pattern of the floral homeotic genes APETALA1, APETALA3, PISTIL-LATA, and AGAMOUS. Double mutants of leunig and agamous exhibited a phenotype similar to agamous single mutants, indicating that agamous is epistatic to leunig. Our analysis suggests that a key role of LEUNIG is to negatively regulate AGAMOUS expression in the first two whorls of the Arabidopsis flower.</jats:p>",
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