- -

Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development

Mostrar el registro sencillo del ítem

Ficheros en el ítem

dc.contributor.author Magne, K. es_ES
dc.contributor.author George, J. es_ES
dc.contributor.author Berbel Tornero, Ana es_ES
dc.contributor.author Broquet, B. es_ES
dc.contributor.author Madueño Albi, Francisco es_ES
dc.contributor.author Andersen, S. es_ES
dc.contributor.author Ratet, P. es_ES
dc.date.accessioned 2020-09-12T03:35:27Z
dc.date.available 2020-09-12T03:35:27Z
dc.date.issued 2018-06 es_ES
dc.identifier.issn 0960-7412 es_ES
dc.identifier.uri http://hdl.handle.net/10251/149964
dc.description.abstract [EN] The NOOT-BOP-COCH-LIKE (NBCL) genes are orthologs of Arabidopsis thaliana BLADE-ON-PETIOLE1/2. The NBCLs are developmental regulators essential for plant shaping, mainly through the regulation of organ boundaries, the promotion of lateral organ differentiation and the acquisition of organ identity. In addition to their roles in leaf, stipule and flower development, NBCLs are required for maintaining the identity of indeterminate nitrogen-fixing nodules with persistent meristems in legumes. In legumes forming determinate nodules, without persistent meristem, the roles of NBCL genes are not known. We thus investigated the role of Lotus japonicus NOOT-BOP-COCH-LIKE1 (LjNBCL1) in determinate nodule identity and studied its functions in aerial organ development using LORE1 insertional mutants and RNA interference-mediated silencing approaches. In Lotus, LjNBCL1 is involved in leaf patterning and participates in the regulation of axillary outgrowth. Wild-type Lotus leaves are composed of five leaflets and possess a pair of nectaries at the leaf axil. Legumes such as pea and Medicago have a pair of stipules, rather than nectaries, at the base of their leaves. In Ljnbcl1, nectary development is abolished, demonstrating that nectaries and stipules share a common evolutionary origin. In addition, ectopic roots arising from nodule vascular meristems and reorganization of the nodule vascular bundle vessels were observed on Ljnbcl1 nodules. This demonstrates that NBCL functions are conserved in both indeterminate and determinate nodules through the maintenance of nodule vascular bundle identity. In contrast to its role in floral patterning described in other plants, LjNBCL1 appears essential for the development of both secondary inflorescence meristem and floral meristem. es_ES
dc.description.sponsorship This work was supported by the CNRS and by the grants ANR-14-CE19-0003 (NOOT) from the Agence National de la Recherche (ANR) to PR. This work has benefited from the facilities and expertise of the Servicio de Microscopia Electronica Universitat Politecnica de Valencia (Spain, http://www.upv.es/entidades/SME/) and of the IMAGIF Cell Biology Unit of the Gif campus (France, www.imagif.cnrs.fr) which is supported by the Conseil General de l'Essonne. The authors thank Dr Mathias Brault from the Institute of Plant Sciences Paris-Saclay (France) for providing the pFRN: RNAi plasmid, A. rhizogenes ARqua1 strain and control GUS:RNAi construction, and Dr Simona Radutoiu from the University of Aarhus (Denmark), for providing the Na-Borate/TRIZOL RNA extraction protocol. We are grateful to Dr Cristina Ferrandiz from the Instituto de Biologia Molecular y Celular de Plantas (Spain) for help in interpreting the identity of the meristems in the SEM pictures and Professor Frederique Guinel from the University of Wilfrid Laurier (Canada) for help in interpreting the identity of L. japonicus nodule vascular tissues. We thank Dr Julie Hofer from the University of Auckland (New Zealand), for manuscript revision and English language polishing. es_ES
dc.language Inglés es_ES
dc.publisher Blackwell Publishing es_ES
dc.relation.ispartof The Plant Journal es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject NOOT-BOP-COCH-LIKE genes es_ES
dc.subject Determinate nodule es_ES
dc.subject Nodule identity es_ES
dc.subject Nectary glands es_ES
dc.subject Flower development es_ES
dc.subject Leaf patterning es_ES
dc.subject Lotus japonicus es_ES
dc.subject Organogenesis es_ES
dc.title Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1111/tpj.13905 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/ANR//ANR-14-CE19-0003/FR/The plant NOOT genes are guards for the symbiotic organ identity and abscission capacity/NOOT/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Magne, K.; George, J.; Berbel Tornero, A.; Broquet, B.; Madueño Albi, F.; Andersen, S.; Ratet, P. (2018). Lotus japonicus NOOT-BOP-COCH-LIKE1 is essential for nodule, nectary, leaf and flower development. The Plant Journal. 94(5):880-894. https://doi.org/10.1111/tpj.13905 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1111/tpj.13905 es_ES
dc.description.upvformatpinicio 880 es_ES
dc.description.upvformatpfin 894 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 94 es_ES
dc.description.issue 5 es_ES
dc.identifier.pmid 29570881 es_ES
dc.relation.pasarela S\382360 es_ES
dc.contributor.funder Agence Nationale de la Recherche, Francia es_ES
dc.contributor.funder Centre National de la Recherche Scientifique, Francia es_ES
dc.description.references Aida, M., & Tasaka, M. (2006). Genetic control of shoot organ boundaries. Current Opinion in Plant Biology, 9(1), 72-77. doi:10.1016/j.pbi.2005.11.011 es_ES
dc.description.references Aida, M., & Tasaka, M. (2006). Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex. Plant Molecular Biology, 60(6), 915-928. doi:10.1007/s11103-005-2760-7 es_ES
dc.description.references Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. The Plant Cell, 9(6), 841-857. doi:10.1105/tpc.9.6.841 es_ES
dc.description.references AKASAKA, Y. (1998). Morphological Alterations and Root Nodule Formation inAgrobacterium rhizogenes-mediated Transgenic Hairy Roots of Peanut (Arachis hypogaeaL.). Annals of Botany, 81(2), 355-362. doi:10.1006/anbo.1997.0566 es_ES
dc.description.references Benlloch, R., Berbel, A., Ali, L., Gohari, G., Millán, T., & Madueño, F. (2015). Genetic control of inflorescence architecture in legumes. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.00543 es_ES
dc.description.references Berbel, A., Ferrándiz, C., Hecht, V., Dalmais, M., Lund, O. S., Sussmilch, F. C., … Madueño, F. (2012). VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nature Communications, 3(1). doi:10.1038/ncomms1801 es_ES
dc.description.references Blázquez, M. A., Ferrándiz, C., Madueño, F., & Parcy, F. (2006). How Floral Meristems are Built. Plant Molecular Biology, 60(6), 855-870. doi:10.1007/s11103-006-0013-z es_ES
dc.description.references Brown, S. M., Oparka, K. J., Sprent, J. I., & Walsh, K. B. (1995). Symplastic transport in soybean root nodules. Soil Biology and Biochemistry, 27(4-5), 387-399. doi:10.1016/0038-0717(95)98609-r es_ES
dc.description.references Chen, Y., Chen, W., Li, X., Jiang, H., Wu, P., Xia, K., … Wu, G. (2013). Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant and Cell Physiology, 55(1), 183-193. doi:10.1093/pcp/pct171 es_ES
dc.description.references Cho, E., & Zambryski, P. C. (2011). ORGAN BOUNDARY1defines a gene expressed at the junction between the shoot apical meristem and lateral organs. Proceedings of the National Academy of Sciences, 108(5), 2154-2159. doi:10.1073/pnas.1018542108 es_ES
dc.description.references Couzigou, J.-M., & Ratet, P. (2015). NOOT-Dependent Control of Nodule Identity: Nodule Homeosis and Merirostem Perturbation. Biological Nitrogen Fixation, 487-498. doi:10.1002/9781119053095.ch49 es_ES
dc.description.references Couzigou, J.-M., Zhukov, V., Mondy, S., Abu el Heba, G., Cosson, V., Ellis, T. H. N., … Ratet, P. (2012). NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes. The Plant Cell, 24(11), 4498-4510. doi:10.1105/tpc.112.103747 es_ES
dc.description.references Couzigou, J.-M., Magne, K., Mondy, S., Cosson, V., Clements, J., & Ratet, P. (2015). The legume NOOT-BOP-COCH-LIKE genes are conserved regulators of abscission, a major agronomical trait in cultivated crops. New Phytologist, 209(1), 228-240. doi:10.1111/nph.13634 es_ES
dc.description.references Czechowski, 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.105.063743 es_ES
dc.description.references Dong, Z., Zhao, Z., Liu, C., Luo, J., Yang, J., Huang, W., … Luo, D. (2005). Floral Patterning in Lotus japonicus. Plant Physiology, 137(4), 1272-1282. doi:10.1104/pp.104.054288 es_ES
dc.description.references Ehrhardt, D., Atkinson, E., & Long. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science, 256(5059), 998-1000. doi:10.1126/science.10744524 es_ES
dc.description.references Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Cai, Z., … Luo, D. (2006). Control of petal shape and floral zygomorphy in Lotus japonicus. Proceedings of the National Academy of Sciences, 103(13), 4970-4975. doi:10.1073/pnas.0600681103 es_ES
dc.description.references Ferguson, B. J., & Reid, J. B. (2005). Cochleata: Getting to the Root of Legume Nodules. Plant and Cell Physiology, 46(9), 1583-1589. doi:10.1093/pcp/pci171 es_ES
dc.description.references Ferraioli, S., Tatè, R., Rogato, A., Chiurazzi, M., & Patriarca, E. J. (2004). Development of Ectopic Roots from Abortive Nodule Primordia. Molecular Plant-Microbe Interactions®, 17(10), 1043-1050. doi:10.1094/mpmi.2004.17.10.1043 es_ES
dc.description.references Franssen, H. J., Xiao, T. T., Kulikova, O., Wan, X., Bisseling, T., Scheres, B., & Heidstra, R. (2015). Root developmental programs shape the Medicago truncatula nodule meristem. Development, 142(17), 2941-2950. doi:10.1242/dev.120774 es_ES
dc.description.references Gonzalez-Rizzo, S., Crespi, M., & Frugier, F. (2006). The Medicago truncatula CRE1 Cytokinin Receptor Regulates Lateral Root Development and Early Symbiotic Interaction with Sinorhizobium meliloti. The Plant Cell, 18(10), 2680-2693. doi:10.1105/tpc.106.043778 es_ES
dc.description.references Gourion, B., Sulser, S., Frunzke, J., Francez-Charlot, A., Stiefel, P., Pessi, G., … Fischer, H.-M. (2009). The PhyR-σEcfGsignalling cascade is involved in stress response and symbiotic efficiency inBradyrhizobium japonicum. Molecular Microbiology, 73(2), 291-305. doi:10.1111/j.1365-2958.2009.06769.x es_ES
dc.description.references Gourlay, C. W., Hofer, J. M. I., & Ellis, T. H. N. (2000). Pea Compound Leaf Architecture Is Regulated by Interactions among the Genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS. The Plant Cell, 12(8), 1279-1294. doi:10.1105/tpc.12.8.1279 es_ES
dc.description.references Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M. K., & Bonfante, P. (2009). Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist, 182(1), 200-212. doi:10.1111/j.1469-8137.2008.02725.x es_ES
dc.description.references Guinel, F. C. (2009). Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types. Botany, 87(12), 1117-1138. doi:10.1139/b09-074 es_ES
dc.description.references Ha, C. M. (2003). The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development, 130(1), 161-172. doi:10.1242/dev.00196 es_ES
dc.description.references Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2004). BLADE-ON-PETIOLE1 Encodes a BTB/POZ Domain Protein Required for Leaf Morphogenesis in Arabidopsis thaliana. Plant and Cell Physiology, 45(10), 1361-1370. doi:10.1093/pcp/pch201 es_ES
dc.description.references Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (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(6), 1809-1825. doi:10.1105/tpc.107.051938 es_ES
dc.description.references Handberg, K., & Stougaard, J. (1992). Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal, 2(4), 487-496. doi:10.1111/j.1365-313x.1992.00487.x es_ES
dc.description.references Hepworth, S. R., & Pautot, V. A. (2015). Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01052 es_ES
dc.description.references Hepworth, S. R., Zhang, Y., McKim, S., Li, X., & Haughn, G. W. (2005). BLADE-ON-PETIOLE–Dependent Signaling Controls Leaf and Floral Patterning in Arabidopsis. The Plant Cell, 17(5), 1434-1448. doi:10.1105/tpc.104.030536 es_ES
dc.description.references Hepworth, S. R., Klenz, J. E., & Haughn, G. W. (2005). UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta, 223(4), 769-778. doi:10.1007/s00425-005-0138-3 es_ES
dc.description.references Hibara, K., Karim, M. R., Takada, S., Taoka, K., Furutani, M., Aida, M., & Tasaka, M. (2006). Arabidopsis CUP-SHAPED COTYLEDON3 Regulates Postembryonic Shoot Meristem and Organ Boundary Formation. The Plant Cell, 18(11), 2946-2957. doi:10.1105/tpc.106.045716 es_ES
dc.description.references Høgslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M. A., Goffard, N., … Stougaard, J. (2009). Dissection of Symbiosis and Organ Development by Integrated Transcriptome Analysis of Lotus japonicus Mutant and Wild-Type Plants. PLoS ONE, 4(8), e6556. doi:10.1371/journal.pone.0006556 es_ES
dc.description.references JARVIS, B. D. W., PANKHURST, C. E., & PATEL, J. J. (1982). Rhizobium loti, a New Species of Legume Root Nodule Bacteria. International Journal of Systematic Bacteriology, 32(3), 378-380. doi:10.1099/00207713-32-3-378 es_ES
dc.description.references Karim, M. R., Hirota, A., Kwiatkowska, D., Tasaka, M., & Aida, M. (2009). A Role for Arabidopsis PUCHI in Floral Meristem Identity and Bract Suppression. The Plant Cell, 21(5), 1360-1372. doi:10.1105/tpc.109.067025 es_ES
dc.description.references Khan, M., Xu, M., Murmu, J., Tabb, P., Liu, Y., Storey, K., … Hepworth, S. R. (2011). Antagonistic Interaction of BLADE-ON-PETIOLE1 and 2 with BREVIPEDICELLUS and PENNYWISE Regulates Arabidopsis Inflorescence Architecture. Plant Physiology, 158(2), 946-960. doi:10.1104/pp.111.188573 es_ES
dc.description.references Koch, B., & Evans, H. J. (1966). Reduction of Acetylene to Ethylene by Soybean Root Nodules. Plant Physiology, 41(10), 1748-1750. doi:10.1104/pp.41.10.1748 es_ES
dc.description.references Krall, L., Wiedemann, U., Unsin, G., Weiss, S., Domke, N., & Baron, C. (2002). Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, 99(17), 11405-11410. doi:10.1073/pnas.172390699 es_ES
dc.description.references Kumagai, H., & Kouchi, H. (2003). Gene Silencing by Expression of Hairpin RNA in Lotus japonicus Roots and Root Nodules. Molecular Plant-Microbe Interactions®, 16(8), 663-668. doi:10.1094/mpmi.2003.16.8.663 es_ES
dc.description.references Levin, J. Z., & Meyerowitz, E. M. (1995). UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. The Plant Cell, 7(5), 529-548. doi:10.1105/tpc.7.5.529 es_ES
dc.description.references Long, J., & Barton, M. K. (2000). Initiation of Axillary and Floral Meristems in Arabidopsis. Developmental Biology, 218(2), 341-353. doi:10.1006/dbio.1999.9572 es_ES
dc.description.references Małolepszy, A., Mun, T., Sandal, N., Gupta, V., Dubin, M., Urbański, D., … Andersen, S. U. (2016). The LORE 1 insertion mutant resource. The Plant Journal, 88(2), 306-317. doi:10.1111/tpj.13243 es_ES
dc.description.references McKim, S. M., Stenvik, G.-E., Butenko, M. A., Kristiansen, W., Cho, S. K., Hepworth, S. R., … Haughn, G. W. (2008). The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development, 135(8), 1537-1546. doi:10.1242/dev.012807 es_ES
dc.description.references Mun, T., Bachmann, A., Gupta, V., Stougaard, J., & Andersen, S. U. (2016). Lotus Base: An integrated information portal for the model legume Lotus japonicus. Scientific Reports, 6(1). doi:10.1038/srep39447 es_ES
dc.description.references Norberg, M. (2005). The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development, 132(9), 2203-2213. doi:10.1242/dev.01815 es_ES
dc.description.references Okamoto, S., Yoro, E., Suzaki, T., & Kawaguchi, M. (2013). Hairy Root Transformation in Lotus japonicus. BIO-PROTOCOL, 3(12). doi:10.21769/bioprotoc.795 es_ES
dc.description.references Oldroyd, G. E. D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology, 11(4), 252-263. doi:10.1038/nrmicro2990 es_ES
dc.description.references Oldroyd, G. E. D., & Downie, J. A. (2008). Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes. Annual Review of Plant Biology, 59(1), 519-546. doi:10.1146/annurev.arplant.59.032607.092839 es_ES
dc.description.references Pate, J. S., Gunning, B. E. S., & Briarty, L. G. (1969). Ultrastructure and functioning of the transport system of the leguminous root nodule. Planta, 85(1), 11-34. doi:10.1007/bf00387658 es_ES
dc.description.references Ping, J., Liu, Y., Sun, L., Zhao, M., Li, Y., She, M., … Ma, J. (2014). Dt2 Is a Gain-of-Function MADS-Domain Factor Gene That Specifies Semideterminacy in Soybean. The Plant Cell, 26(7), 2831-2842. doi:10.1105/tpc.114.126938 es_ES
dc.description.references Quandt, H.-J. (1993). Transgenic Root Nodules ofVicia hirsuta:A Fast and Efficient System for the Study of Gene Expression in Indeterminate-Type Nodules. Molecular Plant-Microbe Interactions, 6(6), 699. doi:10.1094/mpmi-6-699 es_ES
dc.description.references Roux, B., Rodde, N., Jardinaud, M.-F., Timmers, T., Sauviac, L., Cottret, L., … Gamas, P. (2014). An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. The Plant Journal, 77(6), 817-837. doi:10.1111/tpj.12442 es_ES
dc.description.references Schultz, E. A., & Haughn, G. W. (1991). LEAFY, a Homeotic Gene That Regulates Inflorescence Development in Arabidopsis. The Plant Cell, 771-781. doi:10.1105/tpc.3.8.771 es_ES
dc.description.references Sinharoy, S., & DasGupta, M. (2009). RNA Interference Highlights the Role of CCaMK in Dissemination of Endosymbionts in the Aeschynomeneae Legume Arachis. Molecular Plant-Microbe Interactions®, 22(11), 1466-1475. doi:10.1094/mpmi-22-11-1466 es_ES
dc.description.references Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., & Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, 92(7), 2647-2651. doi:10.1073/pnas.92.7.2647 es_ES
dc.description.references Soyano, T., Kouchi, H., Hirota, A., & Hayashi, M. (2013). NODULE INCEPTION Directly Targets NF-Y Subunit Genes to Regulate Essential Processes of Root Nodule Development in Lotus japonicus. PLoS Genetics, 9(3), e1003352. doi:10.1371/journal.pgen.1003352 es_ES
dc.description.references Suzaki, T., Yoro, E., & Kawaguchi, M. (2015). Leguminous Plants: Inventors of Root Nodules to Accommodate Symbiotic Bacteria. International Review of Cell and Molecular Biology, 111-158. doi:10.1016/bs.ircmb.2015.01.004 es_ES
dc.description.references Takeda, S., Hanano, K., Kariya, A., Shimizu, S., Zhao, L., Matsui, M., … Aida, M. (2011). CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. The Plant Journal, 66(6), 1066-1077. doi:10.1111/j.1365-313x.2011.04571.x es_ES
dc.description.references Tavakol, E., Okagaki, R., Verderio, G., Shariati J., V., Hussien, A., Bilgic, H., … Rossini, L. (2015). The Barley Uniculme4 Gene Encodes a BLADE-ON-PETIOLE-Like Protein That Controls Tillering and Leaf Patterning. Plant Physiology, 168(1), 164-174. doi:10.1104/pp.114.252882 es_ES
dc.description.references Udvardi, M., & Poole, P. S. (2013). Transport and Metabolism in Legume-Rhizobia Symbioses. Annual Review of Plant Biology, 64(1), 781-805. doi:10.1146/annurev-arplant-050312-120235 es_ES
dc.description.references Van de Velde, W., Guerra, J. C. P., Keyser, A. D., De Rycke, R., Rombauts, S., Maunoury, N., … Goormachtig, S. (2006). Aging in Legume Symbiosis. A Molecular View on Nodule Senescence in Medicago truncatula. Plant Physiology, 141(2), 711-720. doi:10.1104/pp.106.078691 es_ES
dc.description.references Verdier, J., Torres-Jerez, I., Wang, M., Andriankaja, A., Allen, S. N., He, J., … Udvardi, M. K. (2013). Establishment of theLotus japonicusGene Expression Atlas (LjGEA) and its use to explore legume seed maturation. The Plant Journal, 74(2), 351-362. doi:10.1111/tpj.12119 es_ES
dc.description.references WALSH, K. B., McCULLY, M. E., & CANNY, M. J. (1989). Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway. Plant, Cell and Environment, 12(4), 395-405. doi:10.1111/j.1365-3040.1989.tb01955.x es_ES
dc.description.references Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2015). Divide et impera : boundaries shape the plant body and initiate new meristems. New Phytologist, 209(2), 485-498. doi:10.1111/nph.13641 es_ES
dc.description.references Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., … Yang, J. (2011). Petal Development in Lotus japonicus. Journal of Integrative Plant Biology, 53(10), 770-782. doi:10.1111/j.1744-7909.2011.01072.x es_ES
dc.description.references Werner, G. D. A., Cornwell, W. K., Sprent, J. I., Kattge, J., & Kiers, E. T. (2014). A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Communications, 5(1). doi:10.1038/ncomms5087 es_ES
dc.description.references Wopereis, J., Pajuelo, E., Dazzo, F. B., Jiang, Q., Gresshoff, P. M., de Bruijn, F. J., … Szczyglowski, K. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. The Plant Journal, 23(1), 97-114. doi:10.1046/j.1365-313x.2000.00799.x es_ES
dc.description.references Wu, X.-M., Yu, Y., Han, L.-B., Li, C.-L., Wang, H.-Y., Zhong, N.-Q., … Xia, G.-X. (2012). The Tobacco BLADE-ON-PETIOLE2 Gene Mediates Differentiation of the Corolla Abscission Zone by Controlling Longitudinal Cell Expansion. Plant Physiology, 159(2), 835-850. doi:10.1104/pp.112.193482 es_ES
dc.description.references Xu, M., Hu, T., McKim, S. M., Murmu, J., Haughn, G. W., & Hepworth, S. R. (2010). Arabidopsis BLADE-ON-PETIOLE1 and 2 promote floral meristem fate and determinacy in a previously undefined pathway targeting APETALA1 and AGAMOUS-LIKE24. The Plant Journal, 63(6), 974-989. doi:10.1111/j.1365-313x.2010.04299.x es_ES
dc.description.references Xu, C., Park, S. J., Van Eck, J., & Lippman, Z. B. (2016). Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes & Development, 30(18), 2048-2061. doi:10.1101/gad.288415.116 es_ES
dc.description.references Yaxley, J. (2001). Leaf and Flower Development in Pea (Pisum sativum L.): Mutants cochleata andunifoliata. Annals of Botany, 88(2), 225-234. doi:10.1006/anbo.2001.1448 es_ES
dc.description.references Žádníková, P., & Simon, R. (2014). How boundaries control plant development. Current Opinion in Plant Biology, 17, 116-125. doi:10.1016/j.pbi.2013.11.013 es_ES
dc.description.references Zhang, S., Sandal, N., Polowick, P. L., Stiller, J., Stougaard, J., & Fobert, P. R. (2003). Proliferating Floral Organs (Pfo ), a Lotus japonicus gene required for specifying floral meristem determinacy and organ identity, encodes an F-box protein. The Plant Journal, 33(4), 607-619. doi:10.1046/j.1365-313x.2003.01660.x es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem