Gibberellins negatively modulate ovule number in plants

[EN] Ovule formation is a complex developmental process in plants, with a strong impact on the production of seeds. Ovule primordia initiation is controlled by a gene network, including components of the signaling pathways of auxin, brassinosteroids and cytokinins. By contrast, gibberellins (GAs) and DELLA proteins, the negative regulators of GA signaling, have never been shown to be involved in ovule initiation. Here, we provide molecular and genetic evidence that points to DELLA proteins as novel players in the determination of ovule number in Arabidopsis and in species of agronomic interest, such as tomato and rapeseed, adding a new layer of complexity to this important developmental process. DELLA activity correlates positively with ovule number, acting as a positive factor for ovule initiation. In addition, ectopic expression of a dominant DELLA in the placenta is sufficient to increase ovule number. The role of DELLA proteins in ovule number does not appear to be related to auxin transport or signaling in the ovule primordia. Possible crosstalk between DELLA proteins and the molecular and hormonal network controlling ovule initiation is also discussed.This work was supported by grants from the Ministerio de Economia y Competitividad and the European Regional Development Fund (BIO2014-55946) and Generalitat Valenciana (ACOMP/2014/106) to M.A.P.-A, from the National Science Foundation (MCB-0923727) to J.M.A., and from the National Institutes of Health (R01GM112976-01A1) and the Saltman Endowed Chair in Science and Education to M.F.Y. Deposited in PMC for release after 12 months.Gómez Jiménez, MD.; Barro-Trastoy, D.; Escoms, E.; Saura-Sanchez, M.; Sanchez, I.; Briones-Moreno, A.; Vera Sirera, FJ.... (2018). Gibberellins negatively modulate ovule number in plants. Development. 145(13). https://doi.org/10.1242/dev.163865S14513Anders, S., & Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biology, 11(10). doi:10.1186/gb-2010-11-10-r106Bai, M.-Y., Shang, J.-X., Oh, E., Fan, M., Bai, Y., Zentella, R., … Wang, Z.-Y. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biology, 14(8), 810-817. doi:10.1038/ncb2546Balanzà, V., Martínez-Fernández, I., Sato, S., Yanofsky, M. F., Kaufmann, K., Angenent, G. C., … Ferrándiz, C. (2018). Genetic control of meristem arrest and life span in Arabidopsis by a FRUITFULL-APETALA2 pathway. Nature Communications, 9(1). doi:10.1038/s41467-018-03067-5Bartrina, I., Otto, E., Strnad, M., Werner, T., & Schmülling, T. (2011). Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana. The Plant Cell, 23(1), 69-80. doi:10.1105/tpc.110.079079Bencivenga, S., Simonini, S., Benková, E., & Colombo, L. (2012). The Transcription Factors BEL1 and SPL Are Required for Cytokinin and Auxin Signaling During Ovule Development in Arabidopsis. The Plant Cell, 24(7), 2886-2897. doi:10.1105/tpc.112.100164Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., & Friml, J. (2003). Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation. Cell, 115(5), 591-602. doi:10.1016/s0092-8674(03)00924-3Carbonell-Bejerano, P., Urbez, C., Carbonell, J., Granell, A., & Perez-Amador, M. A. (2010). A Fertilization-Independent Developmental Program Triggers Partial Fruit Development and Senescence Processes in Pistils of Arabidopsis. Plant Physiology, 154(1), 163-172. doi:10.1104/pp.110.160044Carrera, E., Ruiz-Rivero, O., Peres, L. E. P., Atares, A., & Garcia-Martinez, J. L. (2012). Characterization of the procera Tomato Mutant Shows Novel Functions of the SlDELLA Protein in the Control of Flower Morphology, Cell Division and Expansion, and the Auxin-Signaling Pathway during Fruit-Set and Development. Plant Physiology, 160(3), 1581-1596. doi:10.1104/pp.112.204552Ceccato, L., Masiero, S., Sinha Roy, D., Bencivenga, S., Roig-Villanova, I., Ditengou, F. A., … Colombo, L. (2013). Maternal Control of PIN1 Is Required for Female Gametophyte Development in Arabidopsis. PLoS ONE, 8(6), e66148. doi:10.1371/journal.pone.0066148Christensen, C. A., King, E. J., Jordan, J. R., & Drews, G. N. (1997). Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sexual Plant Reproduction, 10(1), 49-64. doi:10.1007/s004970050067Clough, S. J., & Bent, A. F. (1998). Floral dip: a simplified method forAgrobacterium-mediated transformation ofArabidopsis thaliana. The Plant Journal, 16(6), 735-743. doi:10.1046/j.1365-313x.1998.00343.xCucinotta, M., Colombo, L., & Roig-Villanova, I. (2014). Ovule development, a new model for lateral organ formation. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00117Cucinotta, M., Manrique, S., Guazzotti, A., Quadrelli, N. E., Mendes, M. A., Benkova, E., & Colombo, L. (2016). Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development. Development, 143(23), 4419-4424. doi:10.1242/dev.143545Curtis, M. D., & Grossniklaus, U. (2003). A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta. Plant Physiology, 133(2), 462-469. doi:10.1104/pp.103.027979Cutcliffe, J. W., Hellmann, E., Heyl, A., & Rashotte, A. M. (2011). CRFs form protein–protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. Journal of Experimental Botany, 62(14), 4995-5002. doi:10.1093/jxb/err199Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K., & Scheible, W.-R. (2005). Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis. Plant Physiology, 139(1), 5-17. doi:10.1104/pp.105.063743Davière, J.-M., & Achard, P. (2016). A Pivotal Role of DELLAs in Regulating Multiple Hormone Signals. Molecular Plant, 9(1), 10-20. doi:10.1016/j.molp.2015.09.011De Vleesschauwer, D., Van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I.-R., … Höfte, M. (2012). Brassinosteroids Antagonize Gibberellin- and Salicylate-Mediated Root Immunity in Rice. Plant Physiology, 158(4), 1833-1846. doi:10.1104/pp.112.193672Deveaux, Y., Toffano-Nioche, C., Claisse, G., Thareau, V., Morin, H., Laufs, P., … Lecharny, A. (2008). Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evolutionary Biology, 8(1), 291. doi:10.1186/1471-2148-8-291Dill, A., Jung, H.-S., & Sun, T. -p. (2001). The DELLA motif is essential for gibberellin-induced degradation of RGA. Proceedings of the National Academy of Sciences, 98(24), 14162-14167. doi:10.1073/pnas.251534098Dorcey, E., Urbez, C., Blázquez, M. A., Carbonell, J., & Perez-Amador, M. A. (2009). Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. The Plant Journal, 58(2), 318-332. doi:10.1111/j.1365-313x.2008.03781.xElliott, R. C., Betzner, A. S., Huttner, E., Oakes, M. P., Tucker, W. Q., Gerentes, D., … Smyth, D. R. (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. The Plant Cell, 8(2), 155-168. doi:10.1105/tpc.8.2.155Endress, P. K. (2011). Angiosperm ovules: diversity, development, evolution. Annals of Botany, 107(9), 1465-1489. doi:10.1093/aob/mcr120Ezura, K., Ji-Seong, K., Mori, K., Suzuki, Y., Kuhara, S., Ariizumi, T., & Ezura, H. (2017). Genome-wide identification of pistil-specific genes expressed during fruit set initiation in tomato (Solanum lycopersicum). PLOS ONE, 12(7), e0180003. doi:10.1371/journal.pone.0180003Ferreira, L. G., de Alencar Dusi, D. M., Irsigler, A. S. T., Gomes, A. C. M. M., Mendes, M. A., Colombo, L., & de Campos Carneiro, V. T. (2017). GID1 expression is associated with ovule development of sexual and apomictic plants. Plant Cell Reports, 37(2), 293-306. doi:10.1007/s00299-017-2230-0Fuentes, S., Ljung, K., Sorefan, K., Alvey, E., Harberd, N. P., & Østergaard, L. (2012). Fruit Growth in Arabidopsis Occurs via DELLA-Dependent and DELLA-Independent Gibberellin Responses. The Plant Cell, 24(10), 3982-3996. doi:10.1105/tpc.112.103192Galbiati, F., Sinha Roy, D., Simonini, S., Cucinotta, M., Ceccato, L., Cuesta, C., … Colombo, L. (2013). An integrative model of the control of ovule primordia formation. The Plant Journal, 76(3), 446-455. doi:10.1111/tpj.12309Gallego-Bartolome, J., Minguet, E. G., Grau-Enguix, F., Abbas, M., Locascio, A., Thomas, S. G., … Blazquez, M. A. (2012). Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, 109(33), 13446-13451. doi:10.1073/pnas.1119992109Gallego-Giraldo, C., Hu, J., Urbez, C., Gomez, M. D., Sun, T., & Perez-Amador, M. A. (2014). Role of the gibberellin receptors GID1 during fruit-set in Arabidopsis. The Plant Journal, 79(6), 1020-1032. doi:10.1111/tpj.12603García-Hurtado, N., Carrera, E., Ruiz-Rivero, O., López-Gresa, M. P., Hedden, P., Gong, F., & García-Martínez, J. L. (2012). The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. Journal of Experimental Botany, 63(16), 5803-5813. doi:10.1093/jxb/ers229Gasser, C. S., Broadhvest, J., & Hauser, B. A. (1998). GENETIC ANALYSIS OF OVULE DEVELOPMENT. Annual Review of Plant Physiology and Plant Molecular Biology, 49(1), 1-24. doi:10.1146/annurev.arplant.49.1.1Gomez, M. D., Ventimilla, D., Sacristan, R., & Perez-Amador, M. A. (2016). Gibberellins Regulate Ovule Integument Development by Interfering with the Transcription Factor ATS. Plant Physiology, 172(4), 2403-2415. doi:10.1104/pp.16.01231Gomez-Mena, C. (2005). Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development, 132(3), 429-438. doi:10.1242/dev.01600Gupta, R., & Chakrabarty, S. K. (2013). Gibberellic acid in plant. Plant Signaling & Behavior, 8(9), e25504. doi:10.4161/psb.25504Hassidim, M., Harir, Y., Yakir, E., Kron, I., & Green, R. M. (2009). Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta, 230(3), 481-491. doi:10.1007/s00425-009-0958-7Heisler, M. G., Ohno, C., Das, P., Sieber, P., Reddy, G. V., Long, J. A., & Meyerowitz, 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(21), 1899-1911. doi:10.1016/j.cub.2005.09.052Huang, H.-Y., Jiang, W.-B., Hu, Y.-W., Wu, P., Zhu, J.-Y., Liang, W.-Q., … Lin, W.-H. (2013). BR Signal Influences Arabidopsis Ovule and Seed Number through Regulating Related Genes Expression by BZR1. Molecular Plant, 6(2), 456-469. doi:10.1093/mp/sss070Khanna, R., Kronmiller, B., Maszle, D. R., Coupland, G., Holm, M., Mizuno, T., & Wu, S.-H. (2009). The Arabidopsis B-Box Zinc Finger Family. The Plant Cell, 21(11), 3416-3420. doi:10.1105/tpc.109.069088Li, Q.-F., Wang, C., Jiang, L., Li, S., Sun, S. S. M., & He, J.-X. (2012). An Interaction Between BZR1 and DELLAs Mediates Direct Signaling Crosstalk Between Brassinosteroids and Gibberellins in Arabidopsis. Science Signaling, 5(244), ra72-ra72. doi:10.1126/scisignal.2002908Mantegazza, O., Gregis, V., Mendes, M. A., Morandini, P., Alves-Ferreira, M., Patreze, C. M., … Colombo, L. (2014). Analysis of the arabidopsis REM gene family predicts functions during flower development. Annals of Botany, 114(7), 1507-1515. doi:10.1093/aob/mcu124La Rosa, N. M. -d., Sotillo, B., Miskolczi, P., Gibbs, D. J., Vicente, J., Carbonero, P., … Blazquez, M. A. (2014). Large-Scale Identification of Gibberellin-Related Transcription Factors Defines Group VII ETHYLENE RESPONSE FACTORS as Functional DELLA Partners. PLANT PHYSIOLOGY, 166(2), 1022-1032. doi:10.1104/pp.114.244723Marín-de la Rosa, N., Pfeiffer, A., Hill, K., Locascio, A., Bhalerao, R. P., Miskolczi, P., … Alabadí, D. (2015). Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins. PLOS Genetics, 11(7), e1005337. doi:10.1371/journal.pgen.1005337Matias-Hernandez, L., Battaglia, R., Galbiati, F., Rubes, M., Eichenberger, C., Grossniklaus, U., … Colombo, L. (2010). VERDANDI Is a Direct Target of the MADS Domain Ovule Identity Complex and Affects Embryo Sac Differentiation in Arabidopsis. The Plant Cell, 22(6), 1702-1715. doi:10.1105/tpc.109.068627McAbee, J. M., Hill, T. A., Skinner, D. J., Izhaki, A., Hauser, B. A., Meister, R. J., … Gasser, C. S. (2006). ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. The Plant Journal, 46(3), 522-531. doi:10.1111/j.1365-313x.2006.02717.xMoore, I., Samalova, M., & Kurup, S. (2006). Transactivated and chemically inducible gene expression in plants. The Plant Journal, 45(4), 651-683. doi:10.1111/j.1365-313x.2006.02660.xMoubayidin, L., Perilli, S., Dello Ioio, R., Di Mambro, R., Costantino, P., & Sabatini, S. (2010). The Rate of Cell Differentiation Controls the Arabidopsis Root Meristem Growth Phase. Current Biology, 20(12), 1138-1143. doi:10.1016/j.cub.2010.05.035Murashige, T., & Skoog, F. (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15(3), 473-497. doi:10.1111/j.1399-3054.1962.tb08052.xNole-Wilson, S., Azhakanandam, S., & Franks, R. G. (2010). Polar auxin transport together with AINTEGUMENTA and REVOLUTA coordinate early Arabidopsis gynoecium development. Developmental Biology, 346(2), 181-195. doi:10.1016/j.ydbio.2010.07.016Pagnussat, G. C. (2005). Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development, 132(3), 603-614. doi:10.1242/dev.01595Peng, J., Carol, P., Richards, D. E., King, K. E., Cowling, R. J., Murphy, G. P., & Harberd, N. P. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses . Genes & Development, 11(23), 3194-3205. doi:10.1101/gad.11.23.3194Plackett, A. R. G., Ferguson, A. C., Powers, S. J., Wanchoo‐Kohli, A., Phillips, A. L., Wilson, Z. A., … Thomas, S. G. (2013). DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytologist, 201(3), 825-836. doi:10.1111/nph.12571Porri, A., Torti, S., Romera-Branchat, M., & Coupland, G. (2012). Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development, 139(12), 2198-2209. doi:10.1242/dev.077164Reyes-Olalde, J. I., Zuñiga-Mayo, V. M., Chávez Montes, R. A., Marsch-Martínez, N., & de Folter, S. (2013). Inside the gynoecium: at the carpel margin. Trends in Plant Science, 18(11), 644-655. doi:10.1016/j.tplants.2013.08.002José Ripoll, J., Bailey, L. J., Mai, Q.-A., Wu, S. L., Hon, C. T., Chapman, E. J., … Yanofsky, M. F. (2015). microRNA regulation of fruit growth. Nature Plants, 1(4). doi:10.1038/nplants.2015.36Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2009). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. doi:10.1093/bioinformatics/btp616Romera-Branchat, M., Ripoll, J. J., Yanofsky, M. F., & Pelaz, S. (2012). TheWOX13homeobox gene promotes replum formation in theArabidopsis thalianafruit. The Plant Journal, 73(1), 37-49. doi:10.1111/tpj.12010Ross, J. J., & Quittenden, L. J. (2016). Interactions between Brassinosteroids and Gibberellins: Synthesis or Signaling? The Plant Cell, 28(4), 829-832. doi:10.1105/tpc.15.00917Schneitz, K., Hulskamp, M., & Pruitt, R. E. (1995). Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. The Plant Journal, 7(5), 731-749. doi:10.1046/j.1365-313x.1995.07050731.xSkinner, D. J., & Gasser, C. S. (2009). Expression-based discovery of candidate ovule development regulators through transcriptional profiling of ovule mutants. BMC Plant Biology, 9(1), 29. doi:10.1186/1471-2229-9-29Skinner, D. J. (2004). Regulation of Ovule Development. THE PLANT CELL ONLINE, 16(suppl_1), S32-S45. doi:10.1105/tpc.015933Smyth, D. R., Bowman, J. L., & Meyerowitz, E. M. (1990). Early flower development in Arabidopsis. The Plant Cell, 2(8), 755-767. doi:10.1105/tpc.2.8.755Sun, T. (2010). Gibberellin-GID1-DELLA: A Pivotal Regulatory Module for Plant Growth and Development. Plant Physiology, 154(2), 567-570. doi:10.1104/pp.110.161554Feraru, E., Feraru, M. I., Kleine-Vehn, J., Martinière, A., Mouille, G., Vanneste, S., … Friml, J. (2011). PIN Polarity Maintenance by the Cell Wall in Arabidopsis. Current Biology, 21(4), 338-343. doi:10.1016/j.cub.2011.01.036Sun, Y., Fan, X.-Y., Cao, D.-M., Tang, W., He, K., Zhu, J.-Y., … Wang, Z.-Y. (2010). Integration of Brassinosteroid Signal Transduction with the Transcription Network for Plant Growth Regulation in Arabidopsis. Developmental Cell, 19(5), 765-777. doi:10.1016/j.devcel.2010.10.010Suzuki, H., Park, S.-H., Okubo, K., Kitamura, J., Ueguchi-Tanaka, M., Iuchi, S., … Nakajima, M. (2009). Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. The Plant Journal, 60(1), 48-55. doi:10.1111/j.1365-313x.2009.03936.xSwain, S. M., & Singh, D. P. (2005). Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends in Plant Science, 10(3), 123-129. doi:10.1016/j.tplants.2005.01.007Tanaka, K., Nakamura, Y., Asami, T., Yoshida, S., Matsuo, T., & Okamoto, S. (2003). Physiological Roles of Brassinosteroids in Early Growth of Arabidopsis: Brassinosteroids Have a Synergistic Relationship with Gibberellin as well as Auxin in Light-Grown Hypocotyl Elongation. Journal of Plant Growth Regulation, 22(3), 259-271. doi:10.1007/s00344-003-0119-3Tong, H., Xiao, Y., Liu, D., Gao, S., Liu, L., Yin, Y., … Chu, C. (2014). Brassinosteroid Regulates Cell Elongation by Modulating Gibberellin Metabolism in Rice. The Plant Cell, 26(11), 4376-4393. doi:10.1105/tpc.114.132092Truernit, E., Bauby, H., Dubreucq, B., Grandjean, O., Runions, J., Barthélémy, J., & Palauqui, J.-C. (2008). High-Resolution Whole-Mount Imaging of Three-Dimensional Tissue Organization and Gene Expression Enables the Study of Phloem Development and Structure in Arabidopsis. The Plant Cell, 20(6), 1494-1503. doi:10.1105/tpc.107.056069Unterholzner, S. J., Rozhon, W., Papacek, M., Ciomas, J., Lange, T., Kugler, K. G., … Poppenberger, B. (2015). Brassinosteroids Are Master Regulators of Gibberellin Biosynthesis in Arabidopsis. The Plant Cell, 27(8), 2261-2272. doi:10.1105/tpc.15.00433Vera-Sirera, F. , Gomez, M. D. and Perez-Amador, M. A. (2015). DELLA proteins, a group of GRAS transcription regulators, mediate gibberellin signaling. In Plant Transcription Factors: Evolutionary, Structural and Functional Aspects (ed. D. H. Gonzalez ), pp. 313-328. San Diego: Elsevier/Academic Press.Villarino, G. H., Hu, Q., Manrique, S., Flores-Vergara, M., Sehra, B., Robles, L., … Franks, R. G. (2016). Transcriptomic Signature of the SHATTERPROOF2 Expression Domain Reveals the Meristematic Nature of Arabidopsis Gynoecial Medial Domain. Plant Physiology, 171(1), 42-61. doi:10.1104/pp.15.01845Weigel, D. and Glazebrook, J. (2002). Arabidopsis: A laboratory Manual . Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.Yadegari, R. (2004). Female Gametophyte Development. THE PLANT CELL ONLINE, 16(suppl_1), S133-S141. doi:10.1105/tpc.018192Zhang, Z.-L., Ogawa, M., Fleet, C. M., Zentella, R., Hu, J., Heo, J.-O., … Sun, T. (2011). SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proceedings of the National Academy of Sciences, 108(5), 2160-2165. doi:10.1073/pnas.101223210

Truth and Robustness in Cross-country Growth Regressions

The work of Levine and Renelt (1992) and Sala-i-Martin (1997a, b) which attempted to test the robustness of various determinants of growth rates of per capita GDP among countries using two variants of Edward Leamerâ??s extreme-bounds analysis is reexamined. In a realistic Monte Carlo experiment in which the universe of potential determinants is drawn from those in Levine and Reneltâ??s study, both versions of the extreme-bounds analysis are evaluated for their ability to recover the true specification. Levine and Reneltâ??s method is shown to have low size and extremely low power: nothing is robust; while Sala-i-Martinâ??s method is shown to have high size and high power: it is undiscriminating. Both methods are compared to a cross-sectional version of the generalto-specific search methodology associated with the LSE approach to econometrics. It is shown to have size near nominal size and high power. Sala-i-Martinâ??s method and the general-to-specific method are then applied to the actual data from the original two studies. The results are consistent with the Monte Carlo results and are suggestive that the factors that most affect differences of growth rates are ones that are beyond the control of policymakers.growth, cross-country growth regressions, extreme-bounds analysis, general-to-specific specification search

Small Ubiquitin-like Modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin

Plants survive adverse conditions by modulating their growth in response to a changing environment. Gibberellins (GAs) play a key role in these adaptive responses by stimulating the degradation of growth-repressing DELLA proteins. GA binding to its receptor GID1 enables association of GID1 with DELLAs. This leads to the ubiquitin-mediated proteasomal degradation of DELLAs and consequently growth promotion. We report that DELLA-dependent growth control can be regulated independently of GA. We demonstrate that when a proportion of DELLAs is conjugated to the Small Ubiquitin-like Modifier (SUMO) protein, the extent of conjugation increases during stress. We identify a SUMO-interacting motif in GID1 and demonstrate that SUMO-conjugated DELLA binds to this motif in a GA-independent manner. The consequent sequestration of GID1 by SUMO-conjugated DELLAs leads to an accumulation of non-SUMOylated DELLAs, resulting in beneficial growth restraint during stress. We conclude that plants have developed a GA-independent mechanism to control growth

Los testamentos de Juana de Mendoza, camarera mayor de Isabel la Católica, y de su marido el poeta Gómez Manrique, corregidor de Toledo (1493 y 1490)

Study and edition of the original texts of the wills of the poet, theatre writer and politician Gómez Manrique (Amusco, h. 1412-Toledo 1490), corregidor in Salamanca, Burgos, Ávila and Toledo, one of queen Isabel I very loyal followers, and that of his wife Juana de Mendoza (Cuenca? h. 1425-Barcelona 1493), counselor and friend of the Catholic Queen, her chamberlain, and preceptor of the noble girls that were educated in the Castilian court. Gómez Manrique’s will has 13 lines in his own handwriting, including the date and his signature.Estudio y edición de los testamentos originales del poeta, autor de teatro y político Gómez Manrique (Amusco, h. 1412-Toledo 1490), corregidor de Salamanca, Burgos, Ávila y Toledo y leal servidor de Isabel I de Castilla, y del de su mujer Juana de Mendoza (¿Cuenca? h. 1425-Barcelona 1493), consejera y amiga de la reina católica, su camarera mayor, y preceptora y guarda de las damas que se educaban en su corte. El testamento de Gómez Manrique lleva trece líneas autógrafas, incluidas la fecha y firma

Evolutionary Analysis of DELLA-Associated Transcriptional Networks

[EN] DELLA proteins are transcriptional regulators present in all land plants which have been shown to modulate the activity of over 100 transcription factors in Arabidopsis, involved in multiple physiological and developmental processes. It has been proposed that DELLAs transduce environmental information to pre-wired transcriptional circuits because their stability is regulated by gibberellins (GAs), whose homeostasis largely depends on environmental signals. The ability of GAs to promote DELLA degradation coincides with the origin of vascular plants, but the presence of DELLAs in other land plants poses at least two questions: what regulatory properties have DELLAs provided to the behavior of transcriptional networks in land plants, and how has the recruitment of DELLAs by GA signaling affected this regulation. To address these issues, we have constructed gene co-expression networks of four different organisms within the green lineage with different properties regarding DELLAs: Arabidopsis thaliana and Solanum lycopersicum (both with GA- regulated DELLA proteins), Physcomitrella patens (with GA- independent DELLA proteins) and Chlamydomonas reinhardtii (a green alga without DELLA), and we have examined the relative evolution of the subnetworks containing the potential DELLA-dependent transcriptomes. Network analysis indicates a relative increase in parameters associated with the degree of interconnectivity in the DELLA-associated subnetworks of land plants, with a stronger effect in species with GA- regulated DELLA proteins. These results suggest that DELLAs may have played a role in the coordination of multiple transcriptional programs along evolution, and the function of DELLAs as regulatory 'hubs' became further consolidated after their recruitment by GA signaling in higher plants.Work in the laboratories was funded by grants BFU2016-80621-P and BIO2014-52425-P of the Spanish Ministry of Economy, Industry and Competitiveness, and H2020-MSCA-RISE-2014-644435 of the European Union. AB-M and JH-G hold Fellowships of the Spanish Ministry of Education, Culture and Sport FPU14/01941 and FPU15/01756, respectively.Briones-Moreno, A.; Hernández-García, J.; Vargas-Chávez, C.; Romero-Campero FJ; Romero, J.; Valverde, F.; Blazquez Rodriguez, MA. (2017). Evolutionary Analysis of DELLA-Associated Transcriptional Networks. Frontiers in Plant Science. 8(626):1-11. https://doi.org/10.3389/fpls.2017.00626S111862

통합적인 생장조절 신호들의 환경변화에 대한 식물 형태 적응에 끼치는 영향에 대한 연구

학위논문(박사) -- 서울대학교대학원 : 자연과학대학 화학부, 2022.2. 박충모.Plants in early developmental stages, from soil emergence to seedling establishment, experience dramatic changes in surrounding environments. Seedlings are particularly sensitive to changes imposed by environmental stimuli, such as light and temperature, and undergo morphological changes to achieve the best fitness. Alterations in plant body are elaborately shaped by coordination of diverse endogenous signaling pathways with external signals. Thus, studies on signaling crosstalks between endogenous and external signaling pathways are essential for understanding physiological responses of seedlings to fluctuating environments. However, not yet unexplored molecular and genetic linkages between endogenous signaling pathway and environmental cues still exist. In this study, I investigated molecular and genetic mechanisms underlying morphogenic adaptation of hypocotyls regulated by endogenous signaling pathways under varying light and temperature environments. In Chapter 1, I discuss the effects of a plant hormone ethylene on hypocotyl thermomorphogenesis in the light. The gaseous phytohormone ethylene plays vital roles in diverse developmental and environmental adaptation processes, such as fruit ripening, seedling establishment, mechanical stress tolerance and submergence escape. It is also known that in the light, ethylene promotes hypocotyl growth by stimulating the expression of PHYTOCHROME-INTERACTING FACTOR 3 (PIF3) transcription factor, which triggers microtubule reorganization during hypocotyl cell elongation. In particular, ethylene has been implicated in plant responses to warm temperatures in recent years. However, it is currently unclear how ethylene signals are functionally associated with hypocotyl thermomorphogenesis at the molecular level. Here, I show that ETHYLENE-INSENSITIVE 3 (EIN3)-mediated ethylene signals attenuate hypocotyl thermomorphogenesis by suppressing auxin responses. At warm temperatures, when the activity of the PIF4 thermomorphogenesis promoter is prominently high, the ethylene-activated EIN3 transcription factor directly induces the transcription of ARABIDOPSIS PP2C CLADE D7 (APD7) gene encoding a protein phosphatase that inactivates the plasma membrane (PM) H+-ATPase proton pumps. In conjunction with the promotive role of the PM H+-ATPases in hypocotyl cell elongation, these observations strongly support that the EIN3-directed induction of APD7 gene is linked with the suppression of auxin-induced cell expansion, leading to the reduction in thermomorphogenic hypocotyl growth. These data demonstrate that APD7 acts as a molecular hub that integrates ethylene and auxin signals into hypocotyl thermomorphogenesis. I propose that the ethylene–auxin signaling crosstalks via the EIN3-APD7 module facilitate the fine-tuning of hypocotyl thermomorphogenesis under natural environments, which often fluctuate in a complex manner. In Chapter 2, studies on molecular crosstalks between karrikin (KAR) and GA (gibberellic acid)/DELLA signaling pathways in the hypocotyl deetiolation process are described. Morphogenic adaptation of young seedlings to light environments is a critical developmental process that ensures plant survival and propagation, as they emerge from the soil. The photomorphogenic responses are facilitated by a network of light and growth hormonal signals, such as auxin and GA. KARs, a group of small butenolide compounds that is produced from burning plant materials in wildfires, are known to stimulate seed germination in fire-prone plant species. Notably, recent studies strongly support that they also facilitate seedling establishment, while underlying molecular mechanisms have been unexplored yet. Here, I demonstrate that SUPPRESSOR OF MAX2 1 (SMAX1), a negative regulator of KAR signaling, integrates light and KAR signals into GA-DELLA pathways that regulate hypocotyl growth during seedling photomorphogenesis and establishment. SMAX1-deficient Arabidopsis mutants exhibited a reduced hypocotyl elongation, and the short hypocotyl phenotypes were efficiently rescued by exogenous GA application and mutations in DELLA genes, such as REPRESSOR OF ga1-3 (RGA) and GIBBERELLIC ACID INSENSITIVE (GAI). Consistently, I found that SMAX1 facilitates the degradation of DELLA proteins in the hypocotyls in the light. Interestingly, light induces the accumulation of SMAX1 proteins, and the SMAX1-mediated degradation of DELLA is elevated in seedling establishment during the dark-to-light transition. These observations indicate that the SMAX1-mediated integration of light and KAR signals into GA pathways elaborately modulates seedling establishment. I propose that SMAX1 serves as a safeguard that ensures an optimized photomorphogenesis upon exposure to KARs, which is indicative of clear growth environments, as encountered following wildfires in nature.새싹돋움에서부터 새싹확립까지의 초기 발달 단계에 있는 식물들은 극심한 주변 환경 변화를 겪게 된다. 새싹들은 빛과 온도와 같은 환경 자극의 작은 변화에도 민감하게 반응하고 기관의 형태적 변화를 통해서 그 환경에 유리한 건강한 식물체를 얻고자 한다. 이런 식물체의 변화들은 외부 환경 신호들과 식물체 내의 신호전달경로들의 조직적 및 통합적인 조절 과정으로 인해 만들어지게 된다. 그러므로, 내•외부 신호전달 경로 간의 신호교차들을 연구하는 것은 환경변화에 대한 식물 새싹의 생리적인 반응들을 이해하는 데 필수적이다. 하지만, 아직까지 연구되지 않은 내•외부 신호전달 경로 간 분자적 유전자적 연결점이 여전히 존재한다. 본 연구에서는 변화하는 빛과 온도 환경 하에서, 내부적인 신호전달경로들에 의해 조절되는 새싹 줄기의 형태적 적응에 대한 분자적•유전자적 기작을 연구하였다. 제 1장에서는 빛이 있는 환경에서의 새싹 줄기 온도형태형성에 대한 식물호르몬 에틸렌의 작용에 대해 연구하였다. 기체 상태의 식물호르몬 에틸렌은 과일숙성, 새싹확립, 물리적 자극에 대한 스트레스 저항력, 그리고 잠수탈출과 같은 다양한 발달적•환경적 적응 과정에 중요한 역할을 한다. 또한, 빛이 있는 환경에서, 에틸렌은 PHYTOCHROME-INTERACTING FACTOR 3 (PIF3) 전사인자의 발현량을 증가시켜 새싹의 줄기 세포의 미소관의 재조립을 통해 새싹의 줄기 생장을 촉진한다고 알려져 있다. 특히, 최근에 식물의 온도 반응성에 대한 에틸렌이 연관되어 있음이 밝혀지고 있었다. 그러나, 아직까지는 어떻게 에틸렌 신호가 새싹 줄기의 온도형태형성을 조절하는 지에 대한 분자적인 수준에서 연구된 바 없다. 본 연구에서는, ETHYLENE-INSENSITIVE 3 (EIN3) 에 의한 에틸렌 신호가 또 다른 식물호르몬인 오옥신 (auxin) 의 반응성을 억제함으로써 새싹 줄기 온도형태형성을 약화시킨다는 것을 밝혔다. 온도형태형성을 촉진하는 PIF4 전사인자가 활성화되는 비교적 따뜻한 온도에서는, 에틸렌에 의해 활성화된 EIN3 전사인자가 직접적으로 원형질막의 H+-ATPase 양성자펌프를 불활성화하는 단백질 탈인산화효소가 코드화되어 있는 ARABIDOPSIS PP2C CLADE D7 (APD7) 유전자의 전사를 유도한다. 기존에 알려진 H+-ATPase의 세포 생장을 촉진하는 역할과 더불어, 본 연구에서 밝힌 EIN3에 의한 APD7 유전자의 전사 유도가 오옥신에 의한 세포 생장을 억제하는 것과 연관되어 제한된 새싹 줄기의 온도형태형성에 기인할 것이라 생각된다. 이에 따라, APD7은 새싹 줄기 온도형태형성에서 에틸렌과 오옥신 신호들을 통합하는 분자적인 중추라고 정리할 수 있다. EIN3-APD7 모듈에 의해 에틸렌-오옥신 신호 전달 경로 간의 교차가 일어나는 것은 여러 환경자극들이 복잡한 방법으로 종종 변하는 자연적인 환경에서 새싹 줄기 온도형태형성을 세밀하게 조정하기 위함이라 생각된다. 제 2장에서는 탈황화과정 (deetiolation process) 에서 새싹의 줄기 안에서 일어나는 카리킨 (KAR) 과 지베렐린산 (gibberellic acid) /DELLA 신호 전달 경로들 간의 교차에 대한 연구를 기술하였다. 빛 자극에 대한 어린 새싹들의 형태적인 적응은 흙 안을 벗어난 후의 생존과 번영을 보장하는 중요한 발달 과정이다. 빛형태형성적 반응들은 오옥신과 지베렐린산과 같은 생장호르몬들과 빛 신호들의 네트워크에 의해 조절된다. 들불에 의해 불타는 식물체에서 생성되는 작은 뷰테놀라이드계 화합물들 중의 일부분인 카리킨은 불에 약한 식물종들의 씨앗 발아를 촉진한다고 알려져 있다. 흥미롭게도, 최근 연구에 따르면, 카리킨은 새싹확립을 용이하게 해준다고 알려져 있다. 하지만 그에 대한 분자적인 기작에 대해서는 아직 알려진 바 없다. 본 연구에서는 카리킨 신호 전달의 음성조절자인 SUPPRESSOR OF MAX2 1 (SMAX1) 이 빛과 카리킨 신호들을 새싹 빛형태형성과 확립 과정 중 새싹 줄기 생장을 조절하는 지베렐린산-DELLA 신호전달경로에 통합시킨다는 것을 밝혔다. SMAX1이 결여된 애기장대 (Arabidopsis thaliana) 돌연변이체들은 짧은 새싹 줄기 표현형을 보여주고, 그 짧은 표현형은 외부적인 지베렐린산 첨가와 REPRESSOR OF ga1-3 (RGA) 과 GIBBERELLIC ACID INSENSITIVE (GAI) 과 같은 DELLA 유전자들을 돌연변이 시킴으로써 회복되는 것을 보여주었다. 이와 일관되게, 빛 조건 하에서 새싹 줄기 내의 SMAX1이 DELLA 단백질들의 분해를 용이하게 해준다는 것을 발견하였다. 흥미롭게도, 빛 자극은 SMAX1 단백질의 축적을 유도하고 SMAX1에 의한 DELLA 단백질의 분해 과정은 빛 환경으로 전환될 때 더 촉진된다. 본 연구에서는 SMAX1에 의해 지베렐린산 신호전달경로로 빛과 카리킨 신호들이 통합되는 것이 새싹확립 과정을 세밀히 조절하는 것을 밝혔다. 이를 통해, 자연적으로 발생하여 주변을 태워 깨끗이 정리하는 들불에 의해 생성되는 카리킨이 주는 최적의 생장 환경이 있다는 지시 신호에 따라 SMAX1은 빛형태형성의 최적화를 보장하는 보호 장치로서 작용한다 생각된다.CONTENTS ABSTRACT i CONTENTS iv LIST OF FIGURES viii LIST OF TABLES xii ABBREVIATIONS xiii CHAPTER 1: EIN3-mediated ethylene signals attenuate auxin response during hypocotyl thermomorphogenesis 2 INTRODUCTION 2 MATERIALS AND METHODS 1. Plant materials 5 2. Plant growth conditions 6 3. Gene expression analysis 6 4. Confocal microscopy 7 5. Immunological assay 7 6. GUS staining 8 7. ChIP assay 8 8. Yeast two-hybrid assay 9 9. Media acidification 12 10. Statistical analysis 13 RESULTS Ethylene suppresses hypocotyl growth at warm temperatures 14 Thermoresponsive action of ethylene on hypocotyl growth is independent of PIF3 17 Ethylene function in hypocotyl thermomorphogenesis is distinct from the triple response 18 Thermoresponsive role of ethylene is functionally associated with PIF4 23 EIN3 is involved in the ethylene-mediated attenuation of hypocotyl thermomorphogenesis 31 EIN3-mediated ethylene signals do not affect the PIF4 activity 35 EIN3 attenuates auxin response during hypocotyl thermomorphogenesis 42 EIN3 directly activates the PP2C-encoding APD7 gene 47 EIN3-mediated ethylene signals inhibit the progression of apoplastic acidification 50 DISCUSSION 59 ACKNOWLEDGEMENTS 66 CHAPTER 2: SMAX1 integrates karrikin and light signals into GA-mediated hypocotyl growth during seedling establishment 68 INTRODUCTION 68 MATERIALS AND METHODS 1. Plant materials 73 2. Plant growth conditions 74 3. Gene expression assays 75 4. Yeast two-hybrid assays 75 5. Coimmunoprecipitation assays 77 6. Immunological analysis 78 7. Confocal microscopy 79 9. Quantitation and statistical analysis 80 RESULTS GA attenuates KAR-induced suppression of hypocotyl growth 81 GA-DELLA module mediates the function of KARs during hypocotyl growth 82 Interaction of SMAX1 with DELLAs is important for hypocotyl growth 90 SMAX1 represses the nuclear accumulation of RGA in hypocotyl cells 93 SMAX1 proteins accumulate in the light 95 Light signals enhance SMAX1 function in DELLA-mediated seedling establishment 105 SMAX1 integrates KAR and light signals into GA-mediated seedling establishment 118 DISCUSSION 120 ACKNOWLEDGEMENTS 124 REFERENCES 125 PUBLICATION LIST 137 ABSTRACT IN KOREAN 139박

Tomato floral induction and flower development are orchestrated by the interplay between gibberellin and two unrelated microRNA-controlled modules

[EN] Age-regulated microRNA156 (miR156) and targets similarly control the competence to flower in diverse species. By contrast, the diterpene hormone gibberellin (GA) and the microRNA319-regulated TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factors promote flowering in the facultative long-day Arabidopsis thaliana, but suppress it in the day-neutral tomato (Solanum lycopersicum). We combined genetic and molecular studies and described a new interplay between GA and two unrelated miRNA-associated pathways that modulates tomato transition to flowering. Tomato PROCERA/DELLA activity is required to promote flowering along with the miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE (SPL/SBP) transcription factors by activating SINGLE FLOWER TRUSS (SFT) in the leaves and the MADS-Boxgene APETALA1(AP1)/MC at the shoot apex. Conversely, miR319-targeted LANCEOLATE represses floral transition by increasing GA concentrations and inactivating SFT in the leaves and AP1/MC at the shoot apex. Importantly, the combination of high GA concentrations/responses with the loss of SPL/SPB function impaired canonical meristem maturation and flower initiation in tomato. Our results reveal a cooperative regulation of tomato floral induction and flower development, integrating age cues (miR156 module) with GA responses and miR319-controlled pathways. Importantly, this study contributes to elucidate the mechanisms underlying the effects of GA in controlling flowering time in a day-neutral species.We thank Dr C. Schommer for kindly providing tcp4-soj8/+ seeds, and Carlos Rojas for Arabidopsis flowering time analyses. This work was supported by FAPESP (grant no. 15/17892-7 and fellowships nos 15/23826-7 and 13/16949-0). The authors declare no conflict of interest.Silva, G.; Silva, E.; Correa, J.; Vicente, M.; Jiang, N.; Notini, M.; Junior, A.... (2018). Tomato floral induction and flower development are orchestrated by the interplay between gibberellin and two unrelated microRNA-controlled modules. New Phytologist. 221(3):1328-1344. https://doi.org/10.1111/nph.15492S132813442213Andrés, F., & Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics, 13(9), 627-639. doi:10.1038/nrg3291Bassel, G. W., Mullen, R. T., & Bewley, J. D. (2008). procerais a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. Journal of Experimental Botany, 59(3), 585-593. doi:10.1093/jxb/erm354Ben‐Naim, O., Eshed, R., Parnis, A., Teper‐Bamnolker, P., Shalit, A., Coupland, G., … Lifschitz, E. (2006). The CCAAT binding factor can mediate interactions between CONSTANS‐like proteins and DNA. The Plant Journal, 46(3), 462-476. doi:10.1111/j.1365-313x.2006.02706.xBoss, P. K., & Thomas, M. R. (2002). Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature, 416(6883), 847-850. doi:10.1038/416847aBurko, Y., Shleizer-Burko, S., Yanai, O., Shwartz, I., Zelnik, I. D., Jacob-Hirsch, J., … Ori, N. (2013). A Role for APETALA1/FRUITFULL Transcription Factors in Tomato Leaf Development. The Plant Cell, 25(6), 2070-2083. doi:10.1105/tpc.113.113035Cardon, G., Höhmann, S., Klein, J., Nettesheim, K., Saedler, H., & Huijser, P. (1999). Molecular characterisation of the Arabidopsis SBP-box genes. Gene, 237(1), 91-104. doi:10.1016/s0378-1119(99)00308-xCarrera, E., Ruiz-Rivero, O., Peres, L. E. P., Atares, A., & Garcia-Martinez, J. L. (2012). Characterization of the procera Tomato Mutant Shows Novel Functions of the SlDELLA Protein in the Control of Flower Morphology, Cell Division and Expansion, and the Auxin-Signaling Pathway during Fruit-Set and Development. Plant Physiology, 160(3), 1581-1596. doi:10.1104/pp.112.204552Carvalho, R. F., Campos, M. L., Pino, L. E., Crestana, S. L., Zsögön, A., Lima, J. E., … Peres, L. E. (2011). Convergence of developmental mutants into a single tomato model system: «Micro-Tom» as an effective toolkit for plant development research. Plant Methods, 7(1), 18. doi:10.1186/1746-4811-7-18Cubas, P., Lauter, N., Doebley, J., & Coen, E. (1999). The TCP domain: a motif found in proteins regulating plant growth and development. The Plant Journal, 18(2), 215-222. doi:10.1046/j.1365-313x.1999.00444.xDavière, J.-M., Wild, M., Regnault, T., Baumberger, N., Eisler, H., Genschik, P., & Achard, P. (2014). Class I TCP-DELLA Interactions in Inflorescence Shoot Apex Determine Plant Height. Current Biology, 24(16), 1923-1928. doi:10.1016/j.cub.2014.07.012Silva, G. F. F. e, Silva, E. M., da Silva Azevedo, M., Guivin, M. A. C., Ramiro, D. A., Figueiredo, C. R., … Nogueira, F. T. S. (2014). microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. The Plant Journal, 78(4), 604-618. doi:10.1111/tpj.12493Gallego-Bartolome, J., Minguet, E. G., Marin, J. A., Prat, S., Blazquez, M. A., & Alabadi, D. (2010). Transcriptional Diversification and Functional Conservation between DELLA Proteins in Arabidopsis. Molecular Biology and Evolution, 27(6), 1247-1256. doi:10.1093/molbev/msq012Gallego-Giraldo, L., García-Martínez, J. L., Moritz, T., & López-Díaz, I. (2007). Flowering in Tobacco Needs Gibberellins but is not Promoted by the Levels of Active GA1 and GA4 in the Apical Shoot. Plant and Cell Physiology, 48(4), 615-625. doi:10.1093/pcp/pcm034Galvao, V. C., Horrer, D., Kuttner, F., & Schmid, M. (2012). Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development, 139(21), 4072-4082. doi:10.1242/dev.080879García-Hurtado, N., Carrera, E., Ruiz-Rivero, O., López-Gresa, M. P., Hedden, P., Gong, F., & García-Martínez, J. L. (2012). The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. Journal of Experimental Botany, 63(16), 5803-5813. doi:10.1093/jxb/ers229Gargul, J. M., Mibus, H., & Serek, M. (2013). Constitutive overexpression of Nicotiana GA 2 ox leads to compact phenotypes and delayed flowering in Kalanchoë blossfeldiana and Petunia hybrida. Plant Cell, Tissue and Organ Culture (PCTOC), 115(3), 407-418. doi:10.1007/s11240-013-0372-5Goldberg-Moeller, R., Shalom, L., Shlizerman, L., Samuels, S., Zur, N., Ophir, R., … Sadka, A. (2013). Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Science, 198, 46-57. doi:10.1016/j.plantsci.2012.09.012Hauvermale, A. L., Ariizumi, T., & Steber, C. M. (2012). Gibberellin Signaling: A Theme and Variations on DELLA Repression. Plant Physiology, 160(1), 83-92. doi:10.1104/pp.112.200956Hyun, Y., Richter, R., Vincent, C., Martinez-Gallegos, R., Porri, A., & Coupland, G. (2016). Multi-layered Regulation of SPL15 and Cooperation with SOC1 Integrate Endogenous Flowering Pathways at the Arabidopsis Shoot Meristem. Developmental Cell, 37(3), 254-266. doi:10.1016/j.devcel.2016.04.001Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M., & Matsuoka, M. (2002). The Gibberellin Signaling Pathway Is Regulated by the Appearance and Disappearance of SLENDER RICE1 in Nuclei. The Plant Cell, 14(1), 57-70. doi:10.1105/tpc.010319Jung, J.-H., Ju, Y., Seo, P. J., Lee, J.-H., & Park, C.-M. (2011). The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. The Plant Journal, 69(4), 577-588. doi:10.1111/j.1365-313x.2011.04813.xKing, R. W., & Ben-Tal, Y. (2001). A Florigenic Effect of Sucrose in Fuchsia hybrida Is Blocked by Gibberellin-Induced Assimilate Competition. Plant Physiology, 125(1), 488-496. doi:10.1104/pp.125.1.488Kubota, A., Ito, S., Shim, J. S., Johnson, R. S., Song, Y. H., Breton, G., … Imaizumi, T. (2017). TCP4-dependent induction of CONSTANS transcription requires GIGANTEA in photoperiodic flowering in Arabidopsis. PLOS Genetics, 13(6), e1006856. doi:10.1371/journal.pgen.1006856Kudla, J., & Bock, R. (2016). Lighting the Way to Protein-Protein Interactions: Recommendations on Best Practices for Bimolecular Fluorescence Complementation Analyses. The Plant Cell, 28(5), 1002-1008. doi:10.1105/tpc.16.00043Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z., … Eshed, Y. (2006). The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proceedings of the National Academy of Sciences, 103(16), 6398-6403. doi:10.1073/pnas.0601620103Liu, J., Cheng, X., Liu, P., Li, D., Chen, T., Gu, X., & Sun, J. (2017). MicroRNA319-regulated TCPs interact with FBHs and PFT1 to activate CO transcription and control flowering time in Arabidopsis. PLOS Genetics, 13(5), e1006833. doi:10.1371/journal.pgen.1006833Livak, K. J., & Schmittgen, T. D. (2001). Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods, 25(4), 402-408. doi:10.1006/meth.2001.1262Livne, S., Lor, V. S., Nir, I., Eliaz, N., Aharoni, A., Olszewski, N. E., … Weiss, D. (2015). Uncovering DELLA-Independent Gibberellin Responses by Characterizing New Tomato procera Mutants. The Plant Cell, 27(6), 1579-1594. doi:10.1105/tpc.114.132795Lombardi-Crestana, S., da Silva Azevedo, M., e Silva, G. F. F., Pino, L. E., Appezzato-da-Glória, B., Figueira, A., … Peres, L. E. P. (2012). The Tomato (Solanum Lycopersicum cv. Micro-Tom) Natural Genetic Variation Rg1 and the DELLA Mutant Procera Control the Competence Necessary to Form Adventitious Roots and Shoots. Journal of Experimental Botany, 63(15), 5689-5703. doi:10.1093/jxb/ers221Lozano, R., Gimenez, E., Cara, B., Capel, J., & Angosto, T. (2009). Genetic analysis of reproductive development in tomato. The International Journal of Developmental Biology, 53(8-9-10), 1635-1648. doi:10.1387/ijdb.072440rlMartin, K., Kopperud, K., Chakrabarty, R., Banerjee, R., Brooks, R., & Goodin, M. M. (2009). Transient expression inNicotiana benthamianafluorescent marker lines provides enhanced definition of protein localization, movement and interactionsin planta. The Plant Journal, 59(1), 150-162. doi:10.1111/j.1365-313x.2009.03850.xMartínez-Bello, L., Moritz, T., & López-Díaz, I. (2015). Silencing C19-GA 2-oxidases induces parthenocarpic development and inhibits lateral branching in tomato plants. Journal of Experimental Botany, 66(19), 5897-5910. doi:10.1093/jxb/erv300Meissner, R., Chague, V., Zhu, Q., Emmanuel, E., Elkind, Y., & Levy, A. A. (2000). A high throughput system for transposon tagging and promoter trapping in tomato. The Plant Journal, 22(3), 265-274. doi:10.1046/j.1365-313x.2000.00735.xMolinero-Rosales, N., Jamilena, M., Zurita, S., Gomez, P., Capel, J., & Lozano, R. (1999). FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. The Plant Journal, 20(6), 685-693. doi:10.1046/j.1365-313x.1999.00641.xMorea, E. G. O., da Silva, E. M., e Silva, G. F. F., Valente, G. T., Barrera Rojas, C. H., Vincentz, M., & Nogueira, F. T. S. (2016). Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biology, 16(1). doi:10.1186/s12870-016-0716-5Mounet, F., Moing, A., Garcia, V., Petit, J., Maucourt, M., Deborde, C., … Lemaire-Chamley, M. (2009). Gene and Metabolite Regulatory Network Analysis of Early Developing Fruit Tissues Highlights New Candidate Genes for the Control of Tomato Fruit Composition and Development. Plant Physiology, 149(3), 1505-1528. doi:10.1104/pp.108.133967Nir, I., Shohat, H., Panizel, I., Olszewski, N., Aharoni, A., & Weiss, D. (2017). The Tomato DELLA Protein PROCERA Acts in Guard Cells to Promote Stomatal Closure. The Plant Cell, 29(12), 3186-3197. doi:10.1105/tpc.17.00542Ohad, N., Shichrur, K., & Yalovsky, S. (2007). The Analysis of Protein-Protein Interactions in Plants by Bimolecular Fluorescence Complementation. Plant Physiology, 145(4), 1090-1099. doi:10.1104/pp.107.107284Ori, N., Cohen, A. R., Etzioni, A., Brand, A., Yanai, O., Shleizer, S., … Eshed, Y. (2007). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics, 39(6), 787-791. doi:10.1038/ng2036Pal, S., Zhao, J., Khan, A., Yadav, N. S., Batushansky, A., Barak, S., … Rachmilevitch, S. (2016). Paclobutrazol induces tolerance in tomato to deficit irrigation through diversified effects on plant morphology, physiology and metabolism. Scientific Reports, 6(1). doi:10.1038/srep39321Palatnik, J. F., Wollmann, H., Schommer, C., Schwab, R., Boisbouvier, J., Rodriguez, R., … Weigel, D. (2007). Sequence and Expression Differences Underlie Functional Specialization of Arabidopsis MicroRNAs miR159 and miR319. Developmental Cell, 13(1), 115-125. doi:10.1016/j.devcel.2007.04.012Parapunova, V., Busscher, M., Busscher-Lange, J., Lammers, M., Karlova, R., Bovy, A. G., … de Maagd, R. A. (2014). Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biology, 14(1), 157. doi:10.1186/1471-2229-14-157Park, S. J., Jiang, K., Schatz, M. C., & Lippman, Z. B. (2011). Rate of meristem maturation determines inflorescence architecture in tomato. Proceedings of the National Academy of Sciences, 109(2), 639-644. doi:10.1073/pnas.1114963109Pharis, R. P., & King, R. W. (1985). Gibberellins and Reproductive Development in Seed Plants. Annual Review of Plant Physiology, 36(1), 517-568. doi:10.1146/annurev.pp.36.060185.002505Porri, A., Torti, S., Romera-Branchat, M., & Coupland, G. (2012). Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development, 139(12), 2198-2209. doi:10.1242/dev.077164Preston, J. C., & Hileman, L. C. (2013). Functional Evolution in the Plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) Gene Family. Frontiers in Plant Science, 4. doi:10.3389/fpls.2013.00080Reinecke, D. M., Wickramarathna, A. D., Ozga, J. A., Kurepin, L. V., Jin, A. L., Good, A. G., & Pharis, R. P. (2013). Gibberellin 3-oxidase Gene Expression Patterns Influence Gibberellin Biosynthesis, Growth, and Development in Pea. PLANT PHYSIOLOGY, 163(2), 929-945. doi:10.1104/pp.113.225987Rubio-Somoza, I., & Weigel, D. (2011). MicroRNA networks and developmental plasticity in plants. Trends in Plant Science, 16(5), 258-264. doi:10.1016/j.tplants.2011.03.001Rubio-Somoza, I., Zhou, C.-M., Confraria, A., Martinho, C., von Born, P., Baena-Gonzalez, E., … Weigel, D. (2014). Temporal Control of Leaf Complexity by miRNA-Regulated Licensing of Protein Complexes. Current Biology, 24(22), 2714-2719. doi:10.1016/j.cub.2014.09.058Salinas, M., Xing, S., Höhmann, S., Berndtgen, R., & Huijser, P. (2011). Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta, 235(6), 1171-1184. doi:10.1007/s00425-011-1565-ySarvepalli, K., & Nath, U. (2011). Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. The Plant Journal, 67(4), 595-607. doi:10.1111/j.1365-313x.2011.04616.xSerrano-Mislata, A., Bencivenga, S., Bush, M., Schiessl, K., Boden, S., & Sablowski, R. (2017). DELLA genes restrict inflorescence meristem function independently of plant height. Nature Plants, 3(9), 749-754. doi:10.1038/s41477-017-0003-yShikata, M., & Ezura, H. (2016). Micro-Tom Tomato as an Alternative Plant Model System: Mutant Collection and Efficient Transformation. Methods in Molecular Biology, 47-55. doi:10.1007/978-1-4939-3115-6_5Stettler, R. F. (1964). DOSAGE EFFECTS OF THE LANCEOLATE GENE IN TOMATO. American Journal of Botany, 51(3), 253-264. doi:10.1002/j.1537-2197.1964.tb06628.xVarkonyi-Gasic, E., Wu, R., Wood, M., Walton, E. F., & Hellens, R. P. (2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3(1), 12. doi:10.1186/1746-4811-3-12Vendemiatti, E., Zsögön, A., Silva, G. F. F. e, de Jesus, F. A., Cutri, L., Figueiredo, C. R. F., … Peres, L. E. P. (2017). Loss of type-IV glandular trichomes is a heterochronic trait in tomato and can be reverted by promoting juvenility. Plant Science, 259, 35-47. doi:10.1016/j.plantsci.2017.03.006Vicente, M. H., Zsögön, A., de Sá, A. F. L., Ribeiro, R. V., & Peres, L. E. P. (2015). Semi-determinate growth habit adjusts the vegetative-to-reproductive balance and increases productivity and water-use efficiency in tomato ( Solanum lycopersicum ). Journal of Plant Physiology, 177, 11-19. doi:10.1016/j.jplph.2015.01.003Wang, J.-W., Czech, B., & Weigel, D. (2009). miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana. Cell, 138(4), 738-749. doi:10.1016/j.cell.2009.06.014Wilkie, J. D., Sedgley, M., & Olesen, T. (2008). Regulation of floral initiation in horticultural trees. Journal of Experimental Botany, 59(12), 3215-3228. doi:10.1093/jxb/ern188Yamaguchi, A., Wu, M.-F., Yang, L., Wu, G., Poethig, R. S., & Wagner, D. (2009). The MicroRNA-Regulated SBP-Box Transcription Factor SPL3 Is a Direct Upstream Activator of LEAFY, FRUITFULL, and APETALA1. Developmental Cell, 17(2), 268-278. doi:10.1016/j.devcel.2009.06.007Yamaguchi, N., Winter, C. M., Wu, M.-F., Kanno, Y., Yamaguchi, A., Seo, M., & Wagner, D. (2014). Gibberellin Acts Positively Then Negatively to Control Onset of Flower Formation in Arabidopsis. Science, 344(6184), 638-641. doi:10.1126/science.1250498Yamaguchi, S. (2008). Gibberellin Metabolism and its Regulation. Annual Review of Plant Biology, 59(1), 225-251. doi:10.1146/annurev.arplant.59.032607.092804Yamamoto, A., Nakamura, T., Adu-Gyamfi, J. J., & Saigusa, M. (2002). RELATIONSHIP BETWEEN CHLOROPHYLL CONTENT IN LEAVES OF SORGHUM AND PIGEONPEA DETERMINED BY EXTRACTION METHOD AND BY CHLOROPHYLL METER (SPAD-502). Journal of Plant Nutrition, 25(10), 2295-2301. doi:10.1081/pln-120014076Yanai, O., Shani, E., Russ, D., & Ori, N. (2011). Gibberellin partly mediates LANCEOLATE activity in tomato. The Plant Journal, 68(4), 571-582. doi:10.1111/j.1365-313x.2011.04716.xYu, S., Galvão, V. C., Zhang, Y.-C., Horrer, D., Zhang, T.-Q., Hao, Y.-H., … Wang, J.-W. (2012). Gibberellin Regulates the Arabidopsis Floral Transition through miR156-Targeted SQUAMOSA PROMOTER BINDING–LIKE Transcription Factors. The Plant Cell, 24(8), 3320-3332. doi:10.1105/tpc.112.101014Yuste-Lisbona, F. J., Quinet, M., Fernández-Lozano, A., Pineda, B., Moreno, V., Angosto, T., & Lozano, R. (2016). Characterization of vegetative inflorescence (mc-vin) mutant provides new insight into the role of MACROCALYX in regulating inflorescence development of tomato. Scientific Reports, 6(1). doi:10.1038/srep18796Zhang, S., Zhang, D., Fan, S., Du, L., Shen, Y., Xing, L., … Han, M. (2016). Effect of exogenous GA 3 and its inhibitor paclobutrazol on floral formation, endogenous hormones, and flowering-associated genes in ‘Fuji’ apple ( Malus domestica Borkh.). Plant Physiology and Biochemistry, 107, 178-186. doi:10.1016/j.plaphy.2016.06.005Zhang, X., Zou, Z., Zhang, J., Zhang, Y., Han, Q., Hu, T., … Ye, Z. (2010). Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Letters, 585(2), 435-439. doi:10.1016/j.febslet.2010.12.03

Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms

This is the peer reviewed version of the following article: Barro¿Trastoy, D., Carrera, E., Baños, J., Palau-Rodríguez, J., Ruiz-Rivero, O., Tornero, P., Alonso, J.M., López-Díaz, I., Gómez, M.D. and Pérez-Amador, M.A. (2020), Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms. Plant J, 102: 1026-1041, which has been published in final form at https://doi.org/10.1111/tpj.14684. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.[EN] Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co-regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.We wish to thank B. Janssen (Horticulture and Food Research Institute, New Zealand) for the pBJ60 shuttle vector, C. Ferrandiz and M. Colombo (IBMCP, CSIC-UPV, Valencia, Spain) for their help in the generation of 35S:ANT lines and L.E.P. Peres (Universidade de Sao Paulo, Brazil) for the tomato mutant lines. Our thanks also go to C. Fuster for technical assistance. This work was supported by grants from the Spanish Ministry of Economy and Competitiveness-FEDER (BIO2017-83138R) to MAPA and from NSF (DBI-0820755, MCB-1158181, and IOS-1444561) to JMA.Barro-Trastoy, D.; Carrera, E.; Baños, J.; Palau-Rodríguez, J.; Ruiz-Rivero, O.; Tornero Feliciano, P.; Alonso, JM.... (2020). Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms. The Plant Journal. 102(5):1026-1041. https://doi.org/10.1111/tpj.14684S102610411025Azhakanandam, S., Nole-Wilson, S., Bao, F., & Franks, R. G. (2008). SEUSSandAINTEGUMENTAMediate Patterning and Ovule Initiation during Gynoecium Medial Domain Development    . Plant Physiology, 146(3), 1165-1181. doi:10.1104/pp.107.114751Bai, M.-Y., Shang, J.-X., Oh, E., Fan, M., Bai, Y., Zentella, R., … Wang, Z.-Y. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biology, 14(8), 810-817. doi:10.1038/ncb2546Baker, S. C., Robinson-Beers, K., Villanueva, J. M., Gaiser, J. C., & Gasser, C. S. (1997). Interactions Among Genes Regulating Ovule Development in Arabidopsis thaliana. Genetics, 145(4), 1109-1124. doi:10.1093/genetics/145.4.1109Bartrina, I., Otto, E., Strnad, M., Werner, T., & Schmülling, T. (2011). Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana      . The Plant Cell, 23(1), 69-80. doi:10.1105/tpc.110.079079Belkhadir, Y., & Jaillais, Y. (2015). The molecular circuitry of brassinosteroid signaling. New Phytologist, 206(2), 522-540. doi:10.1111/nph.13269Bencivenga, S., Simonini, S., Benková, E., & Colombo, L. (2012). The Transcription Factors BEL1 and SPL Are Required for Cytokinin and Auxin Signaling During Ovule Development in Arabidopsis. The Plant Cell, 24(7), 2886-2897. doi:10.1105/tpc.112.100164Brumos, J., Zhao, C., Gong, Y., Soriano, D., Patel, A. P., Perez-Amador, M. A., … Alonso, J. M. (2019). An Improved Recombineering Toolset for Plants. The Plant Cell, 32(1), 100-122. doi:10.1105/tpc.19.00431Carrera, E., Ruiz-Rivero, O., Peres, L. E. P., Atares, A., & Garcia-Martinez, J. L. (2012). Characterization of the procera Tomato Mutant Shows Novel Functions of the SlDELLA Protein in the Control of Flower Morphology, Cell Division and Expansion, and the Auxin-Signaling Pathway during Fruit-Set and Development    . Plant Physiology, 160(3), 1581-1596. doi:10.1104/pp.112.204552Carvalho, R. F., Campos, M. L., Pino, L. E., Crestana, S. L., Zsögön, A., Lima, J. E., … Peres, L. E. (2011). Convergence of developmental mutants into a single tomato model system: «Micro-Tom» as an effective toolkit for plant development research. Plant Methods, 7(1). doi:10.1186/1746-4811-7-18Chory, J., Nagpal, P., & Peto, C. A. (1991). Phenotypic and Genetic Analysis of det2, a New Mutant That Affects Light-Regulated Seedling Development in Arabidopsis. The Plant Cell, 3(5), 445. doi:10.2307/3869351Clough, S. J., & Bent, A. F. (1998). Floral dip: a simplified method forAgrobacterium-mediated transformation ofArabidopsis thaliana. The Plant Journal, 16(6), 735-743. doi:10.1046/j.1365-313x.1998.00343.xClouse, S. D. (2011). Brassinosteroid Signal Transduction: From Receptor Kinase Activation to Transcriptional Networks Regulating Plant Development. The Plant Cell, 23(4), 1219-1230. doi:10.1105/tpc.111.084475Cucinotta, M., Colombo, L., & Roig-Villanova, I. (2014). Ovule development, a new model for lateral organ formation. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00117Cucinotta, M., Manrique, S., Guazzotti, A., Quadrelli, N. E., Mendes, M. A., Benkova, E., & Colombo, L. (2016). Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development. Development. doi:10.1242/dev.143545Davière, J.-M., & Achard, P. (2016). A Pivotal Role of DELLAs in Regulating Multiple Hormone Signals. Molecular Plant, 9(1), 10-20. doi:10.1016/j.molp.2015.09.011De Vleesschauwer, D., Van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I.-R., … Höfte, M. (2012). Brassinosteroids Antagonize Gibberellin- and Salicylate-Mediated Root Immunity in Rice      . Plant Physiology, 158(4), 1833-1846. doi:10.1104/pp.112.193672Dorcey, E., Urbez, C., Blázquez, M. A., Carbonell, J., & Perez-Amador, M. A. (2009). Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. The Plant Journal, 58(2), 318-332. doi:10.1111/j.1365-313x.2008.03781.xFujioka, S., Li, J., Choi, Y. H., Seto, H., Takatsuto, S., Noguchi, T., … Sakurai, A. (1997). The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. The Plant Cell, 9(11), 1951-1962. doi:10.1105/tpc.9.11.1951Galbiati, F., Sinha Roy, D., Simonini, S., Cucinotta, M., Ceccato, L., Cuesta, C., … Colombo, L. (2013). An integrative model of the control of ovule primordia formation. The Plant Journal, 76(3), 446-455. doi:10.1111/tpj.12309Gallego-Bartolome, J., Minguet, E. G., Grau-Enguix, F., Abbas, M., Locascio, A., Thomas, S. G., … Blazquez, M. A. (2012). Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, 109(33), 13446-13451. doi:10.1073/pnas.1119992109García-Hurtado, N., Carrera, E., Ruiz-Rivero, O., López-Gresa, M. P., Hedden, P., Gong, F., & García-Martínez, J. L. (2012). The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. Journal of Experimental Botany, 63(16), 5803-5813. doi:10.1093/jxb/ers229Gleave, A. P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology, 20(6), 1203-1207. doi:10.1007/bf00028910Gomez, M. D., Ventimilla, D., Sacristan, R., & Perez-Amador, M. A. (2016). Gibberellins Regulate Ovule Integument Development by Interfering with the Transcription Factor ATS. Plant Physiology, 172(4), 2403-2415. doi:10.1104/pp.16.01231He, J.-X., Gendron, J. M., Sun, Y., Gampala, S. S. L., Gendron, N., Sun, C. Q., & Wang, Z.-Y. (2005). BZR1 Is a Transcriptional Repressor with Dual Roles in Brassinosteroid Homeostasis and Growth Responses. Science, 307(5715), 1634-1638. doi:10.1126/science.1107580Huang, H.-Y., Jiang, W.-B., Hu, Y.-W., Wu, P., Zhu, J.-Y., Liang, W.-Q., … Lin, W.-H. (2013). BR Signal Influences Arabidopsis Ovule and Seed Number through Regulating Related Genes Expression by BZR1. Molecular Plant, 6(2), 456-469. doi:10.1093/mp/sss070Kurepin, L. V., Joo, S.-H., Kim, S.-K., Pharis, R. P., & Back, T. G. (2011). Interaction of Brassinosteroids with Light Quality and Plant Hormones in Regulating Shoot Growth of Young Sunflower and Arabidopsis Seedlings. Journal of Plant Growth Regulation, 31(2), 156-164. doi:10.1007/s00344-011-9227-7Li, Q.-F., Wang, C., Jiang, L., Li, S., Sun, S. S. M., & He, J.-X. (2012). An Interaction Between BZR1 and DELLAs Mediates Direct Signaling Crosstalk Between Brassinosteroids and Gibberellins in Arabidopsis. Science Signaling, 5(244). doi:10.1126/scisignal.2002908Li, X.-J., Chen, X.-J., Guo, X., Yin, L.-L., Ahammed, G. J., Xu, C.-J., … Yu, J.-Q. (2015). DWARFoverexpression induces alteration in phytohormone homeostasis, development, architecture and carotenoid accumulation in tomato. Plant Biotechnology Journal, 14(3), 1021-1033. doi:10.1111/pbi.12474Liu, Z., Franks, R. G., & Klink, V. P. (2000). Regulation of Gynoecium Marginal Tissue Formation by LEUNIG and AINTEGUMENTA. The Plant Cell, 12(10), 1879-1891. doi:10.1105/tpc.12.10.1879Marti, E. (2006). Genetic and physiological characterization of tomato cv. Micro-Tom. Journal of Experimental Botany, 57(9), 2037-2047. doi:10.1093/jxb/erj154Mizukami, Y., & Fischer, R. L. (2000). Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proceedings of the National Academy of Sciences, 97(2), 942-947. doi:10.1073/pnas.97.2.942Montoya, T., Nomura, T., Yokota, T., Farrar, K., Harrison, K., Jones, J. G. D., … Bishop, G. J. (2005). Patterns of Dwarf expression and brassinosteroid accumulation in tomato reveal the importance of brassinosteroid synthesis during fruit development. The Plant Journal, 42(2), 262-269. doi:10.1111/j.1365-313x.2005.02376.xMüller, C. J., Larsson, E., Spíchal, L., & Sundberg, E. (2017). Cytokinin-Auxin Crosstalk in the Gynoecial Primordium Ensures Correct Domain Patterning. Plant Physiology, 175(3), 1144-1157. doi:10.1104/pp.17.00805Murashige, T., & Skoog, F. (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15(3), 473-497. doi:10.1111/j.1399-3054.1962.tb08052.xOlimpieri, I., Siligato, F., Caccia, R., Soressi, G. P., Mazzucato, A., Mariotti, L., & Ceccarelli, N. (2007). Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis. Planta, 226(4), 877-888. doi:10.1007/s00425-007-0533-zPaz-Ares, J., & The REGIA Consortium. (2002). REGIA, An EU Project on Functional Genomics of Transcription Factors fromArabidopsis thaliana. Comparative and Functional Genomics, 3(2), 102-108. doi:10.1002/cfg.146Peng, J., Carol, P., Richards, D. E., King, K. E., Cowling, R. J., Murphy, G. P., & Harberd, N. P. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses . Genes & Development, 11(23), 3194-3205. doi:10.1101/gad.11.23.3194Reyes-Olalde, J. I., Zuñiga-Mayo, V. M., Chávez Montes, R. A., Marsch-Martínez, N., & de Folter, S. (2013). Inside the gynoecium: at the carpel margin. Trends in Plant Science, 18(11), 644-655. doi:10.1016/j.tplants.2013.08.002Sabelli, P. A., & Larkins, B. A. (2009). The Development of Endosperm in Grasses. Plant Physiology, 149(1), 14-26. doi:10.1104/pp.108.129437Schneitz, K., Baker, S. C., Gasser, C. S., & Redweik, A. (1998). 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, 125(14), 2555-2563. doi:10.1242/dev.125.14.2555Schneitz, K., Hulskamp, M., & Pruitt, R. E. (1995). Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. The Plant Journal, 7(5), 731-749. doi:10.1046/j.1365-313x.1995.07050731.xSeo, M., Jikumaru, Y., & Kamiya, Y. (2011). Profiling of Hormones and Related Metabolites in Seed Dormancy and Germination Studies. Methods in Molecular Biology, 99-111. doi:10.1007/978-1-61779-231-1_7Serrani, J. C., Sanjuán, R., Ruiz-Rivero, O., Fos, M., & García-Martínez, J. L. (2007). Gibberellin Regulation of Fruit Set and Growth in Tomato. Plant Physiology, 145(1), 246-257. doi:10.1104/pp.107.098335Serrani, J. C., Carrera, E., Ruiz-Rivero, O., Gallego-Giraldo, L., Peres, Lá. E. P., & García-Martínez, J. L. (2010). Inhibition of Auxin Transport from the Ovary or from the Apical Shoot Induces Parthenocarpic Fruit-Set in Tomato Mediated by Gibberellins    . Plant Physiology, 153(2), 851-862. doi:10.1104/pp.110.155424Sun, T. (2010). Gibberellin-GID1-DELLA: A Pivotal Regulatory Module for Plant Growth and Development. Plant Physiology, 154(2), 567-570. doi:10.1104/pp.110.161554Sun, T. (2011). The Molecular Mechanism and Evolution of the GA–GID1–DELLA Signaling Module in Plants. Current Biology, 21(9), R338-R345. doi:10.1016/j.cub.2011.02.036Tanaka, K., Nakamura, Y., Asami, T., Yoshida, S., Matsuo, T., & Okamoto, S. (2003). Physiological Roles of Brassinosteroids in Early Growth of Arabidopsis: Brassinosteroids Have a Synergistic Relationship with Gibberellin as well as Auxin in Light-Grown Hypocotyl Elongation. Journal of Plant Growth Regulation, 22(3), 259-271. doi:10.1007/s00344-003-0119-3Tang, Y., Liu, H., Guo, S., Wang, B., Li, Z., Chong, K., & Xu, Y. (2017). OsmiR396d Affects Gibberellin and Brassinosteroid Signaling to Regulate Plant Architecture in Rice. Plant Physiology, 176(1), 946-959. doi:10.1104/pp.17.00964Tong, H., Xiao, Y., Liu, D., Gao, S., Liu, L., Yin, Y., … Chu, C. (2014). Brassinosteroid Regulates Cell Elongation by Modulating Gibberellin Metabolism in Rice    . The Plant Cell, 26(11), 4376-4393. doi:10.1105/tpc.114.132092Truernit, E., Bauby, H., Dubreucq, B., Grandjean, O., Runions, J., Barthélémy, J., & Palauqui, J.-C. (2008). High-Resolution Whole-Mount Imaging of Three-Dimensional Tissue Organization and Gene Expression Enables the Study of Phloem Development and Structure inArabidopsis . The Plant Cell, 20(6), 1494-1503. doi:10.1105/tpc.107.056069Tursun, B., Cochella, L., Carrera, I., & Hobert, O. (2009). A Toolkit and Robust Pipeline for the Generation of Fosmid-Based Reporter Genes in C. elegans. PLoS ONE, 4(3), e4625. doi:10.1371/journal.pone.0004625Unterholzner, S. J., Rozhon, W., Papacek, M., Ciomas, J., Lange, T., Kugler, K. G., … Poppenberger, B. (2015). Brassinosteroids Are Master Regulators of Gibberellin Biosynthesis in Arabidopsis. The Plant Cell, 27(8), 2261-2272. doi:10.1105/tpc.15.00433Wang, Z.-Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., … Chory, J. (2002). Nuclear-Localized BZR1 Mediates Brassinosteroid-Induced Growth and Feedback Suppression of Brassinosteroid Biosynthesis. Developmental Cell, 2(4), 505-513. doi:10.1016/s1534-5807(02)00153-3Xiao, H., Radovich, C., Welty, N., Hsu, J., Li, D., Meulia, T., & van der Knaap, E. (2009). Integration of tomato reproductive developmental landmarks and expression profiles, and the effect of SUN on fruit shape. BMC Plant Biology, 9(1). doi:10.1186/1471-2229-9-49Xiao, Y., Liu, D., Zhang, G., Tong, H., & Chu, C. (2017). Brassinosteroids Regulate OFP1, a DLT Interacting Protein, to Modulate Plant Architecture and Grain Morphology in Rice. Frontiers in Plant Science, 8. doi:10.3389/fpls.2017.0169

Financial Shocks and Optimal Policy

This paper incorporates banks as well as frictions in the market for bank capital into a standard New Keynesian model and considers the positive and normative implications of various financial shocks. It shows that the frictions matter significantly for the effects of the shocks and the properties of optimal monetary and fiscal policy. For instance, for shocks that increase banks' demand for liquidity, optimal monetary policy accepts an output contraction while it would not in the absence of the frictions (or under suitably conducted fiscal policy). We find that optimal monetary policy can be approximated by a simple interest-rate rule targeting inflation; and it also allows large adjustments in the money supply, a property reminiscent of Poole's analysis.Financial frictions, banking, optimal policy