51 research outputs found

    The essential role of NGATHA genes in style and stigma specification is widely conserved across eudicots

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    [EN] Carpel development and evolution are central issues for plant biology. The conservation of genetic functions conferring carpel identity has been widely studied in higher plants. However, although genetic networks directing the development of characteristic features of angiosperm carpels such as stigma and style are increasingly known in Arabidopsis thaliana, little information is available on the conservation and diversification of these networks in other species. Here, we have studied the functional conservation of NGATHA transcription factors in widely divergent species within the eudicots. We determined by in situ hybridization the expression patterns of NGATHA orthologs in Eschscholzia californica and Nicotiana benthamiana. Virus-induced gene silencing (VIGS)-mediated inactivation of NGATHA genes in both species was performed and different microscopy techniques were used for phenotypic characterization. We found the expression patterns of EcNGA and NbNGA genes during flower development to be highly similar to each other, as well as to those reported for Arabidopsis NGATHA genes. Inactivation of EcNGA and NbNGA also caused severe defects in style and stigma development in both species. These results demonstrate the widely conserved essential role of NGATHA genes in style and stigma specification and suggest that the angiosperm-specific NGATHA genes were likely recruited to direct a carpel-specific developmental program.This work was supported by the Spanish Ministerio de Ciencia e Innovacion (grant no. BIO2009-09920 to C. F.), the Spanish Ministerio de Economia y Competitividad (grant no. BIO2012-32902 to C. F.) and the Generalitat Valenciana (grant no. ACOMP/2012/099 and BEST/2009/054 to C. F.), We thank David Parejo and Victoria Palau (IBMCP) for glasshouse support, Marisol Gascon (IBMCP) for technical advice in microscopy, Amy Litt and Natalia Pabon-Mora (New York Botanical Gardens, Bronx, NY, USA) for providing VIGS plasmids and technical advice, and Barbara Ambrose (NYBG) for critical reading of the manuscript. E. californica germplasm used in this study was obtained from the National Genetic Resources Program (USA).Fourquin, C.; Ferrandiz Maestre, C. (2014). The essential role of NGATHA genes in style and stigma specification is widely conserved across eudicots. New Phytologist. 202(3):1001-1013. https://doi.org/10.1111/nph.12703S10011013202

    A cellular analysis of meristem activity at the end of flowering points to cytokinin as a major regulator of proliferative arrest in Arabidopsis

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    [EN] In monocarpic plants, all reproductive meristem activity arrests and flower production ceases after the production of a certain number of fruits. This proliferative arrest (PA) is an evolutionary adaptation that ensures nutrient availability for seed production. Moreover, PA is a process of agronomic interest because it affects the duration of the flowering period and therefore fruit production. While our knowledge of the inputs and genetic factors controlling the initiation of the flowering period is extensive, little is known about the regulatory pathways and cellular events that participate in the end of flowering and trigger PA. Here, we characterize with high spatiotemporal resolution the cellular and molecular changes related to cell proliferation and meristem activity in the shoot apical meristem throughout the flowering period and PA. Our results suggest that cytokinin (CK) signaling repression precedes PA and that this hormone is sufficient to prevent and revert the process. We have also observed that repression of known CK downstream factors, such as type B cyclins and WUSCHEL (WUS), correlates with PA. These molecular changes are accompanied by changes in cell size and number likely caused by the cessation of cell division and WUS activity during PA. Parallel assays in fruitfull (ful) mutants, which do not undergo PA, have revealed that FUL may promote PA via repression of these CK-dependent pathways. Moreover, our data allow to define two phases, based on the relative contribution of FUL, that lead to PA: an early reduction of CK-related events and a late blocking of these events.We thank Bruno Mudller and Venugopala Reddy for kindly providing the TCSn:GFP-ER and WUSpro:EGFP-WUS lines, respectively, as well as Vicente Balanza, Neha Bhatia, Antonio Serrano-Mislata, Concha Gomez-Mena, and Francisco Madueo for helpful feedback on the manuscript. P.M. acknowledges Fundacion General CSIC (ComFuturo program) for current funding. The laboratory of C.F. is supported by grants from Ministerio de Ciencia e In-novacion (RTI2018-099239-B-I00) and Generalitat Valenciana (PROMETEU/2019/004) .Merelo Cremades, P.; González-Cuadra, I.; Ferrandiz Maestre, C. (2022). A cellular analysis of meristem activity at the end of flowering points to cytokinin as a major regulator of proliferative arrest in Arabidopsis. Current Biology. 32(4):749-762. https://doi.org/10.1016/j.cub.2021.11.06974976232

    The Role of SHI/STY/SRS Genes in Organ Growth and Carpel Development Is Conserved in the Distant Eudicot Species Arabidopsis thaliana and Nicotiana benthamiana

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    [EN] Carpels are a distinctive feature of angiosperms, the ovule-bearing female reproductive organs that endow them with multiple selective advantages likely linked to the evolutionary success of flowering plants. Gene regulatory networks directing the development of carpel specialized tissues and patterning have been proposed based on genetic and molecular studies carried out in Arabidopsis thaliana. However, studies on the conservation/diversification of the elements and the topology of this network are still scarce. In this work, we have studied the functional conservation of transcription factors belonging to the SHI/STY/SRS family in two distant species within the eudicots, Eschscholzia californica and Nicotiana benthamiana. We have found that the expression patterns of EcSRS-L and NbSRS-L genes during flower development are similar to each other and to those reported for Arabidopsis SHI/STY/SRS genes. We have also characterized the phenotypic effects of NbSRS-L gene inactivation and overexpression in Nicotiana. Our results support the widely conserved role of SHI/STY/SRS genes at the top of the regulatory network directing style and stigma development, specialized tissues specific to the angiosperm carpels, at least within core eudicots, providing new insights on the possible evolutionary origin of the carpels.This work was supported by the Spanish MINECO/FEDER grants no BIO2012-32902 and BIO2015-64531-R to CFe. AG-F was supported by a predoctoral contract of the Generalitat Valenciana (ACIF/2013/044). We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Gomariz, A.; Sánchez-Gerschon, V.; Fourquin, C.; Ferrandiz Maestre, C. (2017). The Role of SHI/STY/SRS Genes in Organ Growth and Carpel Development Is Conserved in the Distant Eudicot Species Arabidopsis thaliana and Nicotiana benthamiana. Frontiers in Plant Science. 8:1-17. https://doi.org/10.3389/fpls.2017.00814S1178Alvarez, J. P., Goldshmidt, A., Efroni, I., Bowman, J. L., & Eshed, Y. (2009). The NGATHA Distal Organ Development Genes Are Essential for Style Specification in Arabidopsis. The Plant Cell, 21(5), 1373-1393. doi:10.1105/tpc.109.065482ALVAREZBUYLLA, E., BENITEZ, M., DAVILA, E., CHAOS, A., ESPINOSASOTO, C., & PADILLALONGORIA, P. (2007). Gene regulatory network models for plant development. Current Opinion in Plant Biology, 10(1), 83-91. doi:10.1016/j.pbi.2006.11.008Ballester, P., & Ferrándiz, C. (2017). Shattering fruits: variations on a dehiscent theme. Current Opinion in Plant Biology, 35, 68-75. doi:10.1016/j.pbi.2016.11.008Bombarely, A., Rosli, H. G., Vrebalov, J., Moffett, P., Mueller, L. A., & Martin, G. B. (2012). A Draft Genome Sequence of Nicotiana benthamiana to Enhance Molecular Plant-Microbe Biology Research. Molecular Plant-Microbe Interactions®, 25(12), 1523-1530. doi:10.1094/mpmi-06-12-0148-taBowman, J. L., Smyth, D. R., & Meyerowitz, E. M. (1989). Genes directing flower development in Arabidopsis. The Plant Cell, 1(1), 37-52. doi:10.1105/tpc.1.1.37Bradley, D., Carpenter, R., Sommer, H., Hartley, N., & Coen, E. (1993). Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of antirrhinum. Cell, 72(1), 85-95. doi:10.1016/0092-8674(93)90052-rChávez Montes, R. A., Herrera-Ubaldo, H., Serwatowska, J., & de Folter, S. (2015). Towards a comprehensive and dynamic gynoecium gene regulatory network. Current Plant Biology, 3-4, 3-12. doi:10.1016/j.cpb.2015.08.002Clemente, T. (s. f.). Nicotiana (Nicotiana tobaccum, Nicotiana benthamiana). Agrobacterium Protocols, 143-154. doi:10.1385/1-59745-130-4:143Clough, 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.xColombo, M., Brambilla, V., Marcheselli, R., Caporali, E., Kater, M. M., & Colombo, L. (2010). A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Developmental Biology, 337(2), 294-302. doi:10.1016/j.ydbio.2009.10.043Crawford, B. C. W., Ditta, G., & Yanofsky, M. F. (2007). The NTT Gene Is Required for Transmitting-Tract Development in Carpels of Arabidopsis thaliana. Current Biology, 17(13), 1101-1108. doi:10.1016/j.cub.2007.05.079Crawford, B. C. W., & Yanofsky, M. F. (2011). HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development, 138(14), 2999-3009. doi:10.1242/dev.067793Curtis, 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.103.027979Davidson, E. H., & Levine, M. S. (2008). Properties of developmental gene regulatory networks. Proceedings of the National Academy of Sciences, 105(51), 20063-20066. doi:10.1073/pnas.0806007105Davies, B., Motte, P., Keck, E., Saedler, H., Sommer, H., & Schwarz-Sommer, Z. (1999). PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. The EMBO Journal, 18(14), 4023-4034. doi:10.1093/emboj/18.14.4023Davila-Velderrain, J., Martinez-Garcia, J. C., & Alvarez-Buylla, E. R. (2016). Dynamic network modelling to understand flowering transition and floral patterning. Journal of Experimental Botany, 67(9), 2565-2572. doi:10.1093/jxb/erw123De Lucas, M., & Brady, S. M. (2013). Gene regulatory networks in the Arabidopsis root. Current Opinion in Plant Biology, 16(1), 50-55. doi:10.1016/j.pbi.2012.10.007Dreni, L., Pilatone, A., Yun, D., Erreni, S., Pajoro, A., Caporali, E., … Kater, M. M. (2011). Functional Analysis of All AGAMOUS Subfamily Members in Rice Reveals Their Roles in Reproductive Organ Identity Determination and Meristem Determinacy. The Plant Cell, 23(8), 2850-2863. doi:10.1105/tpc.111.087007Eklund, D. M., Cierlik, I., Ståldal, V., Claes, A. R., Vestman, D., Chandler, J., & Sundberg, E. (2011). Expression of Arabidopsis SHORT INTERNODES/STYLISH Family Genes in Auxin Biosynthesis Zones of Aerial Organs Is Dependent on a GCC Box-Like Regulatory Element. Plant Physiology, 157(4), 2069-2080. doi:10.1104/pp.111.182253Eklund, D. M., Ståldal, V., Valsecchi, I., Cierlik, I., Eriksson, C., Hiratsu, K., … Sundberg, E. (2010). The Arabidopsis thaliana STYLISH1 Protein Acts as a Transcriptional Activator Regulating Auxin Biosynthesis. The Plant Cell, 22(2), 349-363. doi:10.1105/tpc.108.064816Eklund, D. M., Thelander, M., Landberg, K., Staldal, V., Nilsson, A., Johansson, M., … Sundberg, E. (2010). Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens. Development, 137(8), 1275-1284. doi:10.1242/dev.039594Ferrándiz, C., & Fourquin, C. (2013). Role of the FUL–SHP network in the evolution of fruit morphology and function. Journal of Experimental Botany, 65(16), 4505-4513. doi:10.1093/jxb/ert479Fourquin, C., & Ferrándiz, C. (2012). Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots. The Plant Journal, 71(6), 990-1001. doi:10.1111/j.1365-313x.2012.05046.xFourquin, C., & Ferrándiz, C. (2014). The essential role of NGATHA genes in style and stigma specification is widely conserved across eudicots. New Phytologist, 202(3), 1001-1013. doi:10.1111/nph.12703Fourquin, C., Primo, A., Martínez-Fernández, I., Huet-Trujillo, E., & Ferrándiz, C. (2014). The CRC orthologue from Pisum sativum shows conserved functions in carpel morphogenesis and vascular development. Annals of Botany, 114(7), 1535-1544. doi:10.1093/aob/mcu129Fourquin, C., Vinauger-Douard, M., Chambrier, P., Berne-Dedieu, A., & Scutt, C. P. (2007). Functional Conservation between CRABS CLAW Orthologues from Widely Diverged Angiosperms. Annals of Botany, 100(3), 651-657. doi:10.1093/aob/mcm136Fourquin, C., Vinauger-Douard, M., Fogliani, B., Dumas, C., & Scutt, C. P. (2005). Evidence that CRABS CLAW and TOUSLED have conserved their roles in carpel development since the ancestor of the extant angiosperms. Proceedings of the National Academy of Sciences, 102(12), 4649-4654. doi:10.1073/pnas.0409577102Fridborg, I., Kuusk, S., Robertson, M., & Sundberg, E. (2001). The Arabidopsis Protein SHI Represses Gibberellin Responses in Arabidopsis and Barley. Plant Physiology, 127(3), 937-948. doi:10.1104/pp.010388Gremski, K., Ditta, G., & Yanofsky, M. F. (2007). The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development, 134(20), 3593-3601. doi:10.1242/dev.011510Heijmans, K., Ament, K., Rijpkema, A. S., Zethof, J., Wolters-Arts, M., Gerats, T., & Vandenbussche, M. (2012). Redefining C and D in the Petunia ABC. The Plant Cell, 24(6), 2305-2317. doi:10.1105/tpc.112.097030Ishikawa, M., Ohmori, Y., Tanaka, W., Hirabayashi, C., Murai, K., Ogihara, Y., … Hirano, H.-Y. (2009). The spatial expression patterns of DROOPING LEAF orthologs suggest a conserved function in grasses. Genes & Genetic Systems, 84(2), 137-146. doi:10.1266/ggs.84.137Islam, M. A., Lütken, H., Haugslien, S., Blystad, D.-R., Torre, S., Rolcik, J., … Clarke, J. L. (2013). Overexpression of the AtSHI Gene in Poinsettia, Euphorbia pulcherrima, Results in Compact Plants. PLoS ONE, 8(1), e53377. doi:10.1371/journal.pone.0053377Kim, S.-G., Lee, S., Kim, Y.-S., Yun, D.-J., Woo, J.-C., & Park, C.-M. (2010). Activation tagging of an Arabidopsis SHI-RELATED SEQUENCE gene produces abnormal anther dehiscence and floral development. Plant Molecular Biology, 74(4-5), 337-351. doi:10.1007/s11103-010-9677-5Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7), 1870-1874. doi:10.1093/molbev/msw054Kuusk, S., Sohlberg, J. J., Magnus Eklund, D., & Sundberg, E. (2006). Functionally redundantSHIfamily genes regulate Arabidopsis gynoecium development in a dose-dependent manner. The Plant Journal, 47(1), 99-111. doi:10.1111/j.1365-313x.2006.02774.xLarsson, E., Franks, R. G., & Sundberg, E. (2013). Auxin and the Arabidopsis thaliana gynoecium. Journal of Experimental Botany, 64(9), 2619-2627. doi:10.1093/jxb/ert099Larsson, E., Roberts, C. J., Claes, A. R., Franks, R. G., & Sundberg, E. (2014). Polar Auxin Transport Is Essential for Medial versus Lateral Tissue Specification and Vascular-Mediated Valve Outgrowth in Arabidopsis Gynoecia. Plant Physiology, 166(4), 1998-2012. doi:10.1104/pp.114.245951Lee, J.-Y. (2005). Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development, 132(22), 5021-5032. doi:10.1242/dev.02067Marsch-Martínez, N., & de Folter, S. (2016). Hormonal control of the development of the gynoecium. Current Opinion in Plant Biology, 29, 104-114. doi:10.1016/j.pbi.2015.12.006Martínez-Fernández, I., Sanchís, S., Marini, N., Balanzá, V., Ballester, P., Navarrete-Gómez, M., … Ferrándiz, C. (2014). The effect of NGATHA altered activity on auxin signaling pathways within the Arabidopsis gynoecium. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00210Morris, A. L., MacArthur, M. W., Hutchinson, E. G., & Thornton, J. M. (1992). Stereochemical quality of protein structure coordinates. Proteins: Structure, Function, and Genetics, 12(4), 345-364. doi:10.1002/prot.340120407Moubayidin, L., & Østergaard, L. (2014). Dynamic Control of Auxin Distribution Imposes a Bilateral-to-Radial Symmetry Switch during Gynoecium Development. Current Biology, 24(22), 2743-2748. doi:10.1016/j.cub.2014.09.080Ó’Maoiléidigh, D. S., Graciet, E., & Wellmer, F. (2013). Gene networks controllingArabidopsis thalianaflower development. New Phytologist, 201(1), 16-30. doi:10.1111/nph.12444Orashakova, S., Lange, M., Lange, S., Wege, S., & Becker, A. (2009). TheCRABS CLAWortholog from California poppy (Eschscholzia californica,Papaveraceae), EcCRC, is involved in floral meristem termination, gynoecium differentiation and ovule initiation. The Plant Journal, 58(4), 682-693. doi:10.1111/j.1365-313x.2009.03807.xPabón-Mora, N., Ambrose, B. A., & Litt, A. (2012). Poppy APETALA1/FRUITFULL Orthologs Control Flowering Time, Branching, Perianth Identity, and Fruit Development. Plant Physiology, 158(4), 1685-1704. doi:10.1104/pp.111.192104Pabón-Mora, N., Wong, G. K.-S., & Ambrose, B. A. (2014). Evolution of fruit development genes in flowering plants. Frontiers in Plant Science, 5. doi:10.3389/fpls.2014.00300Pan, I. L., McQuinn, R., Giovannoni, J. J., & Irish, V. F. (2010). Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. Journal of Experimental Botany, 61(6), 1795-1806. doi:10.1093/jxb/erq046Pfannebecker, K. C., Lange, M., Rupp, O., & Becker, A. (2016). An Evolutionary Framework for Carpel Developmental Control Genes. Molecular Biology and Evolution, msw229. doi:10.1093/molbev/msw229Pfannebecker, K. C., Lange, M., Rupp, O., & Becker, A. (2017). Seed plant specific gene lineages involved in carpel development. Molecular Biology and Evolution, msw297. doi:10.1093/molbev/msw297Ratcliff, F., Martin-Hernandez, A. M., & Baulcombe, D. C. (2008). Technical Advance: Tobacco rattle virus as a vector for analysis of gene function by silencing. The Plant Journal, 25(2), 237-245. doi:10.1046/j.0960-7412.2000.00942.xReyes-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.2013.08.002Sohlberg, J. J., Myrenås, M., Kuusk, S., Lagercrantz, U., Kowalczyk, M., Sandberg, G., & Sundberg, E. (2006). STY1regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. The Plant Journal, 47(1), 112-123. doi:10.1111/j.1365-313x.2006.02775.xStåldal, V., Cierlik, I., Chen, S., Landberg, K., Baylis, T., Myrenås, M., … Sundberg, E. (2012). The Arabidopsis thaliana transcriptional activator STYLISH1 regulates genes affecting stamen development, cell expansion and timing of flowering. Plant Molecular Biology, 78(6), 545-559. doi:10.1007/s11103-012-9888-zStåldal, V., Sohlberg, J. J., Eklund, D. M., Ljung, K., & Sundberg, E. (2008). Auxin can act independently ofCRC,LUG,SEU,SPTandSTY1in style development but not apical-basal patterning of theArabidopsisgynoecium. New Phytologist, 180(4), 798-808. doi:10.1111/j.1469-8137.2008.02625.xSundberg, E., & Ostergaard, L. (2009). Distinct and Dynamic Auxin Activities During Reproductive Development. Cold Spring Harbor Perspectives in Biology, 1(6), a001628-a001628. doi:10.1101/cshperspect.a001628Tian, C., & Jiao, Y. (2015). A systems approach to understand shoot branching. Current Plant Biology, 3-4, 13-19. doi:10.1016/j.cpb.2015.08.001Trigueros, M., Navarrete-Gómez, M., Sato, S., Christensen, S. K., Pelaz, S., Weigel, D., … Ferrándiz, C. (2009). The NGATHA Genes Direct Style Development in the Arabidopsis Gynoecium. The Plant Cell, 21(5), 1394-1409. doi:10.1105/tpc.109.065508Vialette-Guiraud, A. C. M., Andres-Robin, A., Chambrier, P., Tavares, R., & Scutt, C. P. (2016). The analysis of Gene Regulatory Networks in plant evo-devo. Journal of Experimental Botany, 67(9), 2549-2563. doi:10.1093/jxb/erw119Wege, S., Scholz, A., Gleissberg, S., & Becker, A. (2007). Highly Efficient Virus-induced Gene Silencing (VIGS) in California Poppy (Eschscholzia californica): An Evaluation of VIGS as a Strategy to Obtain Functional Data from Non-model Plants. Annals of Botany, 100(3), 641-649. doi:10.1093/aob/mcm118Yamada, T., Yokota, S., Hirayama, Y., Imaichi, R., Kato, M., & Gasser, C. S. (2011). Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. The Plant Journal, 67(1), 26-36. doi:10.1111/j.1365-313x.2011.04570.xYamaguchi, T., Nagasawa, N., Kawasaki, S., Matsuoka, M., Nagato, Y., & Hirano, H.-Y. (2004). The YABBY Gene DROOPING LEAF Regulates Carpel Specification and Midrib Development in Oryza sativa. The Plant Cell, 16(2), 500-509. doi:10.1105/tpc.018044Yellina, A. L., Orashakova, S., Lange, S., Erdmann, R., Leebens-Mack, J., & Becker, A. (2010). Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). EvoDevo, 1(1), 13. doi:10.1186/2041-9139-1-13Youssef, H. M., Eggert, K., Koppolu, R., Alqudah, A. M., Poursarebani, N., Fazeli, A., … Schnurbusch, T. (2016). VRS2 regulates hormone-mediated inflorescence patterning in barley. Nature Genetics, 49(1), 157-161. doi:10.1038/ng.3717Yuo, T., Yamashita, Y., Kanamori, H., Matsumoto, T., Lundqvist, U., Sato, K., … Taketa, S. (2012). A SHORT INTERNODES (SHI) family transcription factor gene regulates awn elongation and pistil morphology in barley. Journal of Experimental Botany, 63(14), 5223-5232. doi:10.1093/jxb/ers182Zawaski, C., Kadmiel, M., Ma, C., Gai, Y., Jiang, X., Strauss, S. H., & Busov, V. B. (2011). SHORT INTERNODES-like genes regulate shoot growth and xylem proliferation in Populus. New Phytologist, 191(3), 678-691. doi:10.1111/j.1469-8137.2011.03742.

    Intraspecific variation in digit reduction in Testudo : the case of the Hermann's tortoise

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    Phalangeal reduction is a common and widespread phenomenon among tortoises that has been associated with the adaptation to terrestrial life. While reduced manual digit 1 appears characteristic in almost all Testudo species, it is uncertain why the metacarpal I and distal carpal of the same digit are completely missing in some individuals of Hermann's tortoise (Testudo hermanni hermanni). To clarify this issue, we investigated the number of manual claws in six populations of Hermann's tortoise (one from the Ebro Delta in the Iberian Peninsula and five from Minorca Island), their age, sex, genetic lineage, and the substrate type that they inhabit. The number of claws was ascertained based on direct counts (n > 1500 individuals) and by X-rays (n = 32 individuals), obtaining three different phalangeal formulae: (1-2-2-2-1, D-2-2-2-1, 0-2-2-2-1). Thus, claw counts through both methodologies (direct count and X-ray) further confirm that the observed claws serve as a good proxy to assess the actual number of digits. Our results show no loss of phalanges, metacarpal and carpal bones in digit 1 associated with age, sex, or substrate, contrary to some previous authors who hypothesized a relationship between this loss and sexual dimorphism. Therefore, variations in the number of manual digits and the loss of metacarpal I and distal carpal in digit 1 in Hermann's tortoise are related to population and genetic lineage. More detailed comparisons with other Testudo hermanni populations from elsewhere in Europe would be required to understand the evolutionary significance concerning the intrapopulation variability in the number of digits remaining

    A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus

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    [EN] Angiosperms are the most diverse and numerous group of plants, and it is generally accepted that this evolutionary success owes in part to the diversity found in fruits, key for protecting the developing seeds and ensuring seed dispersal. Although studies on the molecular basis of morphological innovations are few, they all illustrate the central role played by transcription factors acting as developmental regulators. Here, we show that a small change in the protein sequence of a MADS-box transcription factor correlates with the origin of a highly modified fruit morphology and the change in seed dispersal strategies that occurred in Medicago, a genus belonging to the large legume family. This protein sequence modification alters the functional properties of the protein, affecting the affinities for other protein partners involved in high-order complexes. Our work illustrates that variation in coding regions can generate evolutionary novelties not based on gene duplication/subfunctionalization but by interactions in complex networks, contributing also to the current debate on the relative importance of changes in regulatory or coding regions of master regulators in generating morphological novelties.This work was supported by the Spanish Ministerio de Ciencia e Innovacion (grant no. BIO2009-09920 to C.Fe.), the European Union (grant no. FP7-PEOPLE-PIRSES-2009-247589 to C.Fe. and A.C.d.O.), and a Fellowship for Foreign Young Postdocs from the Spanish Ministerio de Ciencia e Innovacion (to C.Fo.).Fourquin, C.; Del Cerro Fernández, C.; Victoria, FC.; Vialette-Guiraud, A.; De Oliveira, AC.; Ferrandiz Maestre, C. (2013). A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus. Plant Physiology. 162(2):907-917. https://doi.org/10.1104/pp.113.217570S907917162

    Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia

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    [EN] Controlled spatiotemporal cell division and expansion are responsible for floral bilateral symmetry. Genetic studies have pointed to class II TCP genes as major regulators of cell division and floral patterning in model core eudicots. Here we study their evolution in perianth-bearing Piperales and their expression in Aristolochia, a rare occurrence of bilateral perianth outside eudicots and monocots. The evolution of class II TCP genes reveals single-copy CYCLOIDEA-like genes and three paralogs of CINCINNATA (CIN) in early diverging angiosperms. All class II TCP genes have independently duplicated in Aristolochia subgenus Siphisia. Also CIN2 genes duplicated before the diversification of Saruma and Asarum. Sequence analysis shows that CIN1 and CIN3 share motifs with Cyclin proteins and CIN2 genes have lost the miRNA319a binding site. Expression analyses of all paralogs of class II TCP genes in Aristolochia fimbriata point to a role of CYC and CIN genes in maintaining differential perianth expansion during mid- and late flower developmental stages by promoting cell division in the distal and ventral portion of the limb. It is likely that class II TCP genes also contribute to cell division in the leaf, the gynoecium and the ovules in A. fimbriata.We thank Anny Garces Palacio, Sarita Munoz, Pablo Perez-Mesa (Universidad de Antioquia, Colombia), Cecilia Zumajo-Cardona (The New York Botanical Garden), Ana Berbel and Clara Ines Ortiz-Ramirez (Instituto de Biologia Molecular y Celular de Plantas, CSIC-UVP, Valencia, Spain) for photographs and assistance during laboratory work. We also thank Sebastian Gonzalez (Massachusetts College of Art and Design) for taking some of the photographs in Figs 1 and 2. Thanks are also due to the Dresden Junior Fellowship for allowing the visiting professor fellowship of NPM to the Technishe Universitat Dresden during 2019. This research was funded by Estrategia de Sostenibilidad 2018-2019 the Convocatoria Programaticas 2017-2018 (code 2017-16302), and the 2018-2019 Fondo de Internacionalizacion (code 201926230) from the Universidad de Antioquia, the iCOOP + 2016 grant COOPB20250 from Centro Superior de Investigacion Cientifica, CSIC and the ExpoSEED (H2020.MSCA-RISE2015-691109) EU grant.Pabon-Mora, N.; Madrigal, Y.; Alzate, JF.; Ambrose, BA.; Ferrandiz Maestre, C.; Wanke, S.; Neinhuis, C.... (2020). Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia. New Phytologist. 228(2):752-769. https://doi.org/10.1111/nph.167197527692282Aguilar-Martínez, J. A., Poza-Carrión, C., & Cubas, P. (2007). Arabidopsis BRANCHED1Acts as an Integrator of Branching Signals within Axillary Buds. The Plant Cell, 19(2), 458-472. doi:10.1105/tpc.106.048934Almeida, J., Rocheta, M., & Galego, L. (1997). Genetic control of flower shape in Antirrhinum majus. Development, 124(7), 1387-1392. doi:10.1242/dev.124.7.1387Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. doi:10.1016/s0022-2836(05)80360-2Ambrose, B. A., Lerner, D. R., Ciceri, P., Padilla, C. M., Yanofsky, M. F., & Schmidt, R. J. (2000). Molecular and Genetic Analyses of the Silky1 Gene Reveal Conservation in Floral Organ Specification between Eudicots and Monocots. Molecular Cell, 5(3), 569-579. doi:10.1016/s1097-2765(00)80450-5Ballester, P., Navarrete-Gómez, M., Carbonero, P., Oñate-Sánchez, L., & Ferrándiz, C. (2015). Leaf expansion in Arabidopsis is controlled by a TCP-NGA regulatory module likely conserved in distantly related species. Physiologia Plantarum, 155(1), 21-32. doi:10.1111/ppl.12327Bartlett, M. E., & Specht, C. D. (2011). Changes in expression pattern of the teosinte branched1- like genes in the Zingiberales provide a mechanism for evolutionary shifts in symmetry across the order. American Journal of Botany, 98(2), 227-243. doi:10.3732/ajb.1000246Bliss, B. J., Wanke, S., Barakat, A., Ayyampalayam, S., Wickett, N., Wall, P. K., … dePamphilis, C. W. (2013). Characterization of the basal angiosperm Aristolochia fimbriata: a potential experimental system for genetic studies. BMC Plant Biology, 13(1), 13. doi:10.1186/1471-2229-13-13Busch, A., & Zachgo, S. (2007). Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proceedings of the National Academy of Sciences, 104(42), 16714-16719. doi:10.1073/pnas.0705338104Citerne, H. L., Reyes, E., Le Guilloux, M., Delannoy, E., Simonnet, F., Sauquet, H., … Damerval, C. (2016). Characterization ofCYCLOIDEA-like genes in Proteaceae, a basal eudicot family with multiple shifts in floral symmetry. Annals of Botany, 119(3), 367-378. doi:10.1093/aob/mcw219Corley, S. B., Carpenter, R., Copsey, L., & Coen, E. (2005). Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proceedings of the National Academy of Sciences, 102(14), 5068-5073. doi:10.1073/pnas.0501340102Crawford, B. C. W., Nath, U., Carpenter, R., & Coen, E. S. (2004). CINCINNATA Controls Both Cell Differentiation and Growth in Petal Lobes and Leaves of Antirrhinum. Plant Physiology, 135(1), 244-253. doi:10.1104/pp.103.036368Cubas, P. (2002). Role of TCP genes in the evolution of morphological characters in angiosperms. Developmental Genetics and Plant Evolution, 247-266. doi:10.1201/9781420024982.ch13Cubas, 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.xDamerval, C., Citerne, H., Conde e Silva, N., Deveaux, Y., Delannoy, E., Joets, J., … Nadot, S. (2019). Unraveling the Developmental and Genetic Mechanisms Underpinning Floral Architecture in Proteaceae. Frontiers in Plant Science, 10. doi:10.3389/fpls.2019.00018Damerval, C., Citerne, H., Le Guilloux, M., Domenichini, S., Dutheil, J., Ronse de Craene, L., & Nadot, S. (2013). Asymmetric morphogenetic cues along the transverse plane: Shift from disymmetry to zygomorphy in the flower of Fumarioideae. American Journal of Botany, 100(2), 391-402. doi:10.3732/ajb.1200376Damerval, C., Guilloux, M. L., Jager, M., & Charon, C. (2006). Diversity and Evolution ofCYCLOIDEA-Like TCP Genes in Relation to Flower Development in Papaveraceae. Plant Physiology, 143(2), 759-772. doi:10.1104/pp.106.090324Danisman, S., van der Wal, F., Dhondt, S., Waites, R., de Folter, S., Bimbo, A., … Immink, R. G. H. (2012). Arabidopsis Class I and Class II TCP Transcription Factors Regulate Jasmonic Acid Metabolism and Leaf Development Antagonistically. Plant Physiology, 159(4), 1511-1523. doi:10.1104/pp.112.200303Danisman, S., van Dijk, A. D. J., Bimbo, A., van der Wal, F., Hennig, L., de Folter, S., … Immink, R. G. H. (2013). Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. Journal of Experimental Botany, 64(18), 5673-5685. doi:10.1093/jxb/ert337Doebley, J. (2004). The Genetics of Maize Evolution. Annual Review of Genetics, 38(1), 37-59. doi:10.1146/annurev.genet.38.072902.092425Doebley, J., Stec, A., & Gustus, C. (1995). teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics, 141(1), 333-346. doi:10.1093/genetics/141.1.333Doebley, J., Stec, A., & Hubbard, L. (1997). The evolution of apical dominance in maize. Nature, 386(6624), 485-488. doi:10.1038/386485a0Efroni, I., Blum, E., Goldshmidt, A., & Eshed, Y. (2008). A Protracted and Dynamic Maturation Schedule UnderliesArabidopsisLeaf Development. The Plant Cell, 20(9), 2293-2306. doi:10.1105/tpc.107.057521Elomaa, P., Zhao, Y., & Zhang, T. (2018). Flower heads in Asteraceae—recruitment of conserved developmental regulators to control the flower-like inflorescence architecture. Horticulture Research, 5(1). doi:10.1038/s41438-018-0056-8Endress, P. K. (2012). The Immense Diversity of Floral Monosymmetry and Asymmetry Across Angiosperms. The Botanical Review, 78(4), 345-397. doi:10.1007/s12229-012-9106-3Ferrándiz, C., Liljegren, S. J., & Yanofsky, M. F. (2000). Negative Regulation of the SHATTERPROOF Genes by FRUITFULL During Arabidopsis Fruit Development. Science, 289(5478), 436-438. doi:10.1126/science.289.5478.436Galego, L. (2002). Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes & Development, 16(7), 880-891. doi:10.1101/gad.221002Gaudin, V., Lunness, P. A., Fobert, P. R., Towers, M., Riou-Khamlichi, C., Murray, J. A. H., … Doonan, J. H. (2000). The Expression of D-Cyclin Genes Defines Distinct Developmental Zones in Snapdragon Apical Meristems and Is Locally Regulated by the Cycloidea Gene. Plant Physiology, 122(4), 1137-1148. doi:10.1104/pp.122.4.1137González, F., & Pabón‐Mora, N. (2015). Trickery flowers: the extraordinary chemical mimicry of Aristolochia to accomplish deception to its pollinators. New Phytologist, 206(1), 10-13. doi:10.1111/nph.13328González, F., & Stevenson, D. W. (2000). Perianth development and systematics of Aristolochia. Flora, 195(4), 370-391. doi:10.1016/s0367-2530(17)30995-7Heery, D. M., Kalkhoven, E., Hoare, S., & Parker, M. G. (1997). A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature, 387(6634), 733-736. doi:10.1038/42750Hileman, L. C. (2014). Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1648), 20130348. doi:10.1098/rstb.2013.0348Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q., & Vinh, L. S. (2017). UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35(2), 518-522. doi:10.1093/molbev/msx281Horn, S., Pabón-Mora, N., Theuß, V. S., Busch, A., & Zachgo, S. (2015). Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids. The Plant Journal, 81(4), 559-571. doi:10.1111/tpj.12750Howarth, D. G., & Donoghue, M. J. (2006). Phylogenetic analysis of the «ECE» (CYC/TB1) clade reveals duplications predating the core eudicots. Proceedings of the National Academy of Sciences, 103(24), 9101-9106. doi:10.1073/pnas.0602827103Howarth, D. G., Martins, T., Chimney, E., & Donoghue, M. J. (2011). Diversification of CYCLOIDEA expression in the evolution of bilateral flower symmetry in Caprifoliaceae and Lonicera (Dipsacales). Annals of Botany, 107(9), 1521-1532. doi:10.1093/aob/mcr049Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587-589. doi:10.1038/nmeth.4285Katoh, K. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059-3066. doi:10.1093/nar/gkf436Kosugi, S., & Ohashi, Y. (2002). DNA binding and dimerization specificity and potential targets for the TCP protein family. The Plant Journal, 30(3), 337-348. doi:10.1046/j.1365-313x.2002.01294.xKoyama, T., Furutani, M., Tasaka, M., & Ohme-Takagi, M. (2006). TCP Transcription Factors Control the Morphology of Shoot Lateral Organs via Negative Regulation of the Expression of Boundary-Specific Genes inArabidopsis. The Plant Cell, 19(2), 473-484. doi:10.1105/tpc.106.044792Leppik, E. E. (1972). Origin and Evolution of Bilateral Symmetry in Flowers. Evolutionary Biology, 49-85. doi:10.1007/978-1-4757-0256-9_3Li, C., Potuschak, T., Colon-Carmona, A., Gutierrez, R. A., & Doerner, P. (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proceedings of the National Academy of Sciences, 102(36), 12978-12983. doi:10.1073/pnas.0504039102Li, M., Zhang, D., Gao, Q., Luo, Y., Zhang, H., Ma, B., … Xue, Y. (2019). Genome structure and evolution of Antirrhinum majus L. Nature Plants, 5(2), 174-183. doi:10.1038/s41477-018-0349-9Li, S. (2015). The Arabidopsis thaliana TCP transcription factors: A broadening horizon beyond development. Plant Signaling & Behavior, 10(7), e1044192. doi:10.1080/15592324.2015.1044192Li, S., Gutsche, N., & Zachgo, S. (2011). The ROXY1 C-Terminal L**LL Motif Is Essential for the Interaction with TGA Transcription Factors    . Plant Physiology, 157(4), 2056-2068. doi:10.1104/pp.111.185199Lin, Y.-F., Chen, Y.-Y., Hsiao, Y.-Y., Shen, C.-Y., Hsu, J.-L., Yeh, C.-M., … Tsai, W.-C. (2016). Genome-wide identification and characterization ofTCPgenes involved in ovule development ofPhalaenopsis equestris. Journal of Experimental Botany, 67(17), 5051-5066. doi:10.1093/jxb/erw273Da Luo, Carpenter, R., Copsey, L., Vincent, C., Clark, J., & Coen, E. (1999). Control of Organ Asymmetry in Flowers of Antirrhinum. Cell, 99(4), 367-376. doi:10.1016/s0092-8674(00)81523-8Luo, D., Carpenter, R., Vincent, C., Copsey, L., & Coen, E. (1996). Origin of floral asymmetry in Antirrhinum. Nature, 383(6603), 794-799. doi:10.1038/383794a0Madrigal, Y., Alzate, J. F., & Pabón-Mora, N. (2017). Evolution and Expression Patterns of TCP Genes in Asparagales. Frontiers in Plant Science, 8. doi:10.3389/fpls.2017.00009Martín-Trillo, M., & Cubas, P. (2010). TCP genes: a family snapshot ten years later. Trends in Plant Science, 15(1), 31-39. doi:10.1016/j.tplants.2009.11.003MillerMA PfeifferW SchwartzT.2010.Creating the CIPRES Science Gateway for inference of large phylogenetic trees. [WWW document] URLhttp://www.phylo.org[accessed 5 June 2020].Mondragón-Palomino, M., & Trontin, C. (2011). High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots. Annals of Botany, 107(9), 1533-1544. doi:10.1093/aob/mcr059Nath, U., Crawford, B. C. W., Carpenter, R., & Coen, E. (2003). Genetic Control of Surface Curvature. Science, 299(5611), 1404-1407. doi:10.1126/science.1079354Navaud, O., Dabos, P., Carnus, E., Tremousaygue, D., & Hervé, C. (2007). TCP Transcription Factors Predate the Emergence of Land Plants. Journal of Molecular Evolution, 65(1), 23-33. doi:10.1007/s00239-006-0174-zNguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2014). IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution, 32(1), 268-274. doi:10.1093/molbev/msu300Pabón-Mora, N., Suárez-Baron, H., Ambrose, B. A., & González, F. (2015). Flower Development and Perianth Identity Candidate Genes in the Basal Angiosperm Aristolochia fimbriata (Piperales: Aristolochiaceae). Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01095Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C., & Weigel, D. (2003). Control of leaf morphogenesis by microRNAs. Nature, 425(6955), 257-263. doi:10.1038/nature01958Parapunova, 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). doi:10.1186/1471-2229-14-157Peréz-Mesa, P., Ortíz-Ramírez, C. I., González, F., Ferrándiz, C., & Pabón-Mora, N. (2020). Expression of gynoecium patterning transcription factors in Aristolochia fimbriata (Aristolochiaceae) and their contribution to gynostemium development. EvoDevo, 11(1). doi:10.1186/s13227-020-00149-8Preston, J. C., & Hileman, L. C. (2012). Parallel evolution of TCP and B-class genes in Commelinaceae flower bilateral symmetry. EvoDevo, 3(1), 6. doi:10.1186/2041-9139-3-6Preston, J. C., Kost, M. A., & Hileman, L. C. (2009). Conservation and diversification of the symmetry developmental program among close relatives of snapdragon with divergent floral morphologies. New Phytologist, 182(3), 751-762. doi:10.1111/j.1469-8137.2009.02794.xRambautA.2014.FigTree: tree figure drawing tool. [WWW document] URLhttp://tree.bio.ed.ac.uk/software/figtree/.Rudall, P. J., & Bateman, R. M. (2004). Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytologist, 162(1), 25-44. doi:10.1111/j.1469-8137.2004.01032.xSargent, R. D. (2004). Floral symmetry affects speciation rates in angiosperms. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(1539), 603-608. doi:10.1098/rspb.2003.2644Suárez-Baron, H., Alzate, J. F., González, F., Ambrose, B. A., & Pabón-Mora, N. (2019). Genetic mechanisms underlying perianth epidermal elaboration of Aristolochia ringens Vahl (Aristolochiaceae). Flora, 253, 56-66. doi:10.1016/j.flora.2019.03.004Suárez-Baron, H., Pérez-Mesa, P., Ambrose, B. A., González, F., & Pabón-Mora, N. (2016). Deep into the Aristolochia Flower: Expression of C, D, and E-Class Genes inAristolochia fimbriata(Aristolochiaceae). Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 328(1-2), 55-71. doi:10.1002/jez.b.22686Viola, I. L., Uberti Manassero, N. G., Ripoll, R., & Gonzalez, D. H. (2011). The Arabidopsis class I TCP transcription factor AtTCP11 is a developmental regulator with distinct DNA-binding properties due to the presence of a threonine residue at position 15 of the TCP domain. Biochemical Journal, 435(1), 143-155. doi:10.1042/bj20101019Wang, J., Wang, Y., & Luo, D. (2010). LjCYC Genes Constitute Floral Dorsoventral Asymmetry in Lotus japonicus. Journal of Integrative Plant Biology, 52(11), 959-970. doi:10.1111/j.1744-7909.2010.00926.xYuan, Z., Gao, S., Xue, D.-W., Luo, D., Li, L.-T., Ding, S.-Y., … Zhang, D.-B. (2008). RETARDED PALEA1 Controls Palea Development and Floral Zygomorphy in Rice  . Plant Physiology, 149(1), 235-244. doi:10.1104/pp.108.128231Zhang, W., Kramer, E. M., & Davis, C. C. (2010). Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proceedings of the National Academy of Sciences, 107(14), 6388-6393. doi:10.1073/pnas.0910155107Zhang, W., Steinmann, V. W., Nikolov, L., Kramer, E. M., & Davis, C. C. (2013). Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors. Frontiers in Plant Science, 4. doi:10.3389/fpls.2013.0030

    Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia

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    [EN] Controlled spatiotemporal cell division and expansion are responsible for floral bilateral symmetry. Genetic studies have pointed to class II TCP genes as major regulators of cell division and floral patterning in model core eudicots. Here we study their evolution in perianth-bearing Piperales and their expression in Aristolochia, a rare occurrence of bilateral perianth outside eudicots and monocots. The evolution of class II TCP genes reveals single-copy CYCLOIDEA-like genes and three paralogs of CINCINNATA (CIN) in early diverging angiosperms. All class II TCP genes have independently duplicated in Aristolochia subgenus Siphisia. Also CIN2 genes duplicated before the diversification of Saruma and Asarum. Sequence analysis shows that CIN1 and CIN3 share motifs with Cyclin proteins and CIN2 genes have lost the miRNA319a binding site. Expression analyses of all paralogs of class II TCP genes in Aristolochia fimbriata point to a role of CYC and CIN genes in maintaining differential perianth expansion during mid- and late flower developmental stages by promoting cell division in the distal and ventral portion of the limb. It is likely that class II TCP genes also contribute to cell division in the leaf, the gynoecium and the ovules in A. fimbriata.We thank Anny Garces Palacio, Sarita Munoz, Pablo Perez-Mesa (Universidad de Antioquia, Colombia), Cecilia Zumajo-Cardona (The New York Botanical Garden), Ana Berbel and Clara Ines Ortiz-Ramirez (Instituto de Biologia Molecular y Celular de Plantas, CSIC-UVP, Valencia, Spain) for photographs and assistance during laboratory work. We also thank Sebastian Gonzalez (Massachusetts College of Art and Design) for taking some of the photographs in Figs 1 and 2. Thanks are also due to the Dresden Junior Fellowship for allowing the visiting professor fellowship of NPM to the Technishe Universitat Dresden during 2019. This research was funded by Estrategia de Sostenibilidad 2018-2019 the Convocatoria Programaticas 2017-2018 (code 2017-16302), and the 2018-2019 Fondo de Internacionalizacion (code 201926230) from the Universidad de Antioquia, the iCOOP + 2016 grant COOPB20250 from Centro Superior de Investigacion Cientifica, CSIC and the ExpoSEED (H2020.MSCA-RISE2015-691109) EU grant.Pabon-Mora, N.; Madrigal, Y.; Alzate, JF.; Ambrose, BA.; Ferrandiz Maestre, C.; Wanke, S.; Neinhuis, C.... (2020). Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia. New Phytologist. 228(2):752-769. https://doi.org/10.1111/nph.16719S7527692282Aguilar-Martínez, J. A., Poza-Carrión, C., & Cubas, P. (2007). Arabidopsis BRANCHED1Acts as an Integrator of Branching Signals within Axillary Buds. The Plant Cell, 19(2), 458-472. doi:10.1105/tpc.106.048934Almeida, J., Rocheta, M., & Galego, L. (1997). Genetic control of flower shape in Antirrhinum majus. Development, 124(7), 1387-1392. doi:10.1242/dev.124.7.1387Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. doi:10.1016/s0022-2836(05)80360-2Ambrose, B. A., Lerner, D. R., Ciceri, P., Padilla, C. M., Yanofsky, M. F., & Schmidt, R. J. (2000). Molecular and Genetic Analyses of the Silky1 Gene Reveal Conservation in Floral Organ Specification between Eudicots and Monocots. Molecular Cell, 5(3), 569-579. doi:10.1016/s1097-2765(00)80450-5Ballester, P., Navarrete-Gómez, M., Carbonero, P., Oñate-Sánchez, L., & Ferrándiz, C. (2015). Leaf expansion in Arabidopsis is controlled by a TCP-NGA regulatory module likely conserved in distantly related species. Physiologia Plantarum, 155(1), 21-32. doi:10.1111/ppl.12327Bartlett, M. E., & Specht, C. D. (2011). Changes in expression pattern of the teosinte branched1- like genes in the Zingiberales provide a mechanism for evolutionary shifts in symmetry across the order. American Journal of Botany, 98(2), 227-243. doi:10.3732/ajb.1000246Bliss, B. J., Wanke, S., Barakat, A., Ayyampalayam, S., Wickett, N., Wall, P. K., … dePamphilis, C. W. (2013). Characterization of the basal angiosperm Aristolochia fimbriata: a potential experimental system for genetic studies. BMC Plant Biology, 13(1), 13. doi:10.1186/1471-2229-13-13Busch, A., & Zachgo, S. (2007). Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proceedings of the National Academy of Sciences, 104(42), 16714-16719. doi:10.1073/pnas.0705338104Citerne, H. L., Reyes, E., Le Guilloux, M., Delannoy, E., Simonnet, F., Sauquet, H., … Damerval, C. (2016). Characterization ofCYCLOIDEA-like genes in Proteaceae, a basal eudicot family with multiple shifts in floral symmetry. Annals of Botany, 119(3), 367-378. doi:10.1093/aob/mcw219Corley, S. B., Carpenter, R., Copsey, L., & Coen, E. (2005). Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proceedings of the National Academy of Sciences, 102(14), 5068-5073. doi:10.1073/pnas.0501340102Crawford, B. C. W., Nath, U., Carpenter, R., & Coen, E. S. (2004). CINCINNATA Controls Both Cell Differentiation and Growth in Petal Lobes and Leaves of Antirrhinum. Plant Physiology, 135(1), 244-253. doi:10.1104/pp.103.036368Cubas, P. (2002). Role of TCP genes in the evolution of morphological characters in angiosperms. Developmental Genetics and Plant Evolution, 247-266. doi:10.1201/9781420024982.ch13Cubas, 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.xDamerval, C., Citerne, H., Conde e Silva, N., Deveaux, Y., Delannoy, E., Joets, J., … Nadot, S. (2019). Unraveling the Developmental and Genetic Mechanisms Underpinning Floral Architecture in Proteaceae. Frontiers in Plant Science, 10. doi:10.3389/fpls.2019.00018Damerval, C., Citerne, H., Le Guilloux, M., Domenichini, S., Dutheil, J., Ronse de Craene, L., & Nadot, S. (2013). Asymmetric morphogenetic cues along the transverse plane: Shift from disymmetry to zygomorphy in the flower of Fumarioideae. American Journal of Botany, 100(2), 391-402. doi:10.3732/ajb.1200376Damerval, C., Guilloux, M. L., Jager, M., & Charon, C. (2006). Diversity and Evolution ofCYCLOIDEA-Like TCP Genes in Relation to Flower Development in Papaveraceae. Plant Physiology, 143(2), 759-772. doi:10.1104/pp.106.090324Danisman, S., van der Wal, F., Dhondt, S., Waites, R., de Folter, S., Bimbo, A., … Immink, R. G. H. (2012). Arabidopsis Class I and Class II TCP Transcription Factors Regulate Jasmonic Acid Metabolism and Leaf Development Antagonistically. Plant Physiology, 159(4), 1511-1523. doi:10.1104/pp.112.200303Danisman, S., van Dijk, A. D. J., Bimbo, A., van der Wal, F., Hennig, L., de Folter, S., … Immink, R. G. H. (2013). Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. Journal of Experimental Botany, 64(18), 5673-5685. doi:10.1093/jxb/ert337Doebley, J. (2004). The Genetics of Maize Evolution. Annual Review of Genetics, 38(1), 37-59. doi:10.1146/annurev.genet.38.072902.092425Doebley, J., Stec, A., & Gustus, C. (1995). teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics, 141(1), 333-346. doi:10.1093/genetics/141.1.333Doebley, J., Stec, A., & Hubbard, L. (1997). The evolution of apical dominance in maize. Nature, 386(6624), 485-488. doi:10.1038/386485a0Efroni, I., Blum, E., Goldshmidt, A., & Eshed, Y. (2008). A Protracted and Dynamic Maturation Schedule UnderliesArabidopsisLeaf Development. The Plant Cell, 20(9), 2293-2306. doi:10.1105/tpc.107.057521Elomaa, P., Zhao, Y., & Zhang, T. (2018). Flower heads in Asteraceae—recruitment of conserved developmental regulators to control the flower-like inflorescence architecture. Horticulture Research, 5(1). doi:10.1038/s41438-018-0056-8Endress, P. K. (2012). The Immense Diversity of Floral Monosymmetry and Asymmetry Across Angiosperms. The Botanical Review, 78(4), 345-397. doi:10.1007/s12229-012-9106-3Ferrándiz, C., Liljegren, S. J., & Yanofsky, M. F. (2000). Negative Regulation of the SHATTERPROOF Genes by FRUITFULL During Arabidopsis Fruit Development. Science, 289(5478), 436-438. doi:10.1126/science.289.5478.436Galego, L. (2002). Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes & Development, 16(7), 880-891. doi:10.1101/gad.221002Gaudin, V., Lunness, P. A., Fobert, P. R., Towers, M., Riou-Khamlichi, C., Murray, J. A. H., … Doonan, J. H. (2000). The Expression of D-Cyclin Genes Defines Distinct Developmental Zones in Snapdragon Apical Meristems and Is Locally Regulated by the Cycloidea Gene. Plant Physiology, 122(4), 1137-1148. doi:10.1104/pp.122.4.1137González, F., & Pabón‐Mora, N. (2015). Trickery flowers: the extraordinary chemical mimicry of Aristolochia to accomplish deception to its pollinators. New Phytologist, 206(1), 10-13. doi:10.1111/nph.13328González, F., & Stevenson, D. W. (2000). Perianth development and systematics of Aristolochia. Flora, 195(4), 370-391. doi:10.1016/s0367-2530(17)30995-7Heery, D. M., Kalkhoven, E., Hoare, S., & Parker, M. G. (1997). A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature, 387(6634), 733-736. doi:10.1038/42750Hileman, L. C. (2014). Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1648), 20130348. doi:10.1098/rstb.2013.0348Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q., & Vinh, L. S. (2017). UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35(2), 518-522. doi:10.1093/molbev/msx281Horn, S., Pabón-Mora, N., Theuß, V. S., Busch, A., & Zachgo, S. (2015). Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids. The Plant Journal, 81(4), 559-571. doi:10.1111/tpj.12750Howarth, D. G., & Donoghue, M. J. (2006). Phylogenetic analysis of the «ECE» (CYC/TB1) clade reveals duplications predating the core eudicots. Proceedings of the National Academy of Sciences, 103(24), 9101-9106. doi:10.1073/pnas.0602827103Howarth, D. G., Martins, T., Chimney, E., & Donoghue, M. J. (2011). Diversification of CYCLOIDEA expression in the evolution of bilateral flower symmetry in Caprifoliaceae and Lonicera (Dipsacales). Annals of Botany, 107(9), 1521-1532. doi:10.1093/aob/mcr049Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587-589. doi:10.1038/nmeth.4285Katoh, K. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059-3066. doi:10.1093/nar/gkf436Kosugi, S., & Ohashi, Y. (2002). DNA binding and dimerization specificity and potential targets for the TCP protein family. The Plant Journal, 30(3), 337-348. doi:10.1046/j.1365-313x.2002.01294.xKoyama, T., Furutani, M., Tasaka, M., & Ohme-Takagi, M. (2006). TCP Transcription Factors Control the Morphology of Shoot Lateral Organs via Negative Regulation of the Expression of Boundary-Specific Genes inArabidopsis. The Plant Cell, 19(2), 473-484. doi:10.1105/tpc.106.044792Leppik, E. E. (1972). Origin and Evolution of Bilateral Symmetry in Flowers. Evolutionary Biology, 49-85. doi:10.1007/978-1-4757-0256-9_3Li, C., Potuschak, T., Colon-Carmona, A., Gutierrez, R. A., & Doerner, P. (2005). Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proceedings of the National Academy of Sciences, 102(36), 12978-12983. doi:10.1073/pnas.0504039102Li, M., Zhang, D., Gao, Q., Luo, Y., Zhang, H., Ma, B., … Xue, Y. (2019). Genome structure and evolution of Antirrhinum majus L. Nature Plants, 5(2), 174-183. doi:10.1038/s41477-018-0349-9Li, S. (2015). The Arabidopsis thaliana TCP transcription factors: A broadening horizon beyond development. Plant Signaling & Behavior, 10(7), e1044192. doi:10.1080/15592324.2015.1044192Li, S., Gutsche, N., & Zachgo, S. (2011). The ROXY1 C-Terminal L**LL Motif Is Essential for the Interaction with TGA Transcription Factors    . Plant Physiology, 157(4), 2056-2068. doi:10.1104/pp.111.185199Lin, Y.-F., Chen, Y.-Y., Hsiao, Y.-Y., Shen, C.-Y., Hsu, J.-L., Yeh, C.-M., … Tsai, W.-C. (2016). Genome-wide identification and characterization ofTCPgenes involved in ovule development ofPhalaenopsis equestris. Journal of Experimental Botany, 67(17), 5051-5066. doi:10.1093/jxb/erw273Da Luo, Carpenter, R., Copsey, L., Vincent, C., Clark, J., & Coen, E. (1999). Control of Organ Asymmetry in Flowers of Antirrhinum. Cell, 99(4), 367-376. doi:10.1016/s0092-8674(00)81523-8Luo, D., Carpenter, R., Vincent, C., Copsey, L., & Coen, E. (1996). Origin of floral asymmetry in Antirrhinum. Nature, 383(6603), 794-799. doi:10.1038/383794a0Madrigal, Y., Alzate, J. F., & Pabón-Mora, N. (2017). Evolution and Expression Patterns of TCP Genes in Asparagales. Frontiers in Plant Science, 8. doi:10.3389/fpls.2017.00009Martín-Trillo, M., & Cubas, P. (2010). TCP genes: a family snapshot ten years later. Trends in Plant Science, 15(1), 31-39. doi:10.1016/j.tplants.2009.11.003MillerMA PfeifferW SchwartzT.2010.Creating the CIPRES Science Gateway for inference of large phylogenetic trees. [WWW document] URLhttp://www.phylo.org[accessed 5 June 2020].Mondragón-Palomino, M., & Trontin, C. (2011). High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots. Annals of Botany, 107(9), 1533-1544. doi:10.1093/aob/mcr059Nath, U., Crawford, B. C. W., Carpenter, R., & Coen, E. (2003). Genetic Control of Surface Curvature. Science, 299(5611), 1404-1407. doi:10.1126/science.1079354Navaud, O., Dabos, P., Carnus, E., Tremousaygue, D., & Hervé, C. (2007). TCP Transcription Factors Predate the Emergence of Land Plants. Journal of Molecular Evolution, 65(1), 23-33. doi:10.1007/s00239-006-0174-zNguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2014). IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution, 32(1), 268-274. doi:10.1093/molbev/msu300Pabón-Mora, N., Suárez-Baron, H., Ambrose, B. A., & González, F. (2015). Flower Development and Perianth Identity Candidate Genes in the Basal Angiosperm Aristolochia fimbriata (Piperales: Aristolochiaceae). Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.01095Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C., & Weigel, D. (2003). Control of leaf morphogenesis by microRNAs. Nature, 425(6955), 257-263. doi:10.1038/nature01958Parapunova, 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). doi:10.1186/1471-2229-14-157Peréz-Mesa, P., Ortíz-Ramírez, C. I., González, F., Ferrándiz, C., & Pabón-Mora, N. (2020). Expression of gynoecium patterning transcription factors in Aristolochia fimbriata (Aristolochiaceae) and their contribution to gynostemium development. EvoDevo, 11(1). doi:10.1186/s13227-020-00149-8Preston, J. C., & Hileman, L. C. (2012). Parallel evolution of TCP and B-class genes in Commelinaceae flower bilateral symmetry. EvoDevo, 3(1), 6. doi:10.1186/2041-9139-3-6Preston, J. C., Kost, M. A., & Hileman, L. C. (2009). Conservation and diversification of the symmetry developmental program among close relatives of snapdragon with divergent floral morphologies. New Phytologist, 182(3), 751-762. doi:10.1111/j.1469-8137.2009.02794.xRambautA.2014.FigTree: tree figure drawing tool. [WWW document] URLhttp://tree.bio.ed.ac.uk/software/figtree/.Rudall, P. J., & Bateman, R. M. (2004). Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytologist, 162(1), 25-44. doi:10.1111/j.1469-8137.2004.01032.xSargent, R. D. (2004). Floral symmetry affects speciation rates in angiosperms. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(1539), 603-608. doi:10.1098/rspb.2003.2644Suárez-Baron, H., Alzate, J. F., González, F., Ambrose, B. A., & Pabón-Mora, N. (2019). Genetic mechanisms underlying perianth epidermal elaboration of Aristolochia ringens Vahl (Aristolochiaceae). Flora, 253, 56-66. doi:10.1016/j.flora.2019.03.004Suárez-Baron, H., Pérez-Mesa, P., Ambrose, B. A., González, F., & Pabón-Mora, N. (2016). Deep into the Aristolochia Flower: Expression of C, D, and E-Class Genes inAristolochia fimbriata(Aristolochiaceae). Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 328(1-2), 55-71. doi:10.1002/jez.b.22686Viola, I. L., Uberti Manassero, N. G., Ripoll, R., & Gonzalez, D. H. (2011). The Arabidopsis class I TCP transcription factor AtTCP11 is a developmental regulator with distinct DNA-binding properties due to the presence of a threonine residue at position 15 of the TCP domain. Biochemical Journal, 435(1), 143-155. doi:10.1042/bj20101019Wang, J., Wang, Y., & Luo, D. (2010). LjCYC Genes Constitute Floral Dorsoventral Asymmetry in Lotus japonicus. Journal of Integrative Plant Biology, 52(11), 959-970. doi:10.1111/j.1744-7909.2010.00926.xYuan, Z., Gao, S., Xue, D.-W., Luo, D., Li, L.-T., Ding, S.-Y., … Zhang, D.-B. (2008). RETARDED PALEA1 Controls Palea Development and Floral Zygomorphy in Rice  . Plant Physiology, 149(1), 235-244. doi:10.1104/pp.108.128231Zhang, W., Kramer, E. M., & Davis, C. C. (2010). Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proceedings of the National Academy of Sciences, 107(14), 6388-6393. doi:10.1073/pnas.0910155107Zhang, W., Steinmann, V. W., Nikolov, L., Kramer, E. M., & Davis, C. C. (2013). Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors. Frontiers in Plant Science, 4. doi:10.3389/fpls.2013.0030

    Identifying SARS-CoV-2 'memory' NK cells from COVID-19 convalescent donors for adoptive cell therapy

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    COVID-19 disease is the manifestation of syndrome coronavirus 2 (SARS-CoV-2) infection, which is causing a worldwide pandemic. This disease can lead to multiple and different symptoms, being lymphopenia associated with severity one of the most persistent. Natural killer cells (NK cells) are part of the innate immune system, being fighting against virus-infected cells one of their key roles. In this study, we determined the phenotype of NK cells after COVID-19 and the main characteristic of SARS-CoV-2-specific-like NK population in the blood of convalescent donors. CD57+ NKG2C+ phenotype in SARS-CoV-2 convalescent donors indicates the presence of 'memory'/activated NK cells as it has been shown for cytomegalovirus infections. Although the existence of this population is donor dependent, its expression may be crucial for the specific response against SARS-CoV-2, so that, it gives us a tool for selecting the best donors to produce off-the-shelf living drug for cell therapy to treat COVID-19 patients under the RELEASE clinical trial (NCT04578210)

    A large outbreak of COVID-19 linked to an end of term trip to Menorca (Spain) by secondary school students in summer 2021

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    Coronavirus SARS-CoV-2; COVID-19; 2019-nCov; Joves; BrotCoronavirus SARS-CoV-2; COVID-19; 2019-nCov; Jóvenes; BroteCoronavirus SARS-CoV-2; COVID-19; 2019-nCov; Youths; OutbreakBackground: An outbreak of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) occurred in young people from Catalonia (Spain) who travelled to Menorca (Spain) in summer 2021. This outbreak appeared when governments relaxed Covid-19 preventive measures: the mask usage and the opening of nightlife. It was related to a super-disseminating mass event: Sant Joan festivities in Ciutadella. The aim of this article is to describe an outbreak of COVID-19 in young people aged 17–19 years from Catalonia travelling to Menorca. Methods: This is an observational study of a COVID-19 outbreak. The study population comprised Catalonian youth aged 17–19 years who travelled to Menorca from 15 June to 10 July. Epidemiological descriptive indicators were obtained. Descriptive and geographical statistics were carried out. Bivariate Moran’s I test was used to identify spatial autocorrelation between the place of residence and deprivation. The outbreak control method was based on identifying and stopping chains of transmission by implementing the test-trace-isolate-quarantine (TTIQ) strategy. Results: We identified 515 confirmed cases infected in Menorca, 296 (57.5%) in girls and 219 (42.5%) in boys, with a total of 2,280 close contacts. Of them, 245 (10.7%) were confirmed as cases. The cases were diagnosed between 15 June and 10 July. None of the persons with confirmed infection died or required hospitalisation. The attack rate was 27.2%. There was an inverse relationship between deprivation and number of confirmed cases (p<0.005), there were clusters of confirmed cases in the most socioeconomic favoured areas. Discussion: The outbreak is related with young people from socioeconomic favoured areas who travelled to Menorca in summer 2021. Failure to comply with preventive measures in binge-drinking events and during holidays may have favoured SARS-CoV-2 transmission. The interauthority coordination and establishment of a clear line of leadership allowed continuous communication between institutions, which were key to managing this complex COVID-19 outbreak

    Q-SAPS?: què saben sobre salut pública a l’atenció primària?

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    Malalties; Declaració obligatòria; Brots epidèmicsEnfermedades; Declaración obligatoria; Brotes epidémicosDiseases; Mandatory declaration; Epidemic outbreaksEl treball d’aquesta comunitat de pràctica (CoP) pretén ajudar a detectar mancances de coneixement sobre la salut pública entre els professionals de l’atenció primària i elaborar un document de propostes per millorar el coneixement referit en aquest àmbit. Amb les següents propostes de valor: 1-Conèixer les funcions de cada actor en les malalties de declaració obligatòria (MDO), emergents i brots epidèmics. 2-Detectar mancances de coneixement i dificultats per a declarar. 3-Saber la utilitat de declarar MDO i brots epidèmics, ja que no és només un simple registre sinó que hi ha una actuació al darrere. 4-Conèixer les actuacions comunitàries que cal fer en cada malaltia per controlar-la, i brots epidèmics.El trabajo de esta comunidad de práctica (CoP) pretende ayudar a detectar carencias de conocimiento sobre la salud pública entre los profesionales de la atención primaria y elaborar un documento de propuestas para mejorar el conocimiento referido en este ámbito. Con las siguientes propuestas de valor: 1-Conocer las funciones de cada actor en las enfermedades de declaración obligatoria (MDO), emergentes y brotes epidémicos. 2-Detectar carencias de conocimiento y dificultades para declarar. 3-Saber la utilidad de declarar EDO y brotes epidémicos, ya que no es sólo un simple registro sino que hay una actuación detrás. 4-Conocer las actuaciones comunitarias a realizar en cada enfermedad para controlarla, y brotes epidémicos.The work of this community of practice (CoP) aims to help detect gaps in knowledge about public health among primary care professionals and prepare a document of proposals to improve the knowledge referred to in this area. With the following value propositions: 1-Know the functions of each actor in notifiable diseases, emerging diseases and epidemic outbreaks. 2-Detect knowledge gaps and difficulties in declaring. 3-Know the usefulness of declaring notifiable diseases and epidemic outbreaks, since it is not just a simple record but there is an action behind it. 4-Know the community actions to be carried out in each disease to control it, and epidemic outbreaks
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