2 Gynoecium Patterning in Arabidopsis: A Basic Plan Behind a Complex Structure
Eva Sundberg
Department of Plant Biology and Forest Genetics, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
Search for more papers by this authorCristina Ferrándiz
Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC), Campus de la Universidad Politécnica de Valencia, Avda de los Naranjos s/n, Valencia, Spain
Search for more papers by this authorEva Sundberg
Department of Plant Biology and Forest Genetics, Uppsala BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
Search for more papers by this authorCristina Ferrándiz
Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC), Campus de la Universidad Politécnica de Valencia, Avda de los Naranjos s/n, Valencia, Spain
Search for more papers by this authorAbstract
The Arabidopsis gynoecium consists of two congenitally fused carpels that, at maturity, form a bilocular chamber protecting the ovules and placentae produced by the meristematic regions of the carpel margins. This meristematic region also gives rise to a style capped with stigmatic papillae at the apical end of the developing gynoecia and a transmitting tract that connects the stigma to the ovule-bearing chambers. Most data point towards a common evolutionary origin of leaves and carpels and suggest that leaves can be transformed to carpels by expressing only a few carpel identity genes. In this review, we have therefore approached the carpels from the leaf-like organ hidden within by stressing the parallels between leaf and carpel development. Many of the genes with a role in leaf development were first identified by the effect their mutations cause in carpel development, suggesting that the regulatory networks may be more robust in leaves than in the more complex and evolutionary younger carpels. Similar genetic networks ensure the maintenance of adaxial–abaxial, proximal–distal and medial–lateral dichotomies in leaves and carpels. Data have emerged showing that crosstalk and redundancies are characteristics of these pathways, as well as a general interplay of hormonal balances, with auxin as a major morphogen.
References
- Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouché, N., Gasciolli, V. andVaucheret, H.(2006)DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7.Current Biology 16, 927–932.
- Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. andTasaka, M.(1997)Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.The Plant Cell 9, 841–857.
- Aida, M. andTasaka, M.(2006)Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex.Plant Molecular Biology 60, 915–928.
- Aloni, R., Schwalm, K., Langhans, M. andUllrich, C.I.(2003)Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis .Planta 216, 841–853.
- Alonso-Cantabrana, H., Ripoll, J.J., Ochando, I., Vera, A., Ferrándiz, C. andMartínez-Laborda, A.(2007)Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene.Development 134, 2663–2671.
- Alvarez, J. andSmyth, D.R.(1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS .Development 126, 2377–2386.
- Alvarez, J. andSmyth, D.R.(2002) CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana.International Journal of Plant Sciences 163, 17–41.
- Alvarez, J.P., Goldshmidt, A., Efroni, I., Bowman, J.L. andEshed Y.(2009)The NGATHA distal organ development genes are essential for style specification in Arabidopsis.Plant Cell 21, 1373–1393.
- Alvarez, J.P., Pekker, I., Goldshmidt, A., Blum, E., Amsellem, Z. andEshed, Y.(2006)Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species.The Plant Cell 18, 1134–1151.
- Anastasiou, E. andLenhard, M.(2007)Growing up to one's standard.Current Opinion in Plant Biology 10, 63–69.
- Avsian-Kretchmer, O., Cheng, J.C., Chen, L., Moctezuma, E. andSung, Z.R.(2002)Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny.Plant Physiology 130, 199–209.
- Azhakanandam, S., Nole-Wilson, S., Bao, F. andFranks, R.G.(2008) SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development.Plant Physiology 146, 1165–1181.
- Balanzá, V., Navarrete, M., Trigueros, M. andFerrándiz, C.(2006)Patterning the female side of Arabidopsis: the importance of hormones.Journal of Experimental Botany 57, 3457–3469.
- Bao, N., Lye, K.-W. andBarton, M.K.(2004a)MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome.Developmental Cell 7, 653–662.
- Bao, X., Franks, R.G., Levin, J.Z. andLiu, Z.(2004b)Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems.The Plant Cell 16, 1478–1489.
- Barkoulas, M., Galinha, C., Grigg, S.P. andTsiantis, M.(2007)From genes to shape: regulatory interactions in leaf development.Current Opinion in Plant Biology 10, 660–666.
- Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G. andFriml, J.(2003)Local, efflux-dependent auxin gradients as a common module for plant organ formation.Cell 115, 591–602.
- Bennett, S.R.M., Alvarez, J., Bossinger, G. andSmyth, D.R.(1995)Morphogenesis in pinoid mutants of Arabidopsis thaliana .Plant Journal 8, 505–520.
- Bhatt, A.M., Etchells, J.P., Canales, C., Lagodienko, A. andDickinson, 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.
- Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M. andBenning, C.(1998)AGO1 defines a novel locus of Arabidopsis controlling leaf development.EMBO Journal 17, 170–180.
- Borghi, L., Bureau, M. andSimon, R.(2007)Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity.The Plant Cell 19, 1795–1808.
- Bowman, J., Baum, S., Eshed, Y., Putterill, J. andAlvarez, J.(1999)Molecular genetics of gynoecium development in Arabidopsis.Current Topics in Developmental Biology 45, 155–205.
- Bowman, J. andSmyth, D.(1999)CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains.Development 126, 2387–2396.
- Bowman, J.L., Smyth, D.R. andMeyerowitz, E.M.(1991)Genetic interactions among floral homeotic genes of Arabidopsis .Development 112, 1–20.
- Byrne, M.E.(2005)Networks in leaf development.Current Opinion in Plant Biology 8, 59–66.
- Byrne, M.E.(2006)Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes.PLoS Genetics 2, 785–789.
- Byrne, M.E., Groover, A.T., Fontana, J.R. andMartienssen, R.A.(2003)Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER.Development 130, 3941–3950.
- Castillejo, C., Romera-Branchat, M. andPelaz, S.(2005)A new role of the Arabidopsis SEPALLATA3 gene revealed by its constitutive expression.Plant Journal 43, 586–596.
-
Chen, C., Wang, S. andHuang, H.(2000)
LEUNIG has multiple functions in gynoecium development in Arabidopsis
.Genesis
26, 42–54.
10.1002/(SICI)1526-968X(200001)26:1<42::AID-GENE7>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- Chen, C., Xu, Y., Zeng, M. andHuang, H.(2001)Genetic control by Arabidopsis genes LEUNIG and FILAMENTOUS FLOWER in gynoecium fusion.Journal of Plant Research 114, 465–469.
- Chen, H., Banerjee, A.K. andHannapel, D.J.(2004)The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1 .Plant Journal 38, 276–284.
- Cheng, Y., Dai, X. andZhao, Y.(2006)Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.Genes and Development 20, 1790–1799.
- Cheng, Y., Dai, X. andZhao, Y.(2007)Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis.The Plant Cell 19, 2430–2439.
- Cheng, Y., Kato, N., Wang, W., Li, J. andChen, X.(2003)Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana.Developmental Cell 4, 53–66.
- Chitwood, D.H., Guo, M., Nogueira, F.T.S. andTimmermans, M.C.P.(2007)Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex.Development 134, 813–823.
- Cnops, G., Jover-Gil, S., Peters, J.L., Neyt, P., De Block, S., Robles, P., Ponce, M.R., Gerats, T., Micol, J.L. andvan Lijsebettens, M.(2004)The rotunda2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis.Journal of Experimental Botany 55, 1529–1539.
- Coen, E.S. andMeyerowitz, E.M.(1991)The war of the whorls: genetic interactions controlling flower development.Nature 353, 31–37.
- Conner, J. andLiu, Z.(2000) LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proceedings of the National Academy of Sciences of the United States of America 97, 12902–12907.
- Crawford, B.C.W., Ditta, G. andYanofsky, M.F.(2007)The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana .Current Biology 17, 1101–1108.
- Dewitte, W., Scofield, S., Alcasabas, A.A., Maughan, S.C., Menges, M., Braun, N., Collins, C., Nieuwland, J., Prinsen, E., Sundaresan, V. andMurray, J.A.H.(2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proceedings of the National Academy of Sciences of the United States of America 104, 14537–14542.
- Dinneny, J.R., Weigel, D. andYanofsky, M.F.(2005)A genetic framework for fruit patterning in Arabidopsis thaliana.Development 132, 4687–4696.
- Dinneny, J.R., Weigel, D. andYanofsky, M.F.(2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis .Development 133, 1645–1655.
- Dinneny, J.R., Yadegari, R., Fischer, R.L., Yanofsky, M.F. andWeigel, D.(2004)The role of JAGGED in shaping lateral organs.Development 131, 1101–1110.
- Dinneny, J.R. andYanofsky, M.F.(2005)Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned.BioEssays 27, 42–46.
- Ditta, G., Pinyopich, A., Robles, P., Pelaz, S. andYanofsky, M.F.(2004)The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity.Current Biology 14, 1935–1940.
- Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E. andDengler, N.G.(1999)Cell cycling and cell enlargement in developing leaves of Arabidopsis .Developmental Biology 215, 407–419.
- Efroni, I., Blum, E., Goldschmidt, A. andEshed, Y.(2008)A protracted and dynamic maturation schedule underlies Arabidopsis leaf development.The Plant Cell 20, 2293–2306.
- Ehsan, H., Reichheld, J.-P., Durfee, T. andRoe, J.L.(2004)TOUSLED kinase activity oscillates during the cell cycle and interacts with chromatin regulators.Plant Physiology 134, 1488–1499.
- Eklund, D.M., Ståldal, V., Hiratsu, K., Ohme-Takagi, M., Ezcurra, I. andSundberg, E.(2008) The Arabidopsis STYLISH1 protein acts as a transcriptional activator regulating local auxin biosynthesis. Submitted.
- Elliot, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q.J., Gerentes, D., Perez, P. andSmyth, D.R.(1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth.The Plant Cell 8, 155–168.
- Emery, J.F., Floyd, S.K., Alvarez, J., Eshed, Y., Hawker, N.P., Izhaki, A., Baum, S.F. andBowman, J.L.(2003)Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.Current Biology 13, 1768–1774.
- Endrizzi, K., Moussain, B., Haecker, A., Levin, J.Z. andLaux, T.(1996)The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulator level than the meristem genes WUSCHEL and ZWILLE .Plant Journal 10, 967–979.
- Eshed, Y., Baum, S. andBowman, J.(1999)Distinct mechanisms promote polarity establishment in carpels of Arabidopsis.Cell 99, 199–209.
- Eshed, Y., Baum, S.F., Perea, J.V. andBowman, J.L.(2001)Establishment of polarity in lateral organs of plants.Current Biology 11, 1251–1260.
- Eshed, Y., Izhaki, A., Baum, S.F., Floyd, S.K. andBowman, J.L.(2004)Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities.Development 131, 2997–3006.
- Fahlgren, N., Montgomery, T.A., Howell, M.D., Allen, E., Dvorak, S.K., Alexander, A.L. andCarrington, J.C.(2006)Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis.Current Biology 16, 939–944.
- Ferrándiz, C.(2002)Regulation of fruit dehiscence in Arabidopsis.Journal of Experimental Botany 53, 2031–2038.
- Ferrándiz, C., Gu, Q., Martienssen, R. andYanofsky, M.F.(2000)Negative regulation of SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development.Science 289, 436–438.
- Fleming, A.J.(2005)The control of leaf development.New Phytologist 166, 9–20.
- Franks, R.G., Liu, Z. andFischer, R.L.(2006) SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals.Planta 224, 801–811.
- Franks, R.G., Wang, C., Levin, J.Z. andLiu, Z.(2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG .Development 129, 253–263.
- Fridborg, I., Kuusk, S., Moritz, T. andSundberg, E.(1999)The Arabidopsis dwarf mutant shi exhibitis reduced gibberellin responses conferred by overexpression of a new zinc finger protein.The Plant Cell 11, 1019–1032.
- Fridborg, I., Kuusk, S., Robertson, M. andSundberg, E.(2001)The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley.Plant Physiology 127, 937–948.
- Fu, Y., Xu, L., Xu, B., Yang, L., Ling, Q., Wang, H. andHuang, H.(2007)Genetic interactions between leaf polarity-controlling genes and ASYMMERIC LEAVES1 and 2 in Arabidopsis leaf patterning.Plant and Cell Physiology 48, 724–735.
- Garcia, D., Collier, S.A., Byrne, M.E. andMartienssen, R.A.(2006)Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway.Current Biology 16, 933–938.
-
Goethe, J.W.V.(1790) Versuch die Metamorphose der Pflanzen zu Erklaren. C.W. Ettinger,Gotha,Germany.
10.5962/bhl.title.127448 Google Scholar
- Golz, J.F.(2006)Signalling between the shoot apical meristem and developing lateral organs.Plant Molecular Biology 60, 889–903.
- Gómez-Mena, C., de Folter, S., Costa, M.M., Angenent, G.C. andSablowski, R.(2005)Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis.Development 132, 429–438.
- Gonzales, D., Bowen, A.J., Carroll, T.S. andConlan, R.S.(2007)The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription.Molecular and Cellular Biology 27, 5306–5315.
- Gremski, K., Ditta, G. andYanofsky, M.F.(2007)The HECATE genes regulate female reproductive tract development in Arabdiopsis thaliana .Development 134, 3593–3601.
- Groszmann, M., Paicu, T. andSmyth, D.R.(2008)Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis .Plant Journal, 55 (1), 40–52.
- Gu, Q., Ferrándiz, C., Yanofsky, M.F. andMartienssen, R.(1998)The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development.Development 125, 1509–1517.
- Guo, M., Thomas, J., Collins, G. andTimmermanns, M.C.P.(2008)Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis .The Plant Cell 20, 48–58.
- Ha, C.M., Jun, J.H., Nam, H.G. andFletcher, J.(2004) BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana .Plant and Cell Physiology 45, 1361–1370.
- Ha, C.M., Jun, J.H., Nam, H.G. andFletcher, J.(2007) BLADE-ON-PETIOLE1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes.The Plant Cell 19, 1809–1825.
- Ha, C.M., Kim, G.-T., Kim, B.C., Jun, J.H., Soh, M.S., Ueno, Y., Macida, Y., Tsukaya, H. andNam, H.G.(2003)The BLADE-ON-PETIOLE1 gene controls leaf pattern formation through the modulation of meristem activity in Arabidopsis .Development 130, 161–172.
- Hake, S., Smith, H.M., Holtan, H., Magnani, E., Mele, G. andRamirez, J.(2004)The role of knox genes in plant development.Annual Review of Cell and Developmental Biology 20, 125–151.
- Hay, A., Barkoulas, M. andTsiantis, M.(2006)ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis.Development 133, 3955–3961.
- Hay, A., Kaur, H., Phillips, A., Hedden, P., Hake, S. andTsiantis, M.(2002)The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans.Current Biology 12, 1557–1565.
- Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A. andMeyerowitz, E.M.(2005)Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.Current Biology 15, 1899–1911.
- Heisler, M.G.B., Atkinson, A., Bylstra, Y.H., Walsh, R. andSmyth, D.R.(2001) SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein.Development 128, 1089–1098.
- Hepworth, S.R., Zhang, Y., McKim, S., Li, X. andHaughn, G.W.(2005)BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis.The Plant Cell 17, 1434–1448.
- Hibara, K., Karim, M.R., Takada, S., Taoka, K., Furutani, M., Aida, M. andTasaka, M.(2006)Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation.The Plant Cell 18, 2946–2957.
-
Hill, J.P. andLord, E.M.(1989)Floral development in Arabidopsis thaliana: a comparison of the wild type and the homeotic pistillata mutant.Canadian Journal of Botany
67, 1010–1019.
10.1139/b89-375 Google Scholar
- Honma, T. andGoto, K.(2001)Complexes of MADS-box proteins are sufficient to convert leaves into floral organs.Nature 409, 525–529.
- Horiguchi, G., Kim, G.T. andTsukaya, H.(2005)The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana .Plant Journal 43, 68–78.
- Hu, Y., Xie, Q. andChua, N.H.(2003)The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size.The Plant Cell 15, 1951–1961.
- Hunter, C., Willmann, M.R., Wu, G., Yoshikawa, M., de la Luz Gutiérrez-Nava, M. andPoethig, R.S.(2006)Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis .Development 133, 2973–2981.
- Ingram, G.C. andWaites, R.(2006)Keeping it together: co-ordinating plant growth.Current Opinion in Plant Biology 9, 12–20.
- Ishida, T., Aida, M., Takada, S. andTasaka, M.(2000)Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana.Plant and Cell Physiology 41, 60–67.
- Izhaki, A. andBoman, J.L.(2007)KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis .The Plant Cell 19, 495–508.
- Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P. andTsiantis, M.(2005)KNOX action in Arabidopsis is mediated by co-ordinate regulation of cytokinin and gibberellin activities.Current Biology 15, 1560–1565.
- Kepinski, S.(2006)Integrating hormone signaling and patterning mechanisms in plant development.Current Opinion in Plant Biology 9, 28–34.
- Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K. andPoethig, R.S.(2001) KANADI regulates organ polarity in Arabidopsis .Nature 411, 706–709.
- Kidner, C.A. andMartienssen, R.A.(2003)Spatially restricted microRNA directs leaf polarity through ARGONAUTE1.Nature 428, 81–84.
- Kidner, C.A. andTimmermans, M.C.P.(2007)Mixing and matching pathways in leaf polarity.Current Opinion in Plant Biology 10, 13–20.
- Krizek, B.A.(2003)AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain.Nucleic Acids Research 31, 1859–1868.
- Krizek, B.A. andFletcher, J.C.(2005)Molecular mechanisms of flower development: an armchair guide.Nature Reviews Genetics 6, 688–698.
- Krizek, B.A., Prost, V. andMacais, A.(2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS .The Plant Cell 12, 1357–1366.
- Krizek, B.A. andSulli, C.(2006)Mapping sequences required for nuclear localization and the transcriptional activation function of the Arabidopsis protein AINTEGUMENTA.Planta 224, 612–621.
- Kumaran, M.K., Bowman, J.L. andSundaresan, V.(2002)YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis.The Plant Cell 14, 2761–2770.
- Kuusk, S., Sohlberg, J.J., Eklund, D.M. andSundberg, E.(2006)Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner.Plant Journal 47, 99–111.
- Kuusk, S., Sohlberg, J.J., Long, J.A., Fridborg, I. andSundberg, E.(2002)STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development.Development 129, 4707–4717.
- Laux, T., Mayer, K.F., Berger, J. andJürgens, G.(1996)The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis.Development 122, 87–96.
- Lenhard, M., Bohnert, A., Jurgens, G. andLaux, T.(2001)Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS.Cell 105, 805–814.
- Li, C., Potuschak, T., Colón-Carmona, A., Gutiérrez, R.A. andDoerner, P.(2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proceedings of the National Academy of Sciences of the United States of America 102, 12978–12983.
- Liljegren, S., Ditta, G., Eshed, Y., Savidge, B., Bowman, J. andYanofsky, M.(2000)SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis.Nature 404, 766–769.
- Liljegren, S.J., Roeder, A.H., Kempin, S.A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D.K. andYanofsky, M.F.(2004)Control of fruit patterning in Arabidopsis by INDEHISCENT.Cell 116, 843–853.
- Lin, W.C., Shuai, B. andSpringer, P.S.(2003)The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaial patterning.The Plant Cell 15, 2241–2252.
- Liu, Z., Franks, R. andKlink, V.P.(2000)Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA .The Plant Cell 12, 1879–1891.
- Liu, Z. andMeyerowitz, E.M.(1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers.Development 121, 975–991.
- Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R. andWeigel, D.(2001)A molecular link between stem cell regulation and floral patterning in Arabidopsis.Cell 105, 793–803.
- Long, J.A., Moan, E.I., Medford, J.I. andBarton, M.K.(1996)A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis .Nature 379, 66–69.
- Mallory, A.C., Reinhart, B.J., Jones-Rhoades, M.W., Tang, G., Zamore, P.D., Barton, M.K. andBartel, D.P.(2004)MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region.The EMBO Journal 23, 3356–3364.
- Mandel, M.A. andYanofsky, M.F.(1997)The Arabidopsis AGL9 MADS-box gene is expressed in young flower primordia.Sexual Plant Reproduction 11, 22–28.
- Mattsson, J. Sung, Z.R. andBerleth, T.(1999)Responses to plant vescular systems to auxin transport inhibition.Development 126, 2979–2991.
- McConnell, J.R. andBarton, M.K.(1998)Leaf polarity and meristem formation in Arabidopsis .Development 125, 2935–2942.
- McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J. andBarton, M.K.(2001)Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots.Nature 411, 709–713.
- Misukami, Y. andFischer, R.L.(2000)Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proceedings of the National Academy of Sciences of the United States of America 97, 942–947.
- Nath, U., Crawford, B.C.W., Carpenter, R. andCoen, E.(2003)Genetic control of surface curvature.Science 299, 1404–1407.
- Navarro, C., Efremova, N., Golz, J.F., Rubiera, R., Kuckenberg, M., Castillo, R., Tietz, O., Saedler, H. andSchwarz-Sommer, Z.(2004)Molecular and genetic interactions between STYLOSA and GRAMIONIFOLIA in the control of Antirrhinum vegetative and reproductive development.Development 131, 3649–3659.
- Nemhauser, J.L., Feldman, L.J. andZambryski, P.C.(2000)Auxin and ETTIN in Arabidopsis gynoecium morphogenesis.Development 127, 3877–3888.
- Nikovics, K., Blein, T., Peaucelle, A., Ishida, T., Morin, H., Aida, M. andLaufs, P.(2006)The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis .The Plant Cell 18, 2929–2945.
- Nogueria, F.T.S., Madi, S., Chitwood, D.H., Juarez, M.T. andTimmermans, M.C.P.(2007)Two small regulatory RNAs establish opposing fates of a developmental axis.Genes and Development 21, 750–755.
- Nole-Wilson, S. andKrizek, B.A.(2006) AINTEGUMENTA contributes to organ polarity and regulated growth of lateral organs in combination with YABBY genes.Plant Physiology 141, 977–987.
- Nole-Wilson, S., Tranby, T.L. andKrizek, B.A.(2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states.Plant Molecular Biology 57, 613–628.
- Norberg, M., Holmlund, M. andNilsson, O.(2005)The BLADE-ON-PETIOLE genes act redundantly to control the growth and development of lateral organs.Development 132, 2203–2213.
- Ohno, C.K., Reddy, G.V., Heisler, M.B. andMeyerowitz, E.M.(2004)The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development.Development 131, 1111–1122.
- Okada, K., Ueda, J., Komaki, M.K., Bell, C.J. andShimura, Y.(1991)Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation.The Plant Cell 3, 677–684.
- Ori, N., Cohen, A.R., Etzioni, A., Brand, A., Yani, O., Shliezer, S., Menda, N., Amsellem, Z., Efroni, I., Pekker, I., Alvarez, J.P., Blum, E., Zamir, D. andEshed, Y.(2007)Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato.Nature Genetics 39, 787–791.
- Ori, N., Eshed, Y., Chuck, G., Bowman, J.L. andHake, S.(2000)Mechanisms that control knox gene expression in the Arabidopsis shoot.Development 127, 5523–5532.
- Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C. andWeigel, D.(2003)Control of leaf morphogenesis by microRNAs.Nature 425, 257–263.
- Pautot, V., Dockx, J., Hamant, O., Kronenberger, J., Grandjean, O., Jublot, D. andTraas, J.(2001) KNAT2: evidence for a link between knotted-like genes and carpel development.The Plant Cell 13, 1719–1734.
- Payne, T., Johnson, S.D. andKoltunow, A.M.(2004)KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates the Arabidopsis gynoecium.Development 131, 3737–3749.
- Pekker, I., Alvarez, J.P. andEshed, Y.(2005)Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity.The Plant Cell 17, 2899–2910.
- Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E.R. andYanofsky, M.F.(2001)Conversion of leaves into petals in Arabidopsis .Current Biology 15, 1998–2006.
- Penfield, S., Josse, E.M., Kannangara, R., Gilday, A.D., Halliday, K.J. andGraham, I.A.(2005)Cold and light control seed germination through the bHLH transcription factor SPATULA.Current Biology 15, 1998–2006.
- Pfluger, J. andZambryski, P.(2004)The role of SEUSS in auxin response and floral organ patterning.Development 131, 4697–4707.
- Phelps-Durr, T.L., Thomas, J., Vahab, P. andTimmermans, M.C.(2005)Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis.The Plant Cell 17, 2886–2898.
- Piazza, P., Jasinski, S. andTsiantis, M.(2005)Evolution of leaf developmental mechanisms.New Phytologist 167, 693–710.
- Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E. andYanofsky, M.F.(2003)Assessing the redundancy of MADS-box genes during carpel and ovule development.Nature 424, 85–88.
- Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N. andClark, S.E.(2005)Class III homeodomain-leucin zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development.The Plant Cell 17, 61–67.
- Przemeck, G.K.H., Mattsson, J., Hardtke, C.S., Sung, Z.R. andBerleth, T.(1996)Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization.Planta 200, 229–237.
- Ragni, L., Belles-Boix, E., Günl, M. andPautot, V.(2008)Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis Inflorescences.The Plant Cell 20, 888–900.
- Rajani, S. andSundaresan, V.(2001)The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence.Current Biology 11, 1914–1922.
- Reinhardt, D., Frenz, M., Mandel, T. andKulemeier, C.(2005)Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato.Development 132, 15–26.
- Reinhardt, D., Mandel, T. andKuhlemeier, C.(2000)Auxin regulates the initiation and radial position of plant lateral organs.The Plant Cell 12, 507–518.
- Reinhardt, D., Pesce, E.-R., Steiger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. andKuhlemeier, C.(2003)Regulation of phyllotaxis by polar auxin transport.Nature 426, 255–260.
- Riou-Khamlichi, C., Huntley, R., Jacqmard, A. andMurray, J.A.H.(1999)Cytokinin activation of Arabidopsis cell division through a D-type cyclin.Science 283, 1541–1544.
- Roe, J.L., Nemhauser, J.L. andZambryski, P.C.(1997) TOUSLED participates in apical tissue formation during gynoecium development in Arabidopsis.The Plant Cell 9, 335–353.
- Roe, J.L., Rivin, C.J., Sessions, R.A., Feldmann, K.A. andZambryski, P.C.(1993)The Tousled gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development.Cell 75, 939–950.
- Roeder, A.H., Ferrándiz, C. andYanofsky, M.F.(2003)The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit.Current Biology 13, 1630–1635.
- Roeder, A.H.K. andYanofsky, M.F.(2005)Fruit development in Arabidopsis .The Arabidopsis Book 52, 1–50.
- Savidge, B., Rounsley, S.D. andYanofsky, M.F.(1995)Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes.The Plant Cell 7, 721–733.
- Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Morita, E.H. andOkada, K.(1999)FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains.Genes and Development 13, 1079–1088.
- Sawchuk, M.G., Head, P., Donnery, T.J. andScarpella, E.(2007)Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation.New Phytologist 176, 560–571.
- Scofield, S., Dewitte, W. andMurray, J.A.H.(2007)The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis.Plant Journal 50, 767–781.
- Scutt, C.P., Vinauger-Douard, M., Fourquin, C., Finet, C. andDumas, C.(2006)An evolutionary perspective on the regulation of carpel development.Journal of Experimental Botany 57, 2143–2152.
- Sessions, A., Nemhauser, J., McCall, A., Roe, J.L., Feldmann, K.A. andZambryski, P.C.(1997) ETTIN patterns the Arabidopsis floral meristem and reproductive organs.Development 124, 4481–4491.
- Sessions, R.A. andZambryski, P.C.(1995) Arabidopsis gynoecium structure in the wild type and in ettin mutants.Development 121, 1519–1532.
- Shani, E., Yanai, O. andOri, N.(2006)The role of hormones in shoot apical meristem function.Current Opinion in Plant Biology 9, 484–489.
- Sieber, P., Wellmer, F., Gheyselinck, J., Riechmann, J.L. andMeyerowitz, E.M.(2007)Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness.Development 134, 1051–1060.
- Sieburth, L.E. andMeyerowitz, E.M.(1997)Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically.The Plant Cell 9, 355–365.
- Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N. andBowman, J.L.(1999)Members of the YABBY gene family specify abaxial cell fate in Arabidopsis.Development 126, 4117–4128.
- Sitaraman, J., Bui, M. andLiu, Z.(2008) LEUNIG-HOMOLOG and LEUNIG perform partially redundant functions during Arabidopsis embryo and floral development.Plant Physiology 147, 672–681.
- Smith, H.M.S. andHake, S.(2003)The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis Inflorescence.The Plant Cell 15, 1717–1727.
- Smyth, D.R., Bowman, J.L. andMeyerowitz, E.M.(1990)Early flower development in Arabidopsis .The Plant Cell 2, 755–767.
- Sohlberg, J.J., Myrenås, M., Kuusk, S., Lagercrantz, U., Kowalczyk, M., Sandberg, G. andSundberg, E.(2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium.Plant Journal 47, 112–123.
- Sorefan, K., Girin, T., Liljegren, S.J., Ljung, K., Robles, P., Galván-Ampudia, C.S., Offringa, R., Friml, J., Yanofsky, M.F. andØstergaard, L.(2009)A regulated auxin minimum is required for seed dispersal in Arabidopsis .Nature 459, 583–586.
- Sridhar, V.V., Surendrarao, A., Gonzales, D., Conlan, R.S. andLiu, Z.(2004)Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development.Proceedings of the National Academy of Sciences of the United States of America 101, 11494–11499.
- Ståldal, V., Sohlberg, J.J., Eklund, D.M., Ljung, K. andSundberg, E.(2008)Auxin can act independently of CRC, LUG, SEU, SPT and STY1 in style development, but not in apical-basal patterning of the Arabidopsis gynoecium.New Phytologist 180, 798–808.
- Sussex, I.M.(1954)Morphogenesis in Solanum tuberosum L: experimental investigation of leaf dorsiventrality and orientation in the juvenile shoot.Phytomorphology 5, 286–300.
- Takada, S., Hibara, K., Ishida, T. andTasaka, M.(2001)The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation.Development 128, 1127–1135.
- Tang, G., Reinhart, B.J., Bartel, D.P. andZamore, P.D.(2003)A biochemical framework for RNA silencing in plants.Genes and Development 17, 49–63.
- Theissen, G. andMelzer, R.(2007)Molecular mechanisms underlying origin and diversification of the angiosperm flower.Annals of Botany 100, 603–619.
- Tretter, E.M., Alvarez, J.P., Eshed, Y. andBowman, J.L.(2008)Activity range of Arabidopsis small RNAs derived from different biogenesis pathways.Plant Physiology 147, 58–62.
- Trigueros, M., Navarrete-Gómez, M., Sato, S., Christensen, S.K., Pelaz, S., Weigel, D., Yanofsky, M.F. andFerrándiz, C.(2009)The NGATHA genes direct style development in the Arabidopsis gynoecium.Plant Cell 21, 1394–1409.
- Tsukaya, H.(2003)Organ shape and size: a lesson from studying leaf morphogenesis.Current Opinion in Plant Biology 6, 57–62.
- Tsukaya, H.(2006)Mechanism of leaf shape determination.Annual Reviews of Plant Biology 57, 477–496.
- Van Der Graaff, E.,Den Dulk-Ras, A., Hooykaas, P.J.J. andKeller, B.(2000)Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana .Development 127, 4971–4980.
- Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.-L., Bartel, D.P. andCrété, P.(2004)Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs.Molecular Cell 16, 69–79.
- Venglat, S.P., Dumonceaux, T., Rozwadowski, K., Parnell, L., Babic, V., Keller, W., Martienssen, R., Selvaraj, G. andDatla, R.(2002)The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 99, 4730–4735.
- Vroemen, C.W., Mordhorst, A.P., Albrecht, C., Kwaaitaal, M.A.C.J. andde Vries, S.C.(2003)The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis.The Plant Cell 15, 1563–1577.
- Wang, Y., Liu, J., Xia, R., Wang, J., Shen, J., Cao, R., Hong, X., Zhu, J.-K. andGong, Z.(2007)The protein kinase TOUSLED is required for maintenance of transcriptional gene silencing in Arabidopsis .EMBO reports 8, 77–83.
- Weigel, D., Hoon Ahn, J., Blázquez, M.A., Borevitz, J.O., Christensen, S.K., Frankhauser, C., Ferrándiz, C., Kardailsky, I., Malancharuvil, E.J., Neff, M.M., Nguyen, J.T., Sato, S., Wang, Z.Y., Xia, Y., Dixon, R.A., Harrison, M.J., Lamb, C.J., Yanofsky, M.F. andChory, J.(2000)Activation tagging in Arabidopsis.Plant Physiology 122, 1003–1013.
- Weigel, D. andMeyerowitz, E.M.(1993)Activation of floral homeotic genes in Arabidopsis.Science 261, 1723–1726.
- White, D.W.R(2006) PEAPOD regulates lamina size and curvature in Arabidopsis.Proceedings of the National Academy of Sciences of the United States of America 103, 13238–13243.
- Williams, L., Carles, C.C., Osmont, K.S. andFletcher, J.C.(2005a)A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes.Proceedings of the National Academy of Sciences of the United States of America 102, 9703–9708.
- Williams, L., Grigg, S.P., Xie, M., Christensen, S. andFletcher, J.C.(2005b)Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes.Development 132, 3657–3668.
- Wu, M.F., Tian, Q. andReed, J.W.(2006)Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction.Development 133, 4211–4218.
- Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Xu, Y. andHuang, H.(2003)Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity.Development 130, 4097–4107.
- Xu, L., Yang, L. andHuang, H.(2007)Transcriptional, post-transcriptional and post-translational regulations of gene expression during leaf polarity formation.Cell Research 17, 512–519.
- Yamaguchi, T., Nagasawa, N., Kawasaki, S., Matsuoka, M., Nagato, Y. andHirano, H.Y.(2004)The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa.The Plant Cell 16, 500–509.
- Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A. andOri, N.(2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis.Current Biology 15, 1566–1571.
- Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A. andMeyerowitz, E.M.(1990)The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors.Nature 346, 35–39.
- Zgurski, J.M., Sharma, R., Bolokoski, D.A. andSchultz, E.A.(2005)Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves.The Plant Cell 17, 77–91.
- Zhong, R. andYe, 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 and Cell Physiology 45, 369–385.
- Zhou, G.-K., Kubo, M., Zhong, R., Demura, T andYe, Z.-H.(2007)Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis .Plant and Cell Physiology 48, 391–404.
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