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      Phyllotactic patterning of gerbera flower heads

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          Significance

          Flower heads, such as those of gerbera or sunflower, comprise hundreds of bracts and florets. They are organized into conspicuous spiral patterns with intriguing mathematical properties: For example, the numbers of left- and right-winding spirals are typically consecutive Fibonacci numbers. We examined auxin reporter lines of gerbera and combined diverse microscopy and modeling techniques to understand how these patterns develop. The critical process is the early patterning of bracts, which emerge in a specific order and guide the placement of the subsequent bracts and florets. This process, controlled by expansion and contraction of the organogenetic zone during head growth, is different from the extensively studied phyllotactic patterning in the model plants Arabidopsis and tomato.

          Abstract

          Phyllotaxis, the distribution of organs such as leaves and flowers on their support, is a key attribute of plant architecture. The geometric regularity of phyllotaxis has attracted multidisciplinary interest for centuries, resulting in an understanding of the patterns in the model plants Arabidopsis and tomato down to the molecular level. Nevertheless, the iconic example of phyllotaxis, the arrangement of individual florets into spirals in the heads of the daisy family of plants (Asteraceae), has not been fully explained. We integrate experimental data and computational models to explain phyllotaxis in Gerbera hybrida. We show that phyllotactic patterning in gerbera is governed by changes in the size of the morphogenetically active zone coordinated with the growth of the head. The dynamics of these changes divides the patterning process into three phases: the development of an approximately circular pattern with a Fibonacci number of primordia near the head rim, its gradual transition to a zigzag pattern, and the development of a spiral pattern that fills the head on the template of this zigzag pattern. Fibonacci spiral numbers arise due to the intercalary insertion and lateral displacement of incipient primordia in the first phase. Our results demonstrate the essential role of the growth and active zone dynamics in the patterning of flower heads.

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          Most cited references71

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          Fiji: an open-source platform for biological-image analysis.

          Fiji is a distribution of the popular open-source software ImageJ focused on biological-image analysis. Fiji uses modern software engineering practices to combine powerful software libraries with a broad range of scripting languages to enable rapid prototyping of image-processing algorithms. Fiji facilitates the transformation of new algorithms into ImageJ plugins that can be shared with end users through an integrated update system. We propose Fiji as a platform for productive collaboration between computer science and biology research communities.
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            Model for the regulation of Arabidopsis thaliana leaf margin development.

            Biological shapes are often produced by the iterative generation of repeated units. The mechanistic basis of such iteration is an area of intense investigation. Leaf development in the model plant Arabidopsis is one such example where the repeated generation of leaf margin protrusions, termed serrations, is a key feature of final shape. However, the regulatory logic underlying this process is unclear. Here, we use a combination of developmental genetics and computational modeling to show that serration development is the morphological read-out of a spatially distributed regulatory mechanism, which creates interspersed activity peaks of the growth-promoting hormone auxin and the cup-shaped cotyledon2 (CUC2) transcription factor. This mechanism operates at the growing leaf margin via a regulatory module consisting of two feedback loops working in concert. The first loop relates the transport of auxin to its own distribution, via polar membrane localization of the pinformed1 (PIN1) efflux transporter. This loop captures the potential of auxin to generate self-organizing patterns in diverse developmental contexts. In the second loop, CUC2 promotes the generation of PIN1-dependent auxin activity maxima while auxin represses CUC2 expression. This CUC2-dependent loop regulates activity of the conserved auxin efflux module in leaf margins to generate stable serration patterns. Conceptualizing leaf margin development via this mechanism also helps to explain how other developmental regulators influence leaf shape.
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              Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.

              Plants produce leaf and flower primordia from a specialized tissue called the shoot apical meristem (SAM). Genetic studies have identified a large number of genes that affect various aspects of primordium development including positioning, growth, and differentiation. So far, however, a detailed understanding of the spatio-temporal sequence of events leading to primordium development has not been established. We use confocal imaging of green fluorescent protein (GFP) reporter genes in living plants to monitor the expression patterns of multiple proteins and genes involved in flower primordial developmental processes. By monitoring the expression and polarity of PINFORMED1 (PIN1), the auxin efflux facilitator, and the expression of the auxin-responsive reporter DR5, we reveal stereotypical PIN1 polarity changes which, together with auxin induction experiments, suggest that cycles of auxin build-up and depletion accompany, and may direct, different stages of primordium development. Imaging of multiple GFP-protein fusions shows that these dynamics also correlate with the specification of primordial boundary domains, organ polarity axes, and the sites of floral meristem initiation. These results provide new insight into auxin transport dynamics during primordial positioning and suggest a role for auxin transport in influencing primordial cell type.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                30 March 2021
                26 March 2021
                26 March 2021
                : 118
                : 13
                : e2016304118
                Affiliations
                [1] aDepartment of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki , 00014 Helsinki, Finland;
                [2] bDepartment of Computer Science, University of Calgary , Calgary, AB T2N 1N4, Canada
                Author notes
                2To whom correspondence may be addressed. Email: pwp@ 123456ucalgary.ca or paula.elomaa@ 123456helsinki.fi .

                Edited by Dominique C. Bergmann, Stanford University, Stanford, CA, and approved February 22, 2021 (received for review August 2, 2020)

                Author contributions: T.Z., P.E., and P.P. designed the project; T.Z., T.H.T., P.E., and P.P. designed the experiments; S.K.B. and T.H.T. cloned the DR5 construct; F.W. cloned the GhCLV3 construct and conducted the in situ hybridization; T.Z. carried out all other experiments; M.C., A.O., and P.P. constructed computational and mathematical models; T.Z., M.C., P.E., and P.P. analyzed experimental data and modeling results; and T.Z., M.C., A.O., P.E., and P.P. wrote the paper.

                1T.Z. and M.C. contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-5189-3289
                http://orcid.org/0000-0003-2138-6865
                http://orcid.org/0000-0002-3812-7213
                http://orcid.org/0000-0001-6512-0810
                http://orcid.org/0000-0002-1338-7086
                Article
                202016304
                10.1073/pnas.2016304118
                8020676
                33771923
                6482ab6a-896d-47fc-b526-20a9b9047f98
                Copyright © 2021 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 11
                Funding
                Funded by: Academy of Finland | Biotieteiden ja Ympäristön Tutkimuksen Toimikunta (Forskningsrådet för Biovetenskap och Miljö) 501100005876
                Award ID: 1310318
                Award Recipient : Paula Elomaa
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: 2019-06279
                Award Recipient : Przemyslaw Prusinkiewicz
                Funded by: Plant Phenotyping and Imaging Research Centre / Canada First Research Excellence Fund
                Award ID: N/A
                Award Recipient : Teng Zhang Award Recipient : Mikolaj Cieslak Award Recipient : Przemyslaw Prusinkiewicz
                Funded by: Helsinki University Doctoral Program
                Award ID: N/A
                Award Recipient : Teng Zhang Award Recipient : Mikolaj Cieslak Award Recipient : Przemyslaw Prusinkiewicz
                Funded by: Finnish Cultural Foundation | Etelä-Pohjanmaan Rahasto (South Ostrobothnia Regional Fund) 501100005427
                Award ID: N/A
                Award Recipient : Teng Zhang
                Categories
                428
                Biological Sciences
                Plant Biology

                phyllotaxis,numerical canalization,flower head development,auxin

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