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      Spiral phyllotaxis underlies constrained variation in Anemone (Ranunculaceae) tepal arrangement

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          Abstract

          Stabilization and variation of floral structures are indispensable for plant reproduction and evolution; however, the developmental mechanism regulating their structural robustness is largely unknown. To investigate this mechanism, we examined positional arrangement (aestivation) of excessively produced perianth organs (tepals) of six- and seven-tepaled (lobed) flowers in six Anemone species (Ranunculaceae). We found that the tepal arrangement that occurred in nature varied intraspecifically between spiral and whorled arrangements. Moreover, among the studied species, variation was commonly limited to three types, including whorls, despite five geometrically possible arrangements in six-tepaled flowers and two types among six possibilities in seven-tepaled flowers. A spiral arrangement, on the other hand, was unique to five-tepaled flowers. A spiral phyllotaxis model with stochasticity on initiating excessive primordia accounted for these limited variations in arrangement in cases when the divergence angle between preexisting primordia was less than 144°. Moreover, interspecific differences in the frequency of the observed arrangements were explained by the change of model parameters that represent meristematic growth and differential organ growth. These findings suggest that the phyllotaxis parameters are responsible for not only intraspecific stability but interspecific difference of floral structure. Decreasing arrangements from six-tepaled to seven-tepaled Anemone flowers demonstrate that the stabilization occurs as development proceeds to increase the component (organ) number, in contrast from the intuition that the variation will be larger due to increasing number of possible states (arrangements).

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          Most cited references26

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          The ancestral flower of angiosperms and its early diversification

          Recent advances in molecular phylogenetics and a series of important palaeobotanical discoveries have revolutionized our understanding of angiosperm diversification. Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. We reconstruct the ancestral angiosperm flower as bisexual and radially symmetric, with more than two whorls of three separate perianth organs each (undifferentiated tepals), more than two whorls of three separate stamens each, and more than five spirally arranged separate carpels. Although uncertainty remains for some of the characters, our reconstruction allows us to propose a new plausible scenario for the early diversification of flowers, leading to new testable hypotheses for future research on angiosperms.
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            Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis.

            In plants, the arrangement of organs along the stem (phyllotaxy) follows a predictable pattern. Recent studies have shown that primordium position at the meristem is governed by local auxin gradients, but little is known about the subsequent events leading to the phyllotaxy along the mature stem. We show here that plants expressing a miR164-resistant CUP-SHAPED COTYLEDON2 (CUC2) gene have an abnormal phyllotactic pattern in the fully grown stem, despite the pattern of organ initiation by the meristem being normal. This implies that abnormal phyllotaxy is generated during stem growth. These plants ectopically express CUC2 in the stem, suggesting that the proper timing of CUC2 expression is required to maintain the pattern initiated in the meristem. Furthermore, by carefully comparing the phyllotaxy in the meristem and along the mature inflorescence in wild types, we show that such deviation also occurs during wild-type development, although to a smaller extent. We therefore suggest that the phyllotactic pattern in a fully grown stem results not only from the organogenetic activity of the meristem, but also from the subsequent growth pattern during stem development.
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              Flexibility in the structure of spiral flowers and its underlying mechanisms.

              Spiral flowers usually bear a variable number of organs, suggestive of the flexibility in structure. The mechanisms underlying the flexibility, however, remain unclear. Here we show that in Nigella damascena, a species with spiral flowers, different types of floral organs show different ranges of variation in number. We also show that the total number of organs per flower is largely dependent on the initial size of the floral meristem, whereas the respective numbers of different types of floral organs are determined by the functional domains of corresponding genetic programmes. By conducting extensive expression and functional studies, we further elucidate the genetic programmes that specify the identities of different types of floral organs. Notably, the AGL6-lineage member NdAGL6, rather than the AP1-lineage members NdFL1/2, is an A-function gene, whereas petaloidy of sepals is not controlled by AP3- or PI-lineage members. Moreover, owing to the formation of a regulatory network, some floral organ identity genes also regulate the boundaries between different types of floral organs. On the basis of these results, we propose that the floral organ identity determination programme is highly dynamic and shows considerable flexibility. Transitions from spiral to whorled flowers, therefore, may be explained by evolution of the mechanisms that reduce the flexibility.
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                Author and article information

                Contributors
                kitazawa@celas.osaka-u.ac.jp
                fujimoto@bio.sci.osaka-u.ac.jp
                Journal
                J Plant Res
                J. Plant Res
                Journal of Plant Research
                Springer Japan (Tokyo )
                0918-9440
                1618-0860
                27 March 2018
                27 March 2018
                2018
                : 131
                : 3
                : 459-468
                Affiliations
                [1 ]ISNI 0000 0004 0373 3971, GRID grid.136593.b, Center for Education in Liberal Arts and Sciences, , Osaka University, ; Toyonaka, Osaka Japan
                [2 ]ISNI 0000 0004 0373 3971, GRID grid.136593.b, Department of Biological Sciences, Graduate School of Science, , Osaka University, ; Toyonaka, Osaka Japan
                Article
                1025
                10.1007/s10265-018-1025-x
                5916976
                29589193
                83e20927-7ea2-4cf3-80a3-6eb89edf6f69
                © The Author(s) 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 10 November 2017
                : 26 February 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: Grants-in-Aid for Scientific Research 16H01241, 17
                Categories
                JPR Symposium
                Custom metadata
                © The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

                Plant science & Botany
                floral organ,variation,floral development,mathematical model,phyllotaxis,ranunculaceae

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