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      The Times They Are A-Changin’: Heterochrony in Plant Development and Evolution

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          Abstract

          Alterations in the timing of developmental programs during evolution, that lead to changes in the shape, or size of organs, are known as heterochrony. Heterochrony has been widely studied in animals, but has often been neglected in plants. During plant evolution, heterochronic shifts have played a key role in the origin and diversification of leaves, roots, flowers, and fruits. Heterochrony that results in a juvenile or simpler outcome is known as paedomorphosis, while an adult or more complex outcome is called peramorphosis. Mechanisms that alter developmental timing at the cellular level affect cell proliferation or differentiation, while those acting at the tissue or organismal level change endogenous aging pathways, morphogen signaling, and metabolism. We believe that wider consideration of heterochrony in the context of evolution will contribute to a better understanding of plant development.

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          Most cited references78

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          miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana.

          The FT gene integrates several external and endogenous cues controlling flowering, including information on day length. A complex of the mobile FT protein and the bZIP transcription factor FD in turn has a central role in activating genes that execute the switch from vegetative to reproductive development. Here we reveal that microRNA156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes not only act downstream of FT/FD, but also define a separate endogenous flowering pathway. High levels of miR156 in young plants prevent precocious flowering. A subsequent day length-independent decline in miR156 abundance provides a permissive environment for flowering and is paralleled by a rise in SPL levels. At the shoot apex, FT/FD and SPLs converge on an overlapping set of targets, with SPLs directly activating flower-promoting MADS box genes, providing a molecular substrate for both the redundant activities and the feed-forward action of the miR156/SPL and FT/FD modules in flowering control.
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            Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3.

            SPL3, SPL4 and SPL5 (SPL3/4/5) are closely related members of the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE family of transcription factors in Arabidopsis, and have a target site for the microRNA miR156 in their 3' UTR. The phenotype of Arabidopsis plants constitutively expressing miR156-sensitive and miR156-insensitive forms of SPL3/4/5 revealed that all three genes promote vegetative phase change and flowering, and are strongly repressed by miR156. Constitutive expression of miR156a prolonged the expression of juvenile vegetative traits and delayed flowering. This phenotype was largely corrected by constitutive expression of a miR156-insensitive form of SPL3. The juvenile-to-adult transition is accompanied by a decrease in the level of miR156 and an increase in the abundance of SPL3 mRNA. The complementary effect of hasty on the miR156 and SPL3 transcripts, as well as the miR156-dependent temporal expression pattern of a 35S::GUS-SPL3 transgene, suggest that the decrease in miR156 is responsible for the increase in SPL3 expression during this transition. SPL3 mRNA is elevated by mutations in ZIPPY/AGO7, RNA DEPENDENT RNA POLYMERASE 6 (RDR6) and SUPPRESSOR OF GENE SILENCING 3 (SGS3), indicating that it is directly or indirectly regulated by RNAi. However, our results indicate that RNAi does not contribute to the temporal expression pattern of this gene. We conclude that vegetative phase change in Arabidopsis is regulated by an increase in the expression of SPL3 and probably also SPL4 and SPL5, and that this increase is a consequence of a decrease in the level of miR156.
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              Size and shape in ontogeny and phylogeny

              We present a quantitative method for describing how heterochronic changes in ontogeny relate to phyletic trends. This is a step towards creating a unified view of developmental biology and evolutionary ecology in the study of morphological evolution. Using this representation, we obtain a greatly simplified and logical scheme of classification. We believe that this scheme will be particularly useful in studying the data of paleontology and comparative morphology and in the analysis of processes leading to adaptive radiation. We illustrate this scheme by examples drawn from the literature and our own work.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                18 September 2018
                2018
                : 9
                : 1349
                Affiliations
                Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), Unidad de Genómica Avanzada, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN) , Guanajuato, Mexico
                Author notes

                Edited by: Natalia Pabón-Mora, Universidad de Antioquía, Colombia

                Reviewed by: Jianfei Zhao, University of Pennsylvania, United States; Jill Christine Preston, The University of Vermont, United States

                *Correspondence: Manuel Buendía-Monreal, manuel.buendia@ 123456cinvestav.mx

                This article was submitted to Plant Evolution and Development, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01349
                6157392
                30283473
                678e953b-fb44-4518-a3d2-d153e82da9c9
                Copyright © 2018 Buendía-Monreal and Gillmor.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 June 2018
                : 27 August 2018
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 90, Pages: 8, Words: 0
                Funding
                Funded by: Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional 10.13039/501100008688
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                heterochrony,developmental timing,plant development,plant evolution,cell cycle,mir156

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