127 research outputs found
B-Function Expression in the Flower Center Underlies the Homeotic Phenotype of Lacandonia schismatica (Triuridaceae)
Spontaneous homeotic transformations have been described in natural populations of both plants and animals, but little is known about the molecular-genetic mechanisms underlying these processes in plants. In the ABC model of floral organ identity in Arabidopsis thaliana, the B- and C-functions are necessary for stamen morphogenesis, and C alone is required for carpel identity. We provide ABC model-based molecular-genetic evidence that explains the unique inside-out homeotic floral organ arrangement of the monocotyledonous mycoheterotroph species Lacandonia schismatica (Triuridaceae) from Mexico. Whereas a quarter million flowering plant species bear central carpels surrounded by stamens, L. schismatica stamens occur in the center of the flower and are surrounded by carpels. The simplest explanation for this is that the B-function is displaced toward the flower center. Our analyses of the spatio-temporal pattern of B- and C-function gene expression are consistent with this hypothesis. The hypothesis is further supported by conservation between the B-function genes of L. schismatica and Arabidopsis, as the former are able to rescue stamens in Arabidopsis transgenic complementation lines, and Ls-AP3 and Ls-PI are able to interact with each other and with the corresponding Arabidopsis B-function proteins in yeast. Thus, relatively simple molecular modifications may underlie important morphological shifts in natural populations of extant plant taxa
Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia
[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
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. 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. 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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). 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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
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Duplication and Diversification of REPLUMLESS – A Case Study in the Papaveraceae
There is a vast amount of fruit morphological diversity in terms of their texture, the number of carpels, if those carpels are fused or not and how fruits open to disperse the seeds. Arabidopsis thaliana, a model eudicot, has a dry bicarpellate silique, when the fruit matures, the two valves fall apart through the dehiscence zone leaving the seeds attached to the remaining medial tissue, called the replum. Proper replum development in A. thaliana is mediated by REPLUMLESS (RPL), a TALE Homeodomain protein. RPL represses the valve margin genetic program and the downstream dehiscence zone formation in the medial tissue of the siliques and RPL orthologs have conserved roles across the Brassicaceae eudicots. A RPL homolog, qSH1, has been studied in rice, a monocot, and plays a role in fruit shedding making it difficult to predict functional evolution of this gene lineage across angiosperms. Although RPL orthologs have been identified across all angiosperms, expression and functional analyses are scarce. In order to fill the phylogenetic gap between the Brassicaceae and monocots we have characterized the expression patterns of RPL homologs in two poppies with different fruit types, Bocconia frutescens with operculate valvate dehiscence and a persistent medial tissue, similar to a replum, and Papaver somniferum, a poppy with persistent medial tissue in between the multicarpellate gynoecia. We found that RPL homologs in Papaveraceae have broad expression patterns during plant development; in the shoot apical meristem, during flowering transition and in many floral organs, especially the carpels. These patterns are similar to those of RPL in A. thaliana. However, our results suggest that RPL does not have conserved roles in the maintenance of medial persistent tissues of fruits but may be involved with establishing the putative dehiscence zone in dry poppy fruits
Evolution of Class IITCPgenes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia
[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-
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