Abstract
Flowers are determinate shoots comprised of perianth and reproductive organs displayed in a whorled phyllotactic pattern. Floral organ identity genes display region-specific expression patterns in the developing flower. In Arabidopsis, floral organ identity genes are activated by LEAFY (LFY), which functions with region-specific co-regulators, UNUSUAL FLORAL ORGANS (UFO) and WUSCHEL (WUS), to up-regulate homeotic genes in specific whorls of the flower. PENNYWISE (PNY) and POUND-FOOLISH (PNF) are redundant functioning BELL1-like homeodomain proteins that are expressed in shoot and floral meristems. During flower development, PNY functions with a co-repressor complex to down-regulate the homeotic gene, AGAMOUS (AG), in the outer whorls of the flower. However, the function of PNY as well as PNF in regulating floral organ identity in the central whorls of the flower is not known. In this report, we show that combining mutations in PNY and PNF enhance the floral patterning phenotypes of weak and strong alleles of lfy, indicating that these BELL1-like homeodomain proteins play a role in the specification of petals, stamens and carpels during flower development. Expression studies show that PNY and PNF positively regulate the homeotic genes, APETALA3 and AG, in the inner whorls of the flower. Moreover, PNY and PNF function in parallel with LFY, UFO and WUS to regulate homeotic gene expression. Since PNY and PNF interact with the KNOTTED1-like homeodomain proteins, SHOOTMERISTEMLESS (STM) and KNOTTED-LIKE from ARABIDOPSIS THALIANA2 (KNAT2) that regulate floral development, we propose that PNY/PNF-STM and PNY/PNF-KNAT2 complexes function in the inner whorls to regulate flower patterning events.
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Abbreviations
- SAM:
-
Shoot apical meristem
- KNOX:
-
Knotted1-like homeobox
- BLH:
-
BELL1-like homeobox
- PNY:
-
PENNYWISE
- PNF:
-
POUND-FOOLISH
- LFY:
-
LEAFY
- UFO:
-
UNUSUAL FLORAL ORGANS
- WUS:
-
WUSCHEL
- AP3:
-
APETALA3
- AG:
-
AGAMOUS
- STM:
-
SHOOTMERISTEMLESS
References
Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056
Bao X, Franks RG, Levin JZ, Liu Z (2004) Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems. Plant Cell 16:1478–1489
Bennett T, Leyser O (2006) Something on the side: axillary meristem and plant development. Plant Mol Biol 60:843–854
Bhatt AM, Etchells JP, Canales C, Lagodienko A, Dickinson H (2004) VAAMANA—a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene 328:103–111
Bomblies K, Dagenais N, Weigel D (1999) Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2. Dev Biol 216:260–264
Bortiri E, Hake S (2007) Flowering and determinacy in maize. J Exp Bot 58:909–916
Bowman JL, Smyth DR, Meyerwitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater MM, Colombo L (2007) Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19:2544–2556
Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587
Byrne ME, Groover AT, Fontana JR, Martienssen RA (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 130:3941–3950
Byzova MA, Fraken J, Aarts MG, de Almeida-Engler J, Engler G, Mariani C, Van Lookeren Campagne MM, Angenent GC (1999) Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower and ovule development. Genes Dev 13:1002–1014
Carraro N, Peaucelle A, Laufs P, Trass J (2006) Cell differentiation and organ initiation at the shoot apical meristem. Plant Mol Biol 60:811–826
Chae E, Tan QK, Hill TA, Irish VF (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135:1235–1245
Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025
Ciannamea S, Kaufmann K, Frau M, Nougalli Tonaco IA, Petersen K, Nielsen KK, Angenent GC, Immink RGH (2006) Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne. J Exp Bot 57:3419–3431
Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Coen ES, Romero JM, Doyle S, Murphy G, Carpenter R (1990) Floricula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322
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
de Folter S, Immink RG, Kieffer M, Paenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433
Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:935–1940
Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002
Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS, and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370–5379
Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979
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
Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560
Gregis V, Sessa A, Colombo L, Kater MM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18:1373–1382
Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of Arabidopsis floral homeotic gene APETALA1. Cell 76:131–143
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529
Huala E, Sussex IM (1992) LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4:901–913
Immink RG, Ferrario S, Busscher-Lange J, Kooiker M, Busscher M, Angenent GC (2003) Analysis of the Petunia MADS-box transcription factor family. Mol Genet Genom 268:598–606
Ingram GC, Goodrich J, Wilkinson MD, Simon R, Haughn GW, Coen ES (1995) Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7:1501–1510
Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16:S1–S17
Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and post-transcriptional regulation determine floral organ identity. Cell 6:703–716
Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225
Kanrar S, Onguka O, Smith HMS (2006) Arabidopsis inflorescence architecture requires the activities of KNOX–BELL homeodomain heterodimers. Planta 224:1163–1173
Kanrar S, Bhattacharya M, Arthur B, Courtier J, Smith HMS (2008) Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis. Plant J 54:924–937
Krizek BA, Meyerowitz EM (1996) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 112:11–22
Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12:1357–1366
Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, Hepworth SR, Haughn GH (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19:2719–2735
Lamb RS, Hill TA, Tan QK-G, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086
Lee I, Wolfe DS, Weigel D (1997) A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr Biol 7:95–104
Lenhard M, Bohnert A, Jurgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814
Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, Mao L (2008) Interaction study of MADS-domain proteins in tomato. J Exp Bot 59:2253–2265
Levin JZ, Meyerowitz EM (1995) UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7:529–548
Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11:1007–1018
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. Cell 2:135–142
Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis. Nature 379:66–69
Mandel MA, Gustafson-Brown C, Sabidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277
Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71:119–131
Mizukami Y, Ma H (1995) Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Mol Biol 28:767–784
Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW (1994) Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6:333–349
Pautot V, Dockx J, Hamant O, Kronenberger J, Grandjean O, Jublot D, Trass J (2001) KNAT2: evidence for a link between knotted-like genes and carpel development. Plant Cell 13:1719–1734
Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203
Pelaz S, Gustafson-Brown D, Kohalmi SE, Crosby WL, Yanofsky MF (2001a) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394
Pelaz S, Tapia-Lopex R, Alvarez-Buylla ER, Yanofsky MF (2001b) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184
Proveniers M, Rutjens B, Brand M, Smeekens S (2007) The Arabidopsis TALE homeobox gene ATH1 controls floral competency through positive regulation of FLC. Plant J 52:899–913
Ray A, Robinson-Beers K, Baker SC, Lang JD, Preuss D, Milligan SB, Gasser CS (1994) Arabidopsis floral homeotic gene BELL1 (BEL1) controls ovule development through negative regulation AGAMOUS gene (AG). Proc Natl Acad Sci USA 91:5761–5765
Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fischer RL (1995) The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83:735–742
Robinson-Beers K, Pruitt RE, Gasser CS (1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4:1237–1249
Roeder AH, Ferrandiz C, Yanofsky MF (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr Biol 13:1630–1635
Sablowski R (2007) Flowering and determinacy in Arabidopsis. J Exp Bot 58:899–907
Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL (1999) The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J 20:433–445
Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781
Scofield S, Dewitte W, Murray JA (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J 50:767–781
Sieburth LE, Running MP, Meyerwitz EM (1995) Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell 7:1249–1258
Smith HM, Hake S (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15:1717–1727
Smith HM, Campbell BC, Hake S (2004) Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH. Curr Biol 14:812–817
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Sridhar VV, Surendrarao A, Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133:3159–3166
Theissen G (2001) Development of floral organ identity: stones from the MADS house. Curr Opin Plant Biol 4:75–85
Theissen G, Saedler H (2001) Floral quartets. Nature 409:469–471
Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584
Weigel D, Meyerowitz EM (1993) Activation of floral homeotic genes in Arabidopsis. Science 261:1723–1726
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls flower meristem identity in Arabidopsis. Cell 69:843–859
Western TL, Haughn GW (1999) BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. Plant J 18:329–336
Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059
Wilkinson MD, Haughn GW (1995) UNUSUAL FLORAL ORGANS controls meristem identity and organ primordial fate in Arabidopsis. Plant Cell 7:1485–1499
William DA, Su Y, Smith MR, Lu M, Baldwin DA, Wagner D (2004) Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci USA 101:1775–1780
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
Zik M, Irish VI (2003) Flower development: initiation, differentiation and diversification. Annu Rev Cell Dev 19:119–140
Acknowledgments
We thank Dr. Xuemei Chen for the pCIT565 and pD793 plamids, Dr. Jeff Long for the pDW22.1 plasmid, and Dr. G. Venugopala Reddy for the pBSWUS plasmid. We also thank Drs. Patricia Springer, Xuemei Chen and Susan Byrd for critical reading of this manuscript. We are thankful to the anonymous reviewers for their helpful comments. We are grateful to Dr. Patricia Springer for microscopy help for the in situ images and Dr. David Carter at the Genome Core Facility for help with the SEM. This research was supported by the National Science Foundation grant number IOB-0615774.
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Yu, L., Patibanda, V. & Smith, H.M.S. A novel role of BELL1-like homeobox genes, PENNYWISE and POUND-FOOLISH, in floral patterning. Planta 229, 693–707 (2009). https://doi.org/10.1007/s00425-008-0867-1
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DOI: https://doi.org/10.1007/s00425-008-0867-1