Abstract
Unlike in animals where cell migrations and programmed cell death play key roles in organ shape determination, in plants organ shape is largely a result of coordinated cellular growth (cell divisions and cell elongations). We have investigated the role of the SEUSS and LEUNIG genes in Arabidopsis thaliana (L.) Heynh. petal development to better understand the molecular mechanisms through which cellular growth and organ shape are coordinated in plants. SEUSS and LEUNIG encode components of a putative transcriptional regulatory complex that controls organ identity specification through the repression of the floral organ identity gene AGAMOUS. SEUSS and LEUNIG also regulate petal shape through AGAMOUS-independent mechanisms; however, the molecular and cellular actions of SEUSS and LEUNIG during petal development are unknown. Here we show that SEUSS and LEUNIG control blade cell number and vasculature development within the petal. Furthermore, SEUSS and LEUNIG regulate petal polarity along the adaxial/abaxial axis. We present a model where SEUSS and LEUNIG are required to potentiate the key polarity genes PHABULOSA and FILAMENTOUS FLOWER/YABBY1 and thus influence cellular growth within the developing petal blade.
Similar content being viewed by others
Abbreviations
- HD-ZIP:
-
Homeodomain-leucine zipper
- SEM:
-
Scanning electron microscopy
- s.d.:
-
Standard deviation
- FIL/YAB1 :
-
FILAMENTOUS FLOWER/YABBY1
- PHB :
-
PHABULOSA
References
Agulnick AD, Taira M, Breen JJ, Tanaka T, Dawid IB, Westphal H (1996) Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384:270–272
Avery GS (1933) Structure and development of the tobacco leaf. Am J Bot 20:565–592
Bach I, Carriere C, Ostendorff HP, Andersen B, Rosenfeld MG (1997) A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev 11:1370–1380
Bowman JL (1994) Arabidopsis: an atlas of morphology and development. Springer, Berlin Heidelberg New York
Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Conner J, Liu Z (2000) LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proc Natl Acad Sci USA 97:12902–12907
Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2–like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168
Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774
Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209
Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260
Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006
Fisher AL, Caudy M (1998) Groucho proteins: transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev 12:1931–1940
Flores-Saaib RD, Courey AJ (2000) Analysis of Groucho-histone interactions suggests mechanistic similarities between Groucho- and Tup1-mediated repression. Nucleic Acids Res 28:4189–4196
Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129:253–263
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529
Jurata LW, Gill GN (1997) Functional analysis of the nuclear LIM domain interactor NLI. Mol Cell Biol 17:5688–5698
Kanaya E, Nakajima N, Okada K (2002) Non-sequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA. J Biol Chem 277:11957–11964
Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709
Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153
Krizek BA (1999) Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev Genet 25:224–236
Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12:1357–1366
Kumaran MK, Bowman JL, Sundaresan V (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14:2761–2770
Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–1876
Liu Z, Franks RG, Klink VP (2000) Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12:1879–1892
Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991
Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142
Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035
McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942
McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713
Meister RJ, Kotow LM, Gasser CS (2002) SUPERMAN attenuates positive INNER NO OUTER autoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 129:4281–4289
Meister RJ, Oldenhof H, Bowman JL, Gasser CS (2005) Multiple protein regions contribute to differential activities of YABBY proteins in reproductive development. Plant Physiol 137:651–662
Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947
Morcillo P, Rosen C, Baylies MK, Dorsett D (1997) Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila. Genes Dev 11:2729–2740
Navarro C, Efremova N, Golz JF, Rubiera R, Kuckenberg M, Castillo R, Tietz O, Saedler H, Schwarz-Sommer Z (2004) Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development 131:3649–3659
Nelson T, Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9:1121–1135
Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25:223–236
Pfluger J, Zambryski P (2004) The role of SEUSS in auxin response and floral organ patterning. Development 131:4697–4707
Poethig RS, Sussex IM (1985a) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165:170–184
Poethig RS, Sussex IM (1985b) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165:158–169
Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76
Sawa S, Watanabe K, Goto K, Kanaya E, Morita EH, 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
Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Sridhar VV, Surendrarao A, Gonzalez D, Conlan RS, Liu Z (2004) Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proc Natl Acad Sci USA 101:11494–11499
Sussex IM (1954) Experiments on the cause of dorsoventrality in leaves. Nature 174:351–352
Sussex IM (1955) Morphogenesis in Solanum tuberosum L.: experimental investigation of leaf dorsoventrality and orientation in the juvenile shoot. Phytomorphology 5:286–300
Theissen G, Saedler H (2001) Plant biology: floral quartets. Nature 409:469–471
Timmermans M, Schultes N, Jankovsky J, Nelson T (1998) Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125:2813–2823
van Meyel DJ, Thomas JB, Agulnick AD (2003) Ssdp proteins bind to LIM-interacting co-factors and regulate the activity of LIM-homeodomain protein complexes in vivo. Development 130:1915–1925
Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154
Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346:35–39
Zhong R, Ye Z-H (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, Encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139–2152
Zhong R, Ye Z-H (2004) amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45:369–385
Zik M, Irish VF (2003) Flower development: initiation, differentiation, and diversification. Annu Rev Cell Dev Biol 19:119–140
Acknowledgments
We thank John Bowman for providing PHB and YAB1/FIL in situ probes; Yuki Mizukami for suggestions regarding petal cell size analysis; Sridevi Ashakanandam for technical assistance; undergraduate researchers Sarah Stefanos and Bill Tran; and the UC Berkeley and NCSU Centers for Electron Microscopy. We thank Jose Alonso, Anna Stepanova, Beth Krizek, Tzung-Fu Hsieh, and anonymous reviewers for commenting on the manuscript. This work was funded by the following grants: NSF IOB-0416759, USDA ARS NC06759 and NIH NRSA Postdoctoral Fellowship GM20426-02 to R.G.F.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Franks, R.G., Liu, Z. & Fischer, R.L. SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals. Planta 224, 801–811 (2006). https://doi.org/10.1007/s00425-006-0264-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-006-0264-6