THE PLANT CELL, Vol 6, Issue 3 333-349, Copyright © 1994 by American Society of Plant Biologists

RESEARCH ARTICLES

Homeotic Transformation of Ovules into Carpel-like Structures in Arabidopsis

Z. Modrusan, L. Reiser, K. A. Feldmann, R. L. Fischer and G. W. Haughn
Botany Department, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada

Ovules are specialized reproductive organs that develop within the carpels of higher plants. In Arabidopsis, mutations in two genes, BELL1 (BEL1) and APETALA2 (AP2), disrupt ovule development. In Bel1 ovules, the inner integument fails to form, the outer integument develops abnormally, and the embryo sac arrests at a late stage of megagametogenesis. During later stages of ovule development, cells of the outer integument of a Bel1 ovule sometimes develop into a carpel-like structure with stigmatic papillae and second-order ovules. The frequency of carpel-like structures was highest when plants were grown under conditions that normally induced flowering and was correlated with ectopic expression in the ovule of AGAMOUS (AG), an organ-identity gene required for carpel formation. Together, these results suggested that BEL1 negatively regulates AG late in ovule development. Likewise, mutants homozygous for the strong AP2 allele ap2-6 sometimes displayed structures with carpel-like features in place of ovules. However, such abnormal Ap2 ovules are much less ovulelike in morphology and form earlier than the Bel1 carpel-like structures. Because one role of the AP2 gene is to negatively regulate AG expression early in flower development, it is possible that AP2 works in a similar manner in the ovule. A novel ovule phenotype observed in Bel1/Ap2-6 double mutants suggested that BEL1 and AP2 genes function independently during ovule development.

This article has been cited by other articles:

				N. Winter, G. Kollwig, S. Zhang, and F. Kragler MPB2C, a Microtubule-Associated Protein, Regulates Non-Cell-Autonomy of the Homeodomain Protein KNOTTED1 PLANT CELL, October 1, 2007; 19(10): 3001 - 3018. [Abstract] [Full Text] [PDF]

				R. Kumar, K. Kushalappa, D. Godt, M. S. Pidkowich, S. Pastorelli, S. R. Hepworth, and G. W. Haughn The Arabidopsis BEL1-LIKE HOMEODOMAIN Proteins SAW1 and SAW2 Act Redundantly to Regulate KNOX Expression Spatially in Leaf Margins PLANT CELL, September 1, 2007; 19(9): 2719 - 2735. [Abstract] [Full Text] [PDF]

				V. Brambilla, R. Battaglia, M. Colombo, S. Masiero, S. Bencivenga, M. M. Kater, and L. Colombo Genetic and Molecular Interactions between BELL1 and MADS Box Factors Support Ovule Development in Arabidopsis PLANT CELL, August 1, 2007; 19(8): 2544 - 2556. [Abstract] [Full Text] [PDF]

				M. Gray-Mitsumune, M. O'Brien, C. Bertrand, F. Tebbji, A. Nantel, and D. P. Matton Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense J. Exp. Bot., December 1, 2006; 57(15): 4171 - 4187. [Abstract] [Full Text] [PDF]

				M. Cole, C. Nolte, and W. Werr Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana Nucleic Acids Res., March 2, 2006; 34(4): 1281 - 1292. [Abstract] [Full Text] [PDF]

				D. Chevalier, M. Batoux, L. Fulton, K. Pfister, R. K. Yadav, M. Schellenberg, and K. Schneitz STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis PNAS, June 21, 2005; 102(25): 9074 - 9079. [Abstract] [Full Text] [PDF]

				S. R. Hepworth, Y. Zhang, S. McKim, X. Li, and G. W. Haughn BLADE-ON-PETIOLE-Dependent Signaling Controls Leaf and Floral Patterning in Arabidopsis PLANT CELL, May 1, 2005; 17(5): 1434 - 1448. [Abstract] [Full Text] [PDF]

				M.-a. Ohto, R. L. Fischer, R. B. Goldberg, K. Nakamura, and J. J. Harada Control of seed mass by APETALA2 PNAS, February 22, 2005; 102(8): 3123 - 3128. [Abstract] [Full Text] [PDF]

				T. Payne, S. D. Johnson, and A. M. Koltunow KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium Development, August 1, 2004; 131(15): 3737 - 3749. [Abstract] [Full Text] [PDF]

				X. Bao, R. G. Franks, J. Z. Levin, and Z. Liu Repression of AGAMOUS by BELLRINGER in Floral and Inflorescence Meristems PLANT CELL, June 1, 2004; 16(6): 1478 - 1489. [Abstract] [Full Text] [PDF]

				D. J. Skinner, T. A. Hill, and C. S. Gasser Regulation of Ovule Development PLANT CELL, June 1, 2004; 16(suppl_1): S32 - S45. [Full Text] [PDF]

				M. P. Wakem and S. E. Kohalmi Mutation in the ap2-6 allele causes recognition of a cryptic splice site J. Exp. Bot., December 1, 2003; 54(393): 2655 - 2660. [Abstract] [Full Text] [PDF]

				M. E. Byrne, A. T. Groover, J. R. Fontana, and R. A. Martienssen Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER Development, September 1, 2003; 130(17): 3941 - 3950. [Abstract] [Full Text] [PDF]

				H. M. S. Smith and S. Hake The Interaction of Two Homeobox Genes, BREVIPEDICELLUS and PENNYWISE, Regulates Internode Patterning in the Arabidopsis Inflorescence PLANT CELL, August 1, 2003; 15(8): 1717 - 1727. [Abstract] [Full Text] [PDF]

				H. Chen, F. M. Rosin, S. Prat, and D. J. Hannapel Interacting Transcription Factors from the Three-Amino Acid Loop Extension Superclass Regulate Tuber Formation Plant Physiology, July 1, 2003; 132(3): 1391 - 1404. [Abstract] [Full Text] [PDF]

				S. Balasubramanian and K. Schneitz NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana Development, March 11, 2003; 129(18): 4291 - 4300. [Abstract] [Full Text] [PDF]

				H. M. S. Smith, I. Boschke, and S. Hake Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity PNAS, July 9, 2002; 99(14): 9579 - 9584. [Abstract] [Full Text] [PDF]

				R. Gro{beta}-Hardt, M. Lenhard, and T. Laux WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development Genes & Dev., May 1, 2002; 16(9): 1129 - 1138. [Abstract] [Full Text] [PDF]

				T. L. Western, Y. Cheng, J. Liu, and X. Chen HUA ENHANCER2, a putative DExH-box RNA helicase, maintains homeotic B and C gene expression in Arabidopsis Development, January 4, 2002; 129(7): 1569 - 1581. [Abstract] [Full Text] [PDF]

				T. L. Western, J. Burn, W. L. Tan, D. J. Skinner, L. Martin-McCaffrey, B. A. Moffatt, and G. W. Haughn Isolation and Characterization of Mutants Defective in Seed Coat Mucilage Secretory Cell Development in Arabidopsis Plant Physiology, November 1, 2001; 127(3): 998 - 1011. [Abstract] [Full Text] [PDF]

				T. Maes, N. Van de Steene, J. Zethof, M. Karimi, M. D'Hauw, G. Mares, M. Van Montagu, and T. Gerats Petunia Ap2-like Genes and Their Role in Flower and Seed Development PLANT CELL, February 1, 2001; 13(2): 229 - 244. [Abstract] [Full Text]

				B. A. Krizek, V. Prost, and A. Macias AINTEGUMENTA Promotes Petal Identity and Acts as a Negative Regulator of AGAMOUS PLANT CELL, August 1, 2000; 12(8): 1357 - 1366. [Abstract] [Full Text]

				J. Broadhvest, S. C. Baker, and C. S. Gasser SHORT INTEGUMENTS 2 Promotes Growth During Arabidopsis Reproductive Development Genetics, June 1, 2000; 155(2): 899 - 907. [Abstract] [Full Text]

				S Balasubramanian and K Schneitz NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana Development, January 10, 2000; 127(19): 4227 - 4238. [Abstract] [PDF]

				U. Schiefthaler, S. Balasubramanian, P. Sieber, D. Chevalier, E. Wisman, and K. Schneitz Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana PNAS, September 28, 1999; 96(20): 11664 - 11669. [Abstract] [Full Text] [PDF]

				M. V. Byzova, J. Franken, M. G.M. Aarts, J. de Almeida-Engler, G. Engler, C. Mariani, M. M. Van Lookeren Campagne, and G. C. Angenent Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development Genes & Dev., April 15, 1999; 13(8): 1002 - 1014. [Abstract] [Full Text]

				B. A. Hauser, J. M. Villanueva, and C. S. Gasser Arabidopsis TSO1 Regulates Directional Processes in Cells During Floral Organogenesis Genetics, September 1, 1998; 150(1): 411 - 423. [Abstract] [Full Text]

				G. Chuck, R. B. Meeley, and S. Hake The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1 Genes & Dev., April 15, 1998; 12(8): 1145 - 1154. [Abstract] [Full Text]

				K Schneitz, S. Baker, C. Gasser, and A Redweik Pattern formation and growth during floral organogenesis: HUELLENLOS and AINTEGUMENTA are required for the formation of the proximal region of the ovule primordium in Arabidopsis thaliana Development, January 7, 1998; 125(14): 2555 - 2563. [Abstract] [PDF]

				G. N. Drews, D. Lee, and C. A. Christensen Genetic Analysis of Female Gametophyte Development and Function PLANT CELL, January 1, 1998; 10(1): 5 - 18. [Abstract] [Full Text]

				J. K. Okamuro, B. Caster, R. Villarroel, M. Van Montagu, and K. D. Jofuku The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis PNAS, June 24, 1997; 94(13): 7076 - 7081. [Abstract] [Full Text] [PDF]

				K Schneitz, M Hulskamp, S. Kopczak, and R. Pruitt Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana Development, January 4, 1997; 124(7): 1367 - 1376. [Abstract] [PDF]