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      Comparative analysis of floral transition and floral organ formation in two contrasting species: Disocactus speciosus and D. eichlamii (Cactaceae)

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          Abstract

          Key message

          Contrasting morphologies in Disocactus are the result of differential development of the vegetative and floral tissue where intercalary growth is involved, resulting in a complex structure, the floral axis.

          Abstract

          Species from the Cactaceae bear adaptations related with their growth in environments under hydric stress. These adaptations have translated into the reduction and modification of various structures such as leaves, stems, lateral branches, roots and the structuring of flowers in a so-called flower-shoot. While cacti flowers and fruits have a consistent structure with showy hermaphrodite or unisexual flowers that produce a fruit called cactidium, the developmental dynamics of vegetative and reproductive tissues comprising the reproductive unit have only been inferred through the analysis of pre-anthetic buds. Here we present a comparative analysis of two developmental series covering the early stages of flower formation and organ differentiation in Disocactus speciosus and Disocactus eichlamii, which have contrasting floral morphologies. We observe that within the areole, a shoot apical meristem commences to grow upward, producing lateral leaves with a spiral arrangement, rapidly transitioning to a floral meristem. The floral meristem produces tepal primordia and a staminal ring meristem from which numerous or few stamens develop in a centrifugal manner in D. speciosus and D. eichlamii, respectively. Also, the inferior ovary derives from the floral meristem flattening and an upward growth of the surrounding tissue of the underlying stem, producing the pericarpel. This structure is novel to cacti and lacks a clear anatomical delimitation with the carpel wall. Here, we present a first study that documents the early processes taking place during initial meristem determination related to pericarpel development and early floral organ formation in cacti until the establishment of mature floral organs.

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          Contemporaneous and recent radiations of the world's major succulent plant lineages.

          The cacti are one of the most celebrated radiations of succulent plants. There has been much speculation about their age, but progress in dating cactus origins has been hindered by the lack of fossil data for cacti or their close relatives. Using a hybrid phylogenomic approach, we estimated that the cactus lineage diverged from its closest relatives ≈35 million years ago (Ma). However, major diversification events in cacti were more recent, with most species-rich clades originating in the late Miocene, ≈10-5 Ma. Diversification rates of several cactus lineages rival other estimates of extremely rapid speciation in plants. Major cactus radiations were contemporaneous with those of South African ice plants and North American agaves, revealing a simultaneous diversification of several of the world's major succulent plant lineages across multiple continents. This short geological time period also harbored the majority of origins of C(4) photosynthesis and the global rise of C(4) grasslands. A global expansion of arid environments during this time could have provided new ecological opportunity for both succulent and C(4) plant syndromes. Alternatively, recent work has identified a substantial decline in atmospheric CO(2) ≈15-8 Ma, which would have strongly favored C(4) evolution and expansion of C(4)-dominated grasslands. Lowered atmospheric CO(2) would also substantially exacerbate plant water stress in marginally arid environments, providing preadapted succulent plants with a sharp advantage in a broader set of ecological conditions and promoting their rapid diversification across the landscape.
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            Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences.

            To study the inter- and infrafamilial phylogenetic relationships in the order Caryophyllales sensu lato (s.l.), ∼930 base pairs of the matK plastid gene have been sequenced and analyzed for 127 taxa. In addition, these sequences have been combined with the rbcL plastid gene for 53 taxa and with the rbcL and atpB plastid genes as well as the nuclear 18S rDNA for 26 taxa to provide increased support for deeper branches. The red pigments of Corbichonia, Lophiocarpus, and Sarcobatus have been tested and shown to belong to the betacyanin class of compounds. Most taxa of the order are clearly grouped into two main clades (i.e., "core" and "noncore" Caryophyllales) which are, in turn, divided into well-defined subunits. Phytolaccaceae and Molluginaceae are polyphyletic, and Portulacaceae are paraphyletic, whereas Agdestidaceae, Barbeuiaceae, Petiveriaceae, and Sarcobataceae should be given familial recognition. Two additional lineages are potentially appropriate to be elevated to the family level in the future: the genera Lophiocarpus and Corbichonia form a well-supported clade on the basis of molecular and chemical evidence, and Limeum appears to be separated from other Molluginaceae based on both molecular and ultrastructural data.
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              ETTIN patterns the Arabidopsis floral meristem and reproductive organs.

              ettin (ett) mutations have pleiotropic effects on Arabidopsis flower development, causing increases in perianth organ number, decreases in stamen number and anther formation, and apical-basal patterning defects in the gynoecium. The ETTIN gene was cloned and encodes a protein with homology to DNA binding proteins which bind to auxin response elements. ETT transcript is expressed throughout stage 1 floral meristems and subsequently resolves to a complex pattern within petal, stamen and carpel primordia. The data suggest that ETT functions to impart regional identity in floral meristems that affects perianth organ number spacing, stamen formation, and regional differentiation in stamens and the gynoecium. During stage 5, ETT expression appears in a ring at the top of the floral meristem before morphological appearance of the gynoecium, consistent with the proposal that ETT is involved in prepatterning apical and basal boundaries in the gynoecium primordium. Double mutant analyses and expression studies show that although ETT transcriptional activation occurs independently of the meristem and organ identity genes LEAFY, APETELA1, APETELA2 and AGAMOUS, the functioning of these genes is necessary for ETT activity. Double mutant analyses also demonstrate that ETT functions independently of the 'b' class genes APETELA3 and PISTILLATA. Lastly, double mutant analyses suggest that ETT control of floral organ number acts independently of CLAVATA loci and redundantly with PERIANTHIA.
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                Author and article information

                Contributors
                isaurarosasr@gmail.com
                Journal
                Plant Reprod
                Plant Reprod
                Plant Reproduction
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                2194-7953
                2194-7961
                9 January 2024
                9 January 2024
                2024
                : 37
                : 2
                : 179-200
                Affiliations
                [1 ]Instituto de Biología, Jardín Botánico, Universidad Nacional Autónoma de México, ( https://ror.org/01tmp8f25) C.P.04510 Mexico City, Mexico
                [2 ]GRID grid.7220.7, ISNI 0000 0001 2157 0393, Departamento de Producción Agrícola y Animal, , Universidad Autónoma Metropolitana-Xochimilco, ; C.P.04510 Mexico City, Mexico
                [3 ]Centro de Ciencias de la Complejidad (C3), Universidad Nacional Autónoma de México, ( https://ror.org/01tmp8f25) C.P.04960 Mexico City, Mexico
                [4 ]Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio D, 1° Piso, Circuito de Posgrados, Ciudad Universitaria, Coyoacán, Mexico City, C.P. 04510 Mexico
                [5 ]Present Address: Center for Genomics and Systems Biology, New York University, ( https://ror.org/0190ak572) 12 Waverly Pl, New York, NY 10003 USA
                Author notes

                Communicated by Natalia Pabón-Mora.

                Author information
                https://orcid.org/0009-0007-0607-1263
                https://orcid.org/0000-0001-7349-0096
                https://orcid.org/0000-0001-8905-9102
                https://orcid.org/0000-0002-7674-7050
                http://orcid.org/0000-0001-5397-0666
                Article
                494
                10.1007/s00497-023-00494-3
                11180016
                38193922
                3f2cae7a-23f9-4108-bf2c-ebd90266a4da
                © The Author(s) 2024

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 30 May 2023
                : 14 December 2023
                Categories
                Original Article
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                © Springer-Verlag GmbH Germany, part of Springer Nature 2024

                epiphytic cacti,floral anatomy,hylocereeae,pericarpel,ring meristem

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